Jiarong Cai

Wei Zhang

Liguang Xu

Changlong Hao

Wei Ma

Maozhong Sun

Xiaoling Wu

Xian Qin

Mariano Felippe

Colombari

André Farias De Moura

Jiahui Xu

Mariana Cristina Silva

Evaldo Batista Carneiro-Neto

Weverso Rodrigu Gomes

Renaud A L Vallé

Ernesto Chaves Perei

Xiaogang Liu

Chuanlai Xu

Rafal Klajn
email: rafal.klajn@weizmann.ac.il

Nicholas A Kotov
email: kotov@umich.edu

Hua Kuang
email: kuangh@jiangnan.edu.cn

Polarization-sensitive optoionic membranes from chiral plasmonic nanoparticles

Keywords: Nature Research reporting summaries, source data, extended data, supplementary information

Optoelectronic effects differentiating absorption of right and left circularly polarized photons in thin films of chiral materials are typically prohibitively small for their direct photocurrent observation. Chiral metasurfaces increase the electronic sensitivity to circular polarization, but their out-of-plane architecture entails manufacturing and performance trade-offs. Here, we show that nanoporous thin films of chiral nanoparticles enable high sensitivity to circular polarization due to light-induced polarization-dependent ion accumulation at nanoparticle interfaces. Self-assembled multilayers of gold nanoparticles modified with l-phenylalanine generate a photocurrent under right-handed circularly polarized light as high as 2.41 times higher than under left-handed circularly polarized light. The strong plasmonic coupling between the multiple nanoparticles producing planar chiroplasmonic modes facilitates the ejection of electrons, whose entrapment at the membrane-electrolyte interface is promoted by a thick layer of enantiopure phenylalanine. Demonstrated detection of light ellipticity with equal sensitivity at all incident angles mimics phenomenological aspects of polarization vision in marine animals. The simplicity of self-assembly and sensitivity of polarization detection found in optoionic membranes opens the door to a family of miniaturized fluidic devices for chiral photonics.

I

nteractions between circularly polarized light (CPL) and matter hold promise for many emerging technologies [START_REF] Mciver | Control over topological insulator photocurrents with light polarization[END_REF][START_REF] Hatano | Transverse photovoltage induced by circularly polarized light[END_REF][START_REF] Bai | Manipulating photoinduced voltage in metasurface with circularly polarized light[END_REF] . However, for optoelectronic thin films of chiral organic materials or inorganic nanoparticles (NPs), the difference in light absorption between left-(L) and right-(R) handed photons typically does not exceed a fraction of a percent, which is prohibitively small for polarization-sensitive photocurrent devices [START_REF] Yokoyama | Giant circular dichroism in individual carbon nanotubes induced by extrinsic chirality[END_REF] . Metamaterials and metasurfaces with nanoscale geometries matching helical field distribution of CPL increase the sensitivity of light-matter interactions to circular polarization [START_REF] Ma | Direct optical detection of Weyl fermion chirality in a topological semimetal[END_REF][START_REF] Yang | Circularly polarized light detection by a chiral organic semiconductor transistor[END_REF][START_REF] Li | Circularly polarized light detection with hot electrons in chiral plasmonic metamaterials[END_REF][START_REF] Wang | Observation of Floquet-Bloch states on the surface of a topological insulator[END_REF][START_REF] Higuchi | Light-field-driven currents in graphene[END_REF] . However, the out-of-plane engineering of these metastructures results in both performance and manufacturing trade-offs, hindering the conversion of optical absorption into electron transport and imparting strong angular dependence [START_REF] Yokoyama | Giant circular dichroism in individual carbon nanotubes induced by extrinsic chirality[END_REF] .

Similar to the coupling of CPL with electron clouds in molecules, coupling of spin-angular momentum of photons with the transport of ion clouds in electroactive nanoscale pores can lead to optoelectronic effects [START_REF] Aca | Biomimetic potassium-selective nanopores[END_REF][START_REF] Cheng | Low-voltage electrostatic modulation of ion diffusion through layered graphene-based nanoporous membranes[END_REF][START_REF] Wang | Temperature-sensitive artificial channels through pillar[5] arene-based host-guest interactions[END_REF][START_REF] Zhang | Improved osmotic energy conversion in heterogeneous membrane boosted by three-dimensional hydrogel interface[END_REF][START_REF] Schroeder | An electric-eel-inspired soft power source from stacked hydrogels[END_REF][START_REF] Sun | A biomimetic chiral-driven ionic gate constructed by pillar[6] arene-based host-guest systems[END_REF] . Of particular interest are bioinspired light-sensitive nanoscale channels [START_REF] Sun | A light-regulated host-guest-based nanochannel system inspired by channelrhodopsins protein[END_REF][START_REF] Xie | Photocurrent generation based on a light-driven proton pump in an artificial liquid membrane[END_REF][START_REF] Mourot | Rapid optical control of nociception with an ion-channel photoswitch[END_REF][START_REF] White | Observation of photovoltaic action from photoacid-modified Nafion due to light-driven ion transport[END_REF][START_REF] Xiao | Artificial light-driven ion pump for photoelectric energy conversion[END_REF] , with some of them replicating membranes of retinal cells [START_REF] Palmer | A highly reflective biogenic photonic material from core-shell birefringent nanoparticles[END_REF][START_REF] Roberts | A biological quarter-wave retarder with excellent achromaticity in the visible wavelength region[END_REF][START_REF] Chiou | Circular polarization vision in a stomatopod crustacean[END_REF] , but photocurrents or photovoltages generated across them are not known to be CPL dependent [START_REF] Tang | Photo-driven active ion transport through a Janus microporous membrane[END_REF][START_REF] Yang | Photo-induced ultrafast active ion transport through graphene oxide membranes[END_REF][START_REF] Xiao | Photo-driven ion transport for a photodetector based on an asymmetric carbon nitride nanotube membrane[END_REF] . Here, we show that the optoionic phenomena in thin nanoscale membranes from chiral gold NPs lead to unexpectedly high sensitivity to circular polarization of incident photons. When NPs in the self-assembled membranes (nanofilms) are decorated by l-phenylalanine (Phe), the photoinduced current (photocurrent) across the layer under right-handed circularly polarized (RCP) illumination is 1.47, 1.87, 2.20 and 2.41 times that under left-handed circularly polarized (LCP) illumination for monolayer (1L), three-layer (3L), five-layer (5L) and ten-layer (10L) nanofilms, respectively (Fig. 1a). Experimental and computational studies show that polarization-dependent transduction of CPL incident onto the multilayer NP membranes into photocurrent across thin films of chiral NPs originates from the light-driven ejection of electrons facilitated by the strong plasmonic modes coupled within the plane of the nanofilms. The thick surface layer of enantiopure Phe ligands on the NP surface extends the lifetime of the ejected electrons, while the photoinduced charge accumulated at the interfaces causes reorganization of the ionic atmosphere in the nanoscale channels. These optoionic effects can be utilized in a wide range of microfabricated fluidic devices.

Articles

NaTure NaNOTeCHNOlOgy

Results and discussion

Chiral nanomembranes. l-Phe-and d-Phe-modified spherical Au NPs, 35 nm in diameter, were assembled at a liquid-liquid interface to form NP monolayers [START_REF] Edel | Fundamentals and applications of self-assembled plasmonic nanoparticles at interfaces[END_REF][START_REF] Kotov | Monoparticulate layer and Langmuir-Blodgett-type multiparticulate layers of size-quantized cadmium sulfide clusters: a colloid-chemical approach to superlattice construction[END_REF][START_REF] Udayabhaskararao | Tunable porous nanoallotropes prepared by post-assembly etching of binary nanoparticle superlattices[END_REF] , which were subsequently transferred onto anodized aluminium oxide (AAO) or glass slides for electrochemical or optical measurements using the Langmuir-Blodgett technique. The surfaces of the NP monolayers were uniform over an area of at least several square centimetres and displayed a distinct metallic lustre. Scanning electron microscopy (SEM) and atomic force microscopy (AFM) images of the cross-sections and surfaces of all nanofilms showed densely packed NPs, with nanoscale channels formed between them (Fig. 1b and Supplementary Fig. 1).

The circular dichroism (CD) spectra of l-Phe-and d-Phe-modified NP films displayed amplitudes approaching 350 mdeg at a wavelength of 762 nm (Fig. 1f), whereas nanofilms of Au NPs carrying achiral citrate (Cit) or dl-Phe ligands (that is, a racemic 1:1 mixture of l-and d-Phe) showed near-zero CD spectra (Supplementary Fig. 2). The strong chiroptical activity of these nanofilms is attributed to the coupling of the molecular-scale chirality of Phe and the surface plasmon modes of metallic NPs [START_REF] Knoppe | Chirality in thiolate-protected gold clusters[END_REF][START_REF] Zhang | Unraveling the origin of chirality from plasmonic nanoparticle-protein complexes[END_REF][START_REF] Chen | Nanoparticle superstructures made by polymerase chain reaction: collective interactions of nanoparticles and a new principle for chiral materials[END_REF] in the highly polarizable gold nanofilms [START_REF] Ma | Chiral inorganic nanostructures[END_REF][START_REF] Ben-Moshe | Chirality and chiroptical effects in inorganic nanocrystal systems with plasmon and exciton resonances[END_REF] . Note also that modes localized in the gaps in the planar arrays of plasmonic particles are further enhanced by the short-range order observed for the nanofilms [START_REF] Ebbesen | Extraordinary optical transmission through sub-wavelength hole arrays[END_REF][START_REF] Zhao | Solvated electrons on metal oxide surfaces[END_REF][START_REF] Matricardi | Gold nanoparticle plasmonic superlattices as surface-enhanced Raman spectroscopy substrates[END_REF][START_REF] Wang | Manipulating light-matter interactions in plasmonic nanoparticle lattices[END_REF] . Taking the nanofilm model based on experimental AFM imaging, the chiroplasmonic lattice modes can be visualized by electrodynamic and finite-difference time-domain (FDTD) simulations (Fig. 1c,d). The FDTD-calculated CD spectrum matches nearly perfectly with the experimental data (Fig. 1g), verifying the origin of strong CD bands and the optoionic effects. The simulations also show that these modes have distinct wave-guided behaviour [START_REF] Mueller | Deep strong light-matter coupling in plasmonic nanoparticle crystals[END_REF] propagating along their surface (Fig. 1e). Importantly, such modes concentrate the field and optical energy exactly where the density of the particle-electrolyte interface is the highest, facilitating the coupling of photonic and ionic processes in the electric double layers around the nanoparticles, while reducing the far-field optical scattering along the direction normal to the nanofilm surface.

Photocurrent generation. The photocurrent, I, was measured for monolayers and multilayers of NPs illuminated by 808 nm light (10 mW cm -2 ) over periods of 60 s. The nanofilms were deposited on AAO supports placed between two compartments filled with an aqueous electrolyte (Fig. 1a). Photocurrent I(t) curves and maximal amplitudes (denoted as I || , I L and I R, respectively) were recorded for linearly polarized (LP), LCP and RCP light. The nanofilms from l-Phe -NPs displayed a photocurrent of I R = 10.04 ± 1.25 nA under RCP irradiation, that is, considerably larger than that under LCP illumination; I L = 6.82 ± 1.14 nA. Nanofilms from d-Phe-NPs exhibited I L = 10.35 ± 1.08 nA and I R = 6.87 ± 0.95 nA under LCP and RCP, respectively, displaying a distinct mirror-symmetrical relationship between I and the chirality of Phe (Fig. 1h,i). Concurrently [START_REF] Xie | Photocurrent generation based on a light-driven proton pump in an artificial liquid membrane[END_REF] , the photovoltage-time curves featured a similar change trend and mirror symmetry relationship with the photocurrent (Fig. 1j,k). In control experiments, an AAO membrane without the nanofilm or under other conditions (for example, nanofilms of Cit-NPs or dl-Phe-NPs) displayed little or no change in current across the membrane (Supplementary Fig. 3). No evidence of physical erosion or chemical deterioration of the nanofilms in the electrolyte solution with and without light was observed (Supplementary Fig. 4).

By analogy to CD spectroscopy, ΔI L-R = I L -I R can be used to characterize the polarization dependence of the photocurrent on nanofilm structure and other factors. Illumination at 808 nm was used in most experiments because it produced the highest I and ΔI L-R values (Fig. 2a and Supplementary Fig. 5). Nanofilms of 35 nm Au NPs displayed higher ΔI L-R values than NPs of other sizes (Fig. 2b and Supplementary Fig. 6). We also tested the illumination intensities from 1 to 20 mW cm -2 (Fig. 2c and Supplementary Fig. 7) and illumination times from 0 to 60 s (Fig. 2d and Supplementary Fig. 8); ΔI L-R reached a maximum of 3.22 ± 0.15 nA after continuous illumination for 60 s (10 mW cm -2 ). Even for a single NP monolayer, the photocurrent under RCP was 1.47-fold higher in magnitude than under LCP, which markedly exceeds the subpercentile differences in RCP versus LCP adsorption in thin films of chiral materials. Importantly, it also exceeds the photocurrents generated in metamaterials [START_REF] Lee | Highly photoresponsive and wavelength-selective circularly-polarized-light detector based on metal-oxides hetero-chiral thin film[END_REF][START_REF] Chen | Circularly polarized light detection using chiral hybrid perovskite[END_REF] .

Uniqueness of nanofilms from enantiopure Phe-NPs. To shed light on the polarization dependence of the photocurrent, I and ΔI L-R values of nanofilms modified at different concentrations of l-Phe were analysed. As the l-Phe concentration increased, the amplitude of the chiroplasmonic peak increased from 0 to 350 mdeg at 762 nm, reaching a plateau at 30 mM l-Phe (Fig. 3a). ΔI L-R increased in the same progression and retained a perfect mirror-image symmetry (Fig. 3b and Supplementary Fig. 9). One might expect to see similar amplitudes of ΔI L-R and maxima of CD spectra and concentration dependence for other chiral amino acids, but that was not the case. Surprisingly, however, all 15 seemingly similar surface ligands displayed CD peaks smaller by more than an order magnitude (<25 mdeg) and near-zero ΔI L-R (Fig. 3c and Supplementary Fig. 10).

Structural reasons for the uniqueness of Phe-NP nanofilms can be understood by analysing high-resolution transmission electron microscopy (HRTEM) images of several types of NPs. An unexpectedly thick organic layer was observed on the NPs modified with l-Phe and d-Phe, whereas the layers of surface ligands on all the other NPs were nearly indistinguishable with HRTEM (Fig. 3d). As the l-or d-Phe concentration for Cit-NP modification before nanofilm preparation increased from 10 to 30 mM, the thickness of the organic layer on the NP surface increased from ~0.8 to 2.3 nm and remained unchanged above 30 mM. Our data show that the thickness of the surface layer correlated directly with both the amplitude of the CD peak and ΔI L-R (Fig. 3e and Supplementary Fig. 11). Formation of the organic layer on NP surfaces is attributed to facile d-or l-Phe self-limited self-assembly into non-covalently bonded multilayers (Supplementary Table 1 and Supplementary Figs. 12 and 13) [START_REF] Do | Phenylalanine oligomers and fibrils: the mechanism of assembly and the importance of tetramers and counterions[END_REF][START_REF] Singh | Therapeutic implication of l-phenylalanine aggregation mechanism and its modulation by d-phenylalanine in phenylketonuria[END_REF][START_REF] Amdursky | Circular dichroism of amino acids: following the structural formation of phenylalanine[END_REF][START_REF] Xia | Self-assembly of self-limiting monodisperse supraparticles from polydisperse nanoparticles[END_REF] . The weak CD and near-zero ΔI L-R values of The photoinduced current generated across the membranes was greater for RCP illumination than for LCP illumination in nanofilms made from l-Phe-NPs. The opposite was true for nanofilms made from d-Phe-NPs. b, Structural characterization of nanofilms. Photograph of the photosensitive membranes (diameter 12 mm) carrying a nanofilm from l-Phe-NPs (left). SEM image of the cross-section of the AAO membrane with the nanofilm on top (middle). SEM image of the monolayer l-Phe-NP film (right). c, 3D tomographic image of a monolayer of l-Phe-NP film. d, Schematic illustration of the model system used in the electrodynamics simulations in e. e, Vectors depicting the electric field of the LCP photons at 690 nm that were scattered by the model l-Phe-NP film in d. The NPs are depicted as black dashed lines, and vectors pointing in the z direction stand for the photons that have been scattered at angles close to 90° and are moving inside the membrane, which acts as a wave guide. f,g, Experimental (f) and calculated (g) CD spectra for nanofilms from l-Phe-NP and d-Phe-NP. h,i, Temporal profile of the photocurrent across the photosensitive membrane with nanofilms from l-Phe-NPs (h) and d-Phe-NPs (i). j,k, Temporal profile of the photovoltage across the photosensitive membrane with nanofilms from l-Phe-NPs (j) and d-Phe-NPs (k) induced with CPL illumination (10 mW cm -2 ) at 808 nm.

the other 15 chiral ligands also confirm that the organic layer on the Phe-modified NPs dictates their chirality and the photocurrent in the nanofilm.

Mechanism of CPL-dependent photocurrent generation. We initially hypothesized that the unusually large effect of circular polarization on the photocurrent in nanofilms was attributable to local heating. However, there were no statistically significant differences in the photothermal effects for nanofilms made from Cit-, dl-Phe-, l-Phe-or d-Phe-NPs, for which the photocurrent values exhibited large differences, suggesting that the photothermal effect was not responsible for ΔI L-R (Supplementary Fig. 14).

Then, we tested whether I could be attributed to the irreversible photocatalytic oxidation of the Phe film on the NPs. However, Phe surface ligands remained unchanged under the illumination conditions used in our electrochemical experiments over numerous cycles (Supplementary Figs. 4 and11). These data indicated that the photoinduced decomposition was not responsible for the observed photochemical effects.

We also considered the possible contribution of chiral-induced spin selectivity (CISS) effects [START_REF] Naaman | Chiral molecules and the electron spin[END_REF] , but the lack of response to the external magnetic field in different formats (Supplementary Fig. 15) as well as other tests, including the variation of different amino acids with specific orientation to the gold surface (Fig. 3c and Supplementary Fig. 10), indicated that the contribution of the CISS effects was too small to generate ΔI L-R with a magnitude commensurate with the data shown in Fig. 2.

When the pore diameter becomes comparable to the Debye screening length, light-matter interactions in plasmonic films can also affect the ionic atmosphere and ion transport through the films [START_REF] Sun | A light-regulated host-guest-based nanochannel system inspired by channelrhodopsins protein[END_REF][START_REF] Xie | Photocurrent generation based on a light-driven proton pump in an artificial liquid membrane[END_REF][START_REF] Mourot | Rapid optical control of nociception with an ion-channel photoswitch[END_REF][START_REF] White | Observation of photovoltaic action from photoacid-modified Nafion due to light-driven ion transport[END_REF][START_REF] Xiao | Artificial light-driven ion pump for photoelectric energy conversion[END_REF] . Besides inorganic materials [START_REF] Senocrate | On the way to optoionics[END_REF] , coupled optical and ionic An 808 nm light source showed a high photocurrent of 6.82-10.04 nA and ΔI L-R = 3.22 nA. In contrast, CPL irradiation at 532 nm generated a photocurrent of 1.32 nA; there was no significant difference between LCP and RCP within the error range. CPL with a wavelength of 660 nm generated a photocurrent of 3.95-5.55 nA, and the difference between LCP and RCP was 1.60 nA, which was not as large as that observed at 808 nm. b, ΔI L-R (top) and CD spectra (bottom) observed for nanofilms made from NPs of different sizes. Within this range of NP diameters, the larger the diameter, the higher the CD peak; the maximum-of-absorption peak tended to red shift as the diameter increased. ΔI L-R present concomitant rise and eventual saturation for 35 processes, also known as optoionic effects, may also occur in nanofilms from chiral NPs. When the electrolyte (KCl) concentration around the membrane approached 0.01 mM, no discernible photoeffect was observed. As the electrolyte concentration increased, ΔI L-R increased and reached saturation at 10 mM. At any electrolyte concentration, the rise and decay times of I(t) exceeded 10 s, which is characteristic of the diffusion of ions rather than electrons, and is consistent with expectations for ion fluxes induced by optical phenomena (Supplementary Fig. 16).

Based on the results described above, the polarization-sensitive photocurrent is attributed to the ejection of electrons [START_REF] Brongersma | Plasmon-induced hot carrier science and technology[END_REF][START_REF] Clavero | Plasmon-induced hot-electron generation at nanoparticle/ metal-oxide interfaces for photovoltaic and photocatalytic devices[END_REF] at the particle-medium interface [START_REF] Nakanishi | Photoconductance and inverse photoconductance in films of functionalized metal nanoparticles[END_REF][START_REF] Cortes | Plasmonic hot electron transport drives nano-localized chemistry[END_REF] . These electrons are sometimes referred to as 'hot' electrons and they are analogous with photogenerated solvated electrons in the electromagnetic field of laser pulses [START_REF] Hapiot | Application of laser pulse photoinjection of electrons from metal electrodes to the determination of reduction potentials of organic radicals in aprotic solvents[END_REF] . Their chemical interactions with the delocalized orbitals of aromatic molecules in the medium can lead to entrapment enhanced by the coupling of chiral Phe and metallic NP cores, which subsequently induced ion transport to and from the NP interfaces. Although the ejected electrons are short-lived, continuous illumination causes a steady-state photocurrent at the NP-electrolyte interface, especially under conditions of the wave-guided resonance present in the nanofilms. The strong coupling between out-of-plane NP dipolar moments suppresses radiative decay, trapping light in the plane of the nanofilm and strongly localizing optical fields on each NP [START_REF] Wang | Manipulating light-matter interactions in plasmonic nanoparticle lattices[END_REF][START_REF] Mueller | Deep strong light-matter coupling in plasmonic nanoparticle crystals[END_REF] . To probe this mechanism, the charge density at the NP-electrolyte interface arising from the ejection and entrapment of electrons was evaluated using density functional theory (DFT). Although NP models amenable to DFT simulations (Fig. 4a and Supplementary Fig. 17) are smaller than the particles used in the experiment, and do not have the same thick layer of organic ligands observed in the HRTEM images, the key features in their absorption and CD spectra were similar to those measured experimentally (Fig. 4b and Supplementary Fig. 2).

To further confirm the optoionic mechanism, we note that it necessitates the nanofilm to acquire negative charge at the NP-medium interface on illumination with visible light (Fig. 4c and Supplementary Videos 1 and 2). The dependence of electron excitation on the chemical structure of ligands can be evaluated by fractional occupation number weighted electron density (FOD), which enables calculating the average number of electrons at the NP-electrolyte interface (N FOD ). Comparison of NPs carrying Cit, l-Cys, l-Tyr and different numbers of Phe ligands shows that greater density of surface ligands and higher molecular mass increases N FOD . For example, as the number of Phe ligands rose from 4 to 12, N FOD increased from 74 to 87 (Fig. 4a), which is consistent with the observed rise in ΔI L-R with increasing Phe surface density (Fig. 3a,b). These calculations also indicate that not only the surface density, but also the aromaticity of surface ligands play a role in accommodating temporarily entrapped electrons at the interface. As such, N FOD values for Tyr and Phe are higher than for Cys. The total thickness of surface ligands is also essential for stabilizing photogenerated charges on NP surfaces, which directly affect I. The self-assembled 2.3 nm layer of Phe is approximately ten times thicker than the layers formed by other ligands. The thick layer of Phe entraps electrons in the interfacial region more efficiently than the much thinner layer of Tyr. Such entrapment increases the steady-state concentration of charges at the interface, with the electronic processes being similar to the electron entrapment at semiconductor-gold interfaces [START_REF] Clavero | Plasmon-induced hot-electron generation at nanoparticle/ metal-oxide interfaces for photovoltaic and photocatalytic devices[END_REF] .

The increase of the negative charge at the NP-water interface on illumination, manifesting as polarization-dependent photovoltage (Fig. 1j,k) causes migration of ions through the network of nanoscale channels formed by NPs. The kinetics of the resulting photocurrent calculated by finite element simulations show temporal dependence identical to those observed in the experiment (Fig. 4d and Supplementary Fig. 18). Photocurrent at different wavelengths and in the nanofilms made from differently sized NPs (based on the Poisson-Nernst-Planck equation) also agree very well with experimental results (Supplementary Tables 2 and3).

Detection of circular polarization with multilayer nanofilms.

The optimal conditions for CPL detection using chiral NP membranes were examined to better understand the advantages and disadvantages of polarization-sensitive optoionic effects compared to other technical solutions in chiral photonics. The multilayer films were fabricated by consecutively transferring NP monolayers onto an AAO support (Supplementary Fig. 19). As the number of NP layers increased, the CD amplitude increased significantly from monolayers to bilayers to trilayers, reaching 950 mdeg for the 3L nanofilms (Fig. 5a). The photocurrent also increased, with ΔI L-R reaching 6.43 nA for 3L nanofilms (Fig. 5b). This value represents a large electronic read-out for RCP light, 1.87-fold higher than under LCP illumination and exceeding the photovoltage/photocurrent differences for circularly polarized states on incident photons of organic, inorganic and metastructured thin films [START_REF] Lee | Highly photoresponsive and wavelength-selective circularly-polarized-light detector based on metal-oxides hetero-chiral thin film[END_REF][START_REF] Chen | Circularly polarized light detection using chiral hybrid perovskite[END_REF] . Moreover, the ratio between photocurrent obtained for RCP and LCP was as high as 2.20-fold and 2.41-fold for 5L and 10L nanofilms, respectively (Fig. 5c,d). Importantly, I(t) profiles for the nanofilms from l-Phe-or d-Phe-NPs did not show any evidence of degradation for multiple on-off cycles under LCP and RCP illumination (Fig. 5g and Supplementary Fig. 20). Finally, by rotating the quarter-wave plate at different angles under illumination, we found that the degree of polarization of light affected the intensity of the photocurrent. The established relationship between I and the degree of light polarization enables accurate detection of the ellipticity of the incident light beam (Fig. 5e and Supplementary Fig. 21). Importantly, the detection of CPL was equally accurate regardless of the incident angle, which vividly differentiates our NP-based films from metasurfaces and other polarization-sensitive optoelectronic prototypes (Fig. 5f and Supplementary Fig. 22).

Conclusions

The unexpectedly strong sensitivity of photocurrent to polarization was observed for chiroptically active nanofilms from gold NPs with a uniquely thick self-assembled layer of phenylalanine. The differentiation between RCP and LCP exceeds that previously observed for thin chiral films of organic or inorganic materials by 1-2 orders of magnitude, which is attributed to wave-guided chiroplasmonic modes propagating along the nanofilm surface and charge entrapment in chiral surface ligands around the NPs. Although metamaterials with optoelectronic effects exhibit shorter response times [START_REF] Yang | Circularly polarized light detection by a chiral organic semiconductor transistor[END_REF][START_REF] Li | Circularly polarized light detection with hot electrons in chiral plasmonic metamaterials[END_REF] , manufacturing with self-assembled NP films offers the benefit of simplicity, scalability and energy efficiency. The high CPL contrast of the photocurrent opens the path to the application of

Fig. 1 |

 1 Fig. 1 | Polarization-sensitive optoionic effects in nanofilms from chiral plasmonic NPs. a, Schematic illustration of the electrochemical cell used in the study. The photoinduced current generated across the membranes was greater for RCP illumination than for LCP illumination in nanofilms made from

  (extinction) D-Phe (absorption) D-Phe (scattering) L-Phe (extinction) L-Phe (absorption) L-Phe (scattering) | www.nature.com/naturenanotechnology

Fig. 2 |

 2 Fig. 2 | Photocurrent generation across nanofilms from l-Phe-NPs. a, ΔI L-R (top) and I (bottom) observed for CPL illumination with different wavelengths.An 808 nm light source showed a high photocurrent of 6.82-10.04 nA and ΔI L-R = 3.22 nA. In contrast, CPL irradiation at 532 nm generated a photocurrent of 1.32 nA; there was no significant difference between LCP and RCP within the error range. CPL with a wavelength of 660 nm generated a photocurrent of 3.95-5.55 nA, and the difference between LCP and RCP was 1.60 nA, which was not as large as that observed at 808 nm. b, ΔI L-R (top) and CD spectra (bottom) observed for nanofilms made from NPs of different sizes. Within this range of NP diameters, the larger the diameter, the higher the CD peak; the maximum-of-absorption peak tended to red shift as the diameter increased. ΔI L-R present concomitant rise and eventual saturation for35 nm NPs. c,d, ΔI L-R (top) and I (bottom) observed for different illumination intensity (c) and exposure time (d). The I and ΔI L-R values increased gradually as the illumination intensity and duration increased. The error bars represent the standard deviations of three independent tests.

  Fig. 2 | Photocurrent generation across nanofilms from l-Phe-NPs. a, ΔI L-R (top) and I (bottom) observed for CPL illumination with different wavelengths.An 808 nm light source showed a high photocurrent of 6.82-10.04 nA and ΔI L-R = 3.22 nA. In contrast, CPL irradiation at 532 nm generated a photocurrent of 1.32 nA; there was no significant difference between LCP and RCP within the error range. CPL with a wavelength of 660 nm generated a photocurrent of 3.95-5.55 nA, and the difference between LCP and RCP was 1.60 nA, which was not as large as that observed at 808 nm. b, ΔI L-R (top) and CD spectra (bottom) observed for nanofilms made from NPs of different sizes. Within this range of NP diameters, the larger the diameter, the higher the CD peak; the maximum-of-absorption peak tended to red shift as the diameter increased. ΔI L-R present concomitant rise and eventual saturation for35 nm NPs. c,d, ΔI L-R (top) and I (bottom) observed for different illumination intensity (c) and exposure time (d). The I and ΔI L-R values increased gradually as the illumination intensity and duration increased. The error bars represent the standard deviations of three independent tests.

Fig. 3 |

 3 Fig. 3 | uniqueness of Phe-NPs for generating CPL-dependent photocurrent. a, CD spectra of gold nanofilms modified at different concentrations of l-Phe. b, Dependence of ΔI L-R on the concentration of Phe during the preparation of the gold nanofilms. c, CD amplitudes and ΔI L-R values for NPs with different chiral surface ligands. Cys, cysteine; Tyr, tyrosine; Trp, tryptophan; GSH, glutathione; Pen, penicillamine; Arg, arginine; Pro, proline; Thr, threonine; Val, valine; Ser, serine; Lys, lysine; His, histidine; FF, diphenylalanine; HOMO-Phe, homophenylalanine. d, HRTEM images of Cit-stabilized gold nanofilms and gold nanofilms modified with l-Cys, l-Tyr or dl-Phe, and HRTEM images of the nanofilms after the addition of l-Phe at different concentrations during the surface modification of the NP membrane. The scale bars are 2 nm. e, CD amplitudes (blue) and ΔI L-R changes (red) as a function of the thickness of the organic layer on the surfaces of NPs modified at different concentrations of l-Phe. Inset: the thickness of the organic layer on the surface of NPs modified at different concentrations of l-Phe. As the concentration of l-Phe in the solution used for surface modification increased, the thickness of the l-Phe layer on the surfaces of NPs gradually increased, reaching saturation at 30 mM Phe. The CD amplitudes and ΔI L-R values showed the same changing trends as the thickness of the organic layer. The averages of three independent tests are plotted.

Fig. 4 |

 4 Fig. 4 | Photocurrent generation via plasmon-driven ejection of electrons to the particle-medium interface. a, FOD for different NP-ligand models.All FOD isosurfaces were obtained using 0.002 e/Bohr 3 and 0.02 e/Bohr 3 isovalues for semitransparent grey isosurfaces and opaque blue isosurfaces, respectively. Grey denotes the regions that can be accessible to ejected electrons; blue denotes the regions where they are more likely to be localized. b, CD spectra calculated for NPs decorated with either Phe or a mixture of Cit and Phe. c, DFT simulation of the average transient electrostatic potential distribution of Au 55 (l-Phe)12 and Au 55 (Cit) 4 (l-Phe) 8 under excitation by 808 nm photons. These results directly confirm that both systems produce a non-uniform electrostatic potential of tens of millivolts in the nearby solution, and the adsorbed ions are expected to move in response to the corresponding electric field. Au 55 (Cit) 4 (l-Phe) 8 shows a higher photoexcitation potential under light because it has a stronger solvated-electron-holding capacity. The spherical surfaces around the NPs correspond to the regions in which ions are expected to be adsorbed onto their surfaces. The total electrostatic potential was split into the contribution from the NPs and the ligands. d, The normalized photocurrent difference generated by the different transmembrane potentials driving the directional ion transport calculated with finite element simulations; the photocurrent kinetics were nearly identical to those observed experimentally.

Fig. 5 |

 5 Fig.5| CPL detection using multilayer nanofilms. a, CD spectra of monolayer (1L), bilayer (2L) and three-layer (3L) NP films. b, I registered for 3L nanofilms from l-Phe-modified NPs under CPL illumination. c,d, Dependence of I (c) and ΔI L-R (d) on the number of layers in l-Phe-modified nanofilms; 5L, five layers; 10L, ten layers. e, Polar plots of the polarization dependence of the photocurrent of 1L and 3L nanofilms from l-Phe-modified NPs. The length of the vector from the centre of the coordinates to the point on the curve is equal to I. The polar angle represents the angle of rotation of the quarter-wave plate and the degree of incident light ellipticity. f, The photocurrent measurements for the 3L nanofilms from l-Phe-modified NPs irradiated with light at different incident angles (that is, the angle between the light and the surface of the nanofilm). The error bars represent the standard deviations of three independent tests. g, Stability tests of photocurrent under CPL illumination. Photocurrent generated by the CPL-illuminated nanofilm was reproducible over 30 on-off cycles. Similar results were obtained for n = 3 independent nanofilm samples.

NAtuRE NANotECHNoLoGy | www.nature.com/naturenanotechnology

© The Author(s), under exclusive licence to Springer Nature Limited 2022 NAtuRE NANotECHNoLoGy | www.nature.com/naturenanotechnology

Acknowledgements C.X. acknowledges support from the National Key Research and Development Program of China (grant no. 2017YFA0206902), W.Z. acknowledges support from the National Key Research and Development Program of China (grant no. 2017YFA0303400), H.K., L.X. and M.S. acknowledge support from the National Natural Science Foundation of China (grant nos. 21925402, 32071400 and 21977038), H.K. acknowledges support from the Natural Science Foundation of Jiangsu Province (grant no. BK20212014), W.Z. acknowledges support from the National Natural Science Foundation of China (grant nos. 11774036 and 12174032) and from the National Natural Science Foundation of China/Research Grants Council (grant no. 11861161002). N.A.K. is grateful for support from the National Science Foundation via projects NSF 1463474 "Energy-and Cost-Efficient Manufacturing Employing Nanoparticles" and NSF 1566460 "Nanospiked Particles for Photocatalysis". R.K. acknowledges support from the Minerva Foundation with funding from the Federal German Ministry for Education and Research. F.M.C., W.R.G., M.C.S., E.B.C.-N., E.C.P. and A.F.M. are grateful to the Brazilian funding agencies CAPES (finance code 001), CNPq-INCT (573742/2008-1) and FAPESP (2012/15147-4, 2013/07296-2, 2014/50249-8, 2015/12851-0 and 2017/11986-5) for financial support and the HPC resources provided by the SDumont supercomputer at the National Laboratory for Scientific Computing (LNCC/MCTI, Brazil; http://sdumont.lncc.br) and by the Cloud@UFSCar (https://www.sin.ufscar.br). A.F.M. is grateful to MEC/PET for a fellowship and to CNPq for a research fellowship.

Data availability

Source data are provided with this paper. All data that support the findings of this study have been included in the main text and Supplementary Information. Any additional materials and data are available from the corresponding authors on reasonable request.

Articles

NaTure NaNOTeCHNOlOgy plasmonic materials-based chiral photonics. These findings present the possibility of mimicking the polarization vision of animals in non-biological nanoscale constructs. Integration with microfluidic devices and the absence of incident angle dependence offer the opportunity for conformal technological replicas of CPL-sensitive organs for utilization in machine vision. Further explorations are expected towards constructing optoionic membranes with enhanced mirror asymmetry to improve the polarization recognition characteristics. Furthermore, incorporation of chiral NPs with high g-factors [START_REF] González-Rubio | Micelle-directed chiral seeded growth on anisotropic gold nanocrystals[END_REF] and chiral perovskites [START_REF] Di Nuzzo | Circularly polarized photoluminescence from chiral perovskite thin films at room temperature[END_REF] can lead to their implementation in optical computing and telecommunication technologies.

Articles

NaTure NaNOTeCHNOlOgy

Methods

Preparation of chiral Au

NPs. An Au NP colloid dispersion (d = 35.1 ± 0.8 nm) was synthesized by the citrate reduction of chloroauric acid (HAuCl 4 ) in the aqueous phase [START_REF] Zhao | Tuning the interactions between chiral plasmonic films and living cells[END_REF] . In brief, 6 ml of 10 mM HAuCl 4 solution was added to 195 ml of deionized water and boiled. Then, 3.2 ml of 10% w/v sodium citrate solution and 1.5 ml of 5 nm Au seed solution were added, and the mixture was boiled for 20 min to generate a stable colloid solution of Au NPs. The NPs were concentrated tenfold by centrifugation and resuspended in a 10 mM carbonate buffer solution to obtain a high-concentration Au NP solution. Finally, the desired amount of Phe was added, and the solution was incubated for 2 h at 60 °C. The average particle diameters were determined using TEM on a JEOL JEM-2100 transmission electron microscope (operated at an acceleration voltage of 200 kV). Differently sized Au NPs were synthesized by adjusting the amount of sodium citrate added. The sizes of the NPs were confirmed with a Zetasizer Nano ZS (Malvern) equipped with a 632.8 nm laser.

Preparation of chiroplasmonic membranes. Free-standing nanofilms were formed at a water-oil interface using an aqueous solution of the chiral Au NPs and an n-hexane phase. The self-assembly of the NPs at the interface was induced by the slow addition of ethanol [START_REF] Edel | Fundamentals and applications of self-assembled plasmonic nanoparticles at interfaces[END_REF][START_REF] Hu | Oil-water interfacial self-assembly: a novel strategy for nanofilm and nanodevice fabrication[END_REF] . The n-hexane phase was then allowed to evaporate slowly, and the nanofilm was transferred to an AAO membrane using monolayer lift-off onto a solid support. The AAO membrane with a pore diameter of 20 nm, a thickness of 60 μm and a pore density of 10 11 per cm 2 (Puyuan Hefei Nano) was used as a self-supporting porous template.

Electrochemical measurements. The NP-AAO membranes were placed between two Plexiglass cells with holes 3 mm in diameter. A KCl solution (2 ml) was added to each of the two chambers. A pair of Ag/AgCl electrodes and a CHI-760 electrochemical workstation (CHI) were used to record the change in current over time [START_REF] Gao | Nanofluidics in two-dimensional layered materials: inspirations from nature[END_REF] . CPL with different polarization directions was produced by adjusting a quarter-wave plate. During the test, the change in the current was monitored as the light was turned on and off. Unless otherwise specified, the wavelength used for irradiation was 808 nm, the light intensity was 10 mW cm -2 and the duration of irradiation ('on') and the interval ('off ') between two irradiation cycles were 60 s.

Statistics and reproducibility.

Experimental errors were calculated as the standard error of the mean, with n referring to the number of analysed samples and reported in the figure legends.

Author contributions

H.K., R.K., N.A.K. and C.X. conceived the project and designed the experiments. J.C. was responsible for electrochemical, CD and CPL measurements. W.Z. was responsible for the calculations of optical response (absorption and circular dichroism) and photocurrent calculations based on the Poisson-Nernst-Planck equation. L.X. and C.H. performed the HRTEM, TEM, SEM and AFM experiments. L.X. and W.M. carried out the preparation of gold nanofilms. M.S. and X.W. were responsible for the synthesis and modification of gold NPs with different particle sizes. F.M.C., W.R.G., M.C.S., E.B.C.-N., E.C.P. and A.F.de.M. designed, executed and analysed the simulations of DFT calculations, electrodynamics calculations and finite element calculations and wrote the corresponding text. R.A.L.V., X.L., X.Q. and J.X. carried out calculations related to the interaction between Phe and gold. H.K. and N.A.K. conceptualized the work. C.X. supervised the study. H.K., R.K., N.A.K. and C.X. analysed and discussed the results and wrote the manuscript.

Competing interests

The authors declare no competing interests.

Additional information

Supplementary information

The online version contains supplementary material available at https://doi.org/10.1038/s41565-022-01079-3.

Correspondence and requests for materials should be addressed to Chuanlai Xu, Rafal Klajn, Nicholas A. Kotov or Hua Kuang.

Peer review information Nature Nanotechnology thanks Malcolm Kadodwala, Stefan Meskers and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Reprints and permissions information is available at www.nature.com/reprints.


Stéphanie Vanwalleghem
email: stephanie.vanwalleghem@parisnanterre.fr

Raphaële Miljkovitch

Annie Vinter

Attachment representations among school-age children with intellectual disability

Keywords:

Background: Research data documenting a high risk of insecure and disorganized attachment among children with intellectual disability (ID) in infancy and early childhood raises the question of mutual influences between ID and attachment in later childhood. Aims: The objectives of the present study were to examine attachment among school-age children with ID and whether attachment varies according to level of intellectual functioning, adaptative functioning, and presence of a genetic syndrome (i.e. Down syndrome).

What this paper adds?

A higher risk of disorganized attachment has been described among infants and young children with ID. It is unclear whether this is also true during late childhood. This study shows that attachment representations of school-age children with ID are less secure than those of typically developing children of the same chronological age and more disorganized than those of typically developing children of the same chronological age or of the same mental age.

Previous research has raised the question of a link between level of intellectual functioning and attachment. Findings suggest that attachment representations are related to level of adaptive functioning but not to intellectual functioning.

In the literature, it was unclear whether attachment varies as a consequence of a genetic syndrome underlying ID. In this study, no differences were found in security and disorganized representations between children with Down Syndrome and children with nonspecific ID.

Introduction

According to [START_REF] Bowlby | Attachment and loss[END_REF], seeking contact and proximity with familiar caregivers and the development of an attachment bond are necessary to survive and to adapt to the environment. The attachment system is an innate behavioral system that ensures protection by eliciting care from adult caregivers. Thereby, it enables infants and children to regulate emotions, especially distress, via the intervention of adults. For this to happen, children need to signal attachment cues that elicit appropriate and effective responses from caregivers [START_REF] Ainsworth | Patterns of attachment: A psychological study of the Strange Situation[END_REF]Bowlby, 1973Bowlby, /1980)). This is characteristic of children who are secure in the relationship with their attachment figure: they signal distress efficiently enough to receive sensitive and prompt responses. Insecure children however need to adapt their innate attachment signals to their caregivers' responses by either deactivating (avoidant attachment) or hyperactivating (resistant attachment) their attachment system [START_REF] Kobak | Attachment and emotion regulation during mother-teen problem solving: A control theory analysis[END_REF][START_REF] Main | Cross-cultural studies of attachment organization: Recent studies, changing methodologies, and the concept of conditional strategies[END_REF]. A fourth classification (disorganized attachment) concerns infants who exhibit conflicting tendencies (e.g., avoidance and approach) or disorientation [START_REF] Main | Procedures for identifying disorganized/disoriented infants during the Ainsworth Strange Situation[END_REF] or whose behavior patterns are unusual, bizarre, or contradictory, suggesting failure to develop a coherent attachment strategy.

Because early experiences within attachment relationships contribute to shape mental health [START_REF] Mikulincer | An attachment perspective on psychopathology[END_REF]) and because individuals with intellectual disability (ID) are at increased risk of developing mental health disorders [START_REF] Dykens | Annotation: Psychopathology in children with intellectual disability[END_REF], researchers have examined links between ID and attachment (for a review see [START_REF] Schuengel | Attachment, intellectual disabilities and mental health: Research, assessment and intervention[END_REF]. Research suggests high rates of disorganized attachment among infants and preschool children with ID [START_REF] Feniger-Schaal | Attachment quality of children with ID and its link to maternal sensitivity and structuring[END_REF][START_REF] Vaughn | Quality of toddler-mother attachment in children with Down syndrome: Limits to interpretation of strange situation behavior[END_REF]. This calls for special attention as disorganized attachment is also associated with poor social development and the emergence of externalizing behavior disorders [START_REF] Granqvist | Disorganized attachment in infancy: A review of the phenomenon and its implications for clinicians and policy-makers[END_REF][START_REF] Groh | Attachment in the early life course: Meta-analytic evidence for its role in socioemotional development[END_REF]. The links between ID and attachment are still poorly documented and empirical studies are scarce. Namely, it is unknown whether the high proportion of disorganized attachment also concerns school-age children. The objectives of the present study were to examine attachment representations among children with ID in late childhood and whether attachment is associated with IQ, adaptation, and presence of a genetic syndrome (i.e. Down syndrome).

Attachment and ID in the preschool years

Attachment in preschoolers with ID has been studied using the Strange Situation Procedure (SSP: [START_REF] Ainsworth | Patterns of attachment: A psychological study of the Strange Situation[END_REF]. This procedure consists in triggering infants' or young children's attachment behaviors by exposing them to short separation-reunion sequences with the attachment figure, in the presence of an unfamiliar adult. In this situation, children normally adopt a specific behavioral pattern that reflects quality of attachment to their caregiver: secure (children exhibit distress but are easily calmed and able to explore once the attachment figure is back), insecure-avoidant (infants inhibit attachment behaviors and avoid their attachment figure upon their her return), insecure-resistant (infants show proximity seeking and resistant behaviors during reunion episodes, as well as persisting distress) or disorganized (conflicting attachment strategies).

In a meta-analysis, Van IJzendoorn, [START_REF] Van Ijzendoorn | Disorganized attachment in early childhood: Meta-analysis of precursors, concomitants, and sequelae[END_REF] observed that in low-risk samples 62 % of infants were secure, 15 % were avoidant, 9 % were resistant, and 15 % were disorganized. In older children, the same percentage of disorganization was found. The few studies on attachment behavior patterns among young children with ID showed different proportions: A recent study on 2-6-year-olds with non-specific ID reported that only 40 % of them were secure and 32.5 % were disorganized [START_REF] Feniger-Schaal | Attachment quality of children with ID and its link to maternal sensitivity and structuring[END_REF]. The proportions of avoidant (12.5 %) or resistant (15 %) attachment classifications were close to those of the general population [START_REF] Van Ijzendoorn | Disorganized attachment in early childhood: Meta-analysis of precursors, concomitants, and sequelae[END_REF]. In an earlier study involving 138 children with Down Syndrome (DS) aged 14-54 months [START_REF] Vaughn | Quality of toddler-mother attachment in children with Down syndrome: Limits to interpretation of strange situation behavior[END_REF], a smaller proportion of secure children (46 %) was also found. Of the remaining children, 9 % were avoidant, 3 % resistant, and 42 % "unclassifiable" (see also [START_REF] Atkinson | Maternal sensitivity, child functional level, and attachment in Down syndrome[END_REF] for age-specific results on a subsample of the Vaughn et al. study). In this study, the authors did not use the disorganized category, which was not yet very used at the time. Behavioral patterns of children in the unclassifiable category did not fit any of those of the three Ainsworth categories. Thus, the unclassifiable category presumably overlaps the disorganized category. Both studies suggest a lower proportion of secure attachment and higher rates of disorganized or unclassifiable attachment behavior patterns among preschoolers with ID compared to typically developing children. This raises questions as to possible factors underlying disorganized/unclassifiable attachment and of their continued effect in later childhood. In later childhood, attachment is measured through representational measures, using narrative story stems [START_REF] Allen | Assessing disorganized attachment representations: A systematic psychometric review and metaanalysis of the Manchester Child Attachment Story Task[END_REF], rather than through behavioral measures (Solomon & George, 2016).

Caregiver sensitivity and attachment

In their review on attachment, intellectual disabilities, and mental health, [START_REF] Schuengel | Attachment, intellectual disabilities and mental health: Research, assessment and intervention[END_REF] highlighted that context, starting with caregiver sensitivity, is important to consider when attachment behavior is problematic. During the SSP, children with ID show different attachment patterns [START_REF] Atkinson | Maternal sensitivity, child functional level, and attachment in Down syndrome[END_REF][START_REF] Feniger-Schaal | Attachment quality of children with ID and its link to maternal sensitivity and structuring[END_REF][START_REF] Vaughn | Quality of toddler-mother attachment in children with Down syndrome: Limits to interpretation of strange situation behavior[END_REF], suggesting that they can adapt their attachment behaviors to their caregivers. Similar to what is observed among typically developing children, significant links were found between maternal sensitivity and quality of attachment of children with ID, with insecurity being negatively associated with sensitivity [START_REF] Atkinson | Maternal sensitivity, child functional level, and attachment in Down syndrome[END_REF][START_REF] Feniger-Schaal | Attachment quality of children with ID and its link to maternal sensitivity and structuring[END_REF]. Given the high rates of insecure and disorganized attachment behavior patterns, this finding prompts the question of what may compromise sensitivity among parents of children with ID. Preliminary research suggests that parents may fail to identify their children's attachment needs due to the latter's emotional peculiarities. More specifically, infants and young children with ID exhibit lower intensity of emotional reactivity [START_REF] Moore | Behavior of mothers and infants with and without Down syndrome during the still-face procedure[END_REF], less frequent and more fleeting smiles during the first six months of life (when ID is related to DS; [START_REF] Berger | Aspects of early social smiling by infants with Down's syndrome[END_REF], and greater difficulty in communicating emotions to adults [START_REF] Carvajal | Judgments of facial and vocal signs of emotion in infants with Down syndrome[END_REF]. These particularities may compromise co-adaptive processes and increase affective communication errors. Such interactive disturbances are associated with disorganized attachment [START_REF] Beebe | On the origins of disorganized attachment and internal working models: Paper II. An empirical microanalysis of 4-month mother-Infant interaction[END_REF][START_REF] Lyons-Ruth | Chapter IV. Maternal frightened, frightening, or atypical behavior and disorganized infant attachment patterns[END_REF][START_REF] Solomon | The disorganized attachment-caregiving system: Dysregulation of adaptive processes at multiple levels[END_REF]. Lack of maternal responsiveness in infancy is also known to predict attachment disorganization at the level of representation in the preschool years [START_REF] Miljkovitch | Maternal interactive behaviour as a predictor of preschoolers' attachment representations among full term and premature samples[END_REF]. Therefore, children with ID may be at an increased risk of insecure and disorganized attachment representations due to challenges for their caregivers to properly capture their emotional needs and provide sensitive responses. [START_REF] Atkinson | Maternal sensitivity, child functional level, and attachment in Down syndrome[END_REF] showed that the interaction between level of intellectual functioning and maternal sensitivity predicted attachment security among young children with ID: High levels in these two areas were associated with a greater probability of secure attachment behavior patterns, measured with the Attachment Q-sort [START_REF] Waters | Defining and assessing individual differences in attachment relationships: Q-methodology and the organization of behavior in infancy and early childhood[END_REF]. According to these authors, children with the lowest level of intellectual functioning may have more limited resources in terms of intersubjective sharing capacity (expressing needs, understanding the adult's emotional state or intention), making it more difficult for them to co-construct a secure attachment relationship with their attachment figure. However, in Feniger-Schaal and Joels' study (2018) on 2-6-year-olds with non-specific ID, level of intellectual functioning was not associated with attachment. They also found no evidence of a link between level of adaptive functioning and attachment. Yet these non-significant results may be caused by limited statistical power due to the use of attachment classifications (rather than continuous security scores as in the Attachment Q-sort) and smaller sample sizes.

Intellectual and adaptive impairments and attachment

Reciprocally, because disorganized attachment is associated with poor social development [START_REF] Granqvist | Disorganized attachment in infancy: A review of the phenomenon and its implications for clinicians and policy-makers[END_REF], disorganized attachment in children with ID may increase limitations in cognitive and adaptive functioning. In sum, although there may be reasons to expect links between attachment and, respectively, level of cognitive and adaptive functioning among children with ID, more research is needed to document this issue.

Genetic syndrome and attachment

Genetic syndromes are at the origin of some cases of intellectual disability [START_REF] Schalock | The contemporary view of intellectual and developmental disabilities: Implications for psychologists[END_REF]. They develop during the antenatal period and, beyond intellectual disability, are characterized by cognitive and adaptive features inherent to each syndrome (Farran & Karmiloff-Smith, 2012). For example, children with DS are generally prosocial and insufficiently wary of strangers [START_REF] Porter | The neuropsychological basis of hypersociability in Williams and Down syndrome[END_REF]. Thus, they may not feel threatened in situations such as the strange situation, when they are alone with a stranger. These features raise questions as to the effect of this syndrome on attachment. Studies carried out so far have not explored this question. Yet data from studies conducted on children with DS [START_REF] Atkinson | Maternal sensitivity, child functional level, and attachment in Down syndrome[END_REF][START_REF] Vaughn | Quality of toddler-mother attachment in children with Down syndrome: Limits to interpretation of strange situation behavior[END_REF] are consistent with those on children with non-specific ID [START_REF] Feniger-Schaal | Attachment quality of children with ID and its link to maternal sensitivity and structuring[END_REF], in that there is an under-representation of the secure category and increased rates of disorganized or unclassifiable attachment behavior patterns. These data suggest links between attachment and ID, but not between attachment and genetic syndromes more specifically.

To summarize, a higher risk of insecure and disorganized or unclassifiable attachment behavior patterns has been observed among infants and young children with ID [START_REF] Atkinson | Maternal sensitivity, child functional level, and attachment in Down syndrome[END_REF][START_REF] Feniger-Schaal | Attachment quality of children with ID and its link to maternal sensitivity and structuring[END_REF][START_REF] Vaughn | Quality of toddler-mother attachment in children with Down syndrome: Limits to interpretation of strange situation behavior[END_REF]. However, to our knowledge, no study has explored the link between ID and attachment among school-age children with ID. Authors suggest that these increased rates of insecure or disorganized attachment may be due to problems in parent-child interactions resulting from parental difficulties in capturing their children's needs, given the emotional features of children with ID [START_REF] Atkinson | Maternal sensitivity, child functional level, and attachment in Down syndrome[END_REF][START_REF] Granqvist | Disorganized attachment in infancy: A review of the phenomenon and its implications for clinicians and policy-makers[END_REF]. Reciprocally, insecure or disorganized attachment may prevent the proper development of cognition and adaptation [START_REF] Granqvist | Disorganized attachment in infancy: A review of the phenomenon and its implications for clinicians and policy-makers[END_REF].

The present study is aimed at examining attachment representations among school-age children with ID and determining whether increased insecurity and disorganization continue to be observed. Given the contextual factors that may explain increased rates of insecure and disorganized attachment found in previous studies (e.g., lack of parental sensitivity), we expected children with ID to have more insecure and disorganized attachment representations than typically developing children of the same mental age (H1). Based on the assumption of a mutual influence between attachment and cognitive or adaptative functioning, we expected children with ID to have more insecure and disorganized attachment representations than controls of the same chronological age (H2). We expected to find a link between attachment representations and both IQ and adaptive functioning within the ID group (H3). Finally, as found in previous studies, we did not expect to find differences in security and disorganization between children with DS and children with nonspecific ID (H4).

Method

Design and procedure section

The research project was presented to directors and health professionals from medico-social institutions in charge of children with ID and to school teachers for the typically developing children. When the teachers agreed to participate, a letter presenting the study was sent to the parents. Informed written consent was obtained from participants' parents and then participants gave their oral agreement. The experiment was conducted in accordance with the World Medical Association Declaration of Helsinki on Ethical Principles for Medical Research Involving Human Subjects. This study received a favorable opinion of the "Comité Consultatif sur le Traitement de l'Information en matière de Recherche dans le domaine de la Santé » (CCTIRS n • 15.507bis).

Direct assessments were conducted. The tests were administered individually by graduate students in a quiet room in the children's school for typically developing children. For children with ID, assessments were administered at home or in the medico-social institution, at the families' convenience. The duration of the assessments was approximately 45 min.

Measures

Level of intellectual functioning and reasoning among children with ID

Gr´egoire's (2009) short-form Intellectual Quotient (IQs) was used to determine the level of intellectual functioning of participants with ID, and to make sure children with ID all met the DSM-5 (APA, 2013) significant limitation of cognitive functioning criterion for the diagnosis of ID. In accordance with Gr´egoire's IQs recommendations ( 2009), the assessment of the level of intellectual functioning was based on the Similarities, Matrix reasoning, Letter-Number Sequencing and Symbol Search subtests of the Wechsler Intelligence Scale for Children, 4th edition (WISC-4, [START_REF] Wechsler | WISC-IV. Echelle d'intelligence de Wechsler pour enfants et adolescents -Quatrième édition[END_REF]. These four subtests were selected because they highly correlate with total IQ calculated with the ten main subtests of the WISC-4 at all ages [START_REF] Wechsler | WISC-IV. Echelle d'intelligence de Wechsler pour enfants et adolescents -Quatrième édition[END_REF]. Short-form IQs are highly reliable with regards to IQs obtained using the 10 main subtests of the WISC-4 [START_REF] Grégoire | L'examen clinique de l'intelligence de l'enfant, fondements et pratique du WISC-IV (2`eme ´edition)[END_REF]. IQs scores follow a normal distribution with a mean of 100 and a standard deviation of 15. Scores below 70 indicated the presence of intellectual disability.

The level of reasoning of children with ID was assessed to determine the age of the typically-developing children forming the control group of the same mental age. The level of reasoning was evaluated with the Similarities (verbal modality) and Matrix (visual modality) reasoning subtests of the Wechsler Scales (WISC-4/WPPSI-3). The raw score in these two subtests were converted into a developmental age of reasoning. When children with ID failed the Similarities and Matrix subtests of the WISC-4, those of the Wechsler Preschool and Primary Scale of Intelligence-3rd edition [START_REF] Wechsler | WPPSI-III. Echelle d'intelligence de Wechsler pour la période préscolaire et primaire -Troisième édition[END_REF] were used.

Level of adaptive functioning among children with ID

The Vineland Adaptive Behavior Scales, 2nd edition (Vineland-II, [START_REF] Sparrow | VINELAND-II, Echelle d'´evaluation du comportement adaptatif de Vineland, adaptation française[END_REF] were used to determine an overall adaptive level of functioning (Adaptive Behaviour Composite score) and three sub-scores related to communication, daily living skills, and socialization. These scores follow a normal distribution with a mean of 100 and a standard deviation of 15. Scores below 70 indicate significant adaptive limitations. The questionnaire was completed either by a parent or an educator. These scales were also used to check that participants with ID all met the DSM-5 (APA, 2013) significant limitation of adaptive functioning criterion for the diagnosis of ID.

Attachment

Attachment representations were assessed with the Attachment Story Completion Task (ASCT, [START_REF] Bretherton | Assessing internal working models of the attachment relationship: An attachment story completion task for 3-yearolds[END_REF]. In this task, the examiner uses dolls representing family members to stage story beginnings that are supposed to activate the attachment system (e.g., parents leave home for a few days and leave the children with the grandmother). The examiner then asks the child to complete the stories. The ASCT has several advantages for use with children with ID: it is playful, interactive, allows expression with concrete material that doesn't have to be verbal, refers to situations familiar to the child, and stories are short and thereby suitable for children whose attentional capacities are limited. The staging with characters facilitates comprehension, verbal and non-verbal expression. The ASCT is accessible to children as early as age 3, suggesting that it requires a minimum level of cognitive functioning comparable to that of 3-year-olds. In their literature review, [START_REF] Segal | Narrative skills of youth with Down syndrome: A comprehensive literature review[END_REF] explained that children with DS have basic narrative skills, which match those of children of the same mental age or of the same level of language. They also mention that their stories were eased by the display of a visual aid. Moreover, the coding of the ASCT lies on the analysis of both verbal and non-verbal behaviors, which makes the ASCT all the more suitable for children with DS. The ASCT was adapted to everyday life situations of school-aged children according to accommodations proposed by [START_REF] Granot | Attachment security and adjustment to school in middle childhood[END_REF].

The coding system used to analyze the narratives was based on a Q-sort questionnaire consisting of 65 cards (items) describing behaviors observed during play [START_REF] Miljkovitch | Les représentations d'attachement du jeune enfant. Développement d'un système de codage pour les histoires à compléter[END_REF][START_REF] Miljkovitch | Associations between parental and child attachment representations[END_REF]. Scores ranging from 1 to 7 were assigned for each item. Children's scores were compared to those of 4 attachment prototypes yielding 4 scores. For each participant, a secure, avoidant, resistant, and disorganization Q-score was obtained. Inter-rater reliability, tested on 68 cases chosen at random, ranged between .90 and .94 [START_REF] Miljkovitch | Les représentations d'attachement du jeune enfant. Développement d'un système de codage pour les histoires à compléter[END_REF]. The disorganization prototype is based on the classification scheme proposed by [START_REF] Solomon | Children classified as controlling at age six: Evidence of disorganized representational strategies and aggression at home and at school[END_REF] see also George andSolomon, 1990-2016, a coding system of an abridged version of the ASCT, which was developed according to 6-year-old children's SSP classifications. In line with observed links between the SSP and maternal attachment representations according to the Adult Attachment Interview (AAI: [START_REF] George | The adult attachment interview[END_REF]; for a meta-analysis, see [START_REF] Van Ijzendoorn | Intergenerational transmission of attachment: A move to the contextual level[END_REF], construct validity has been established by significant associations between maternal AAI classifications and each of the ASCT Q-sort attachment dimensions, including disorganization [START_REF] Miljkovitch | Associations between parental and child attachment representations[END_REF]. Additional theoretically consistent links with parental attachment states of mind [START_REF] Bernier | Intergenerational transmission of attachment in father-child dyads: The case of single parenthood[END_REF][START_REF] Miljkovitch | Associations between parental and child attachment representations[END_REF][START_REF] Miljkovitch | Intergenerational transmission of attachment representations in the context of single parenthood in France[END_REF] further established the construct validity of this coding system. The disorganization scale's convergent validity was also demonstrated by consistently higher scores among abused children [START_REF] Berdot-Talmier | Représentations d'attachement chez les enfants, agés de 3 à 7 ans, exposés aux violences conjugales[END_REF][START_REF] Charest | Attachment representations in sexually abused preschoolers: A comparative study[END_REF][START_REF] Fresno | The effect of sexual abuse on children's attachment representations in Chile[END_REF][START_REF] Hébert | Disorganized attachment and emotion dysregulation as mediators of the association between sexual abuse and dissociation in preschoolers[END_REF], similar to research findings with the strange situation [START_REF] Cyr | Attachment security and disorganization in maltreating and high-risk families: A series of meta-analyses[END_REF], and consistently higher scores among children with conduct disorders [START_REF] Miljkovitch | Hostile intention attribution among preschoolers with or without conduct disorder: Links with attachment representations[END_REF], similar to research findings with the Manchester Child Attachment Story Task [START_REF] Green | Disorganized attachment representation and atypical parenting in young school age children with externalizing disorder[END_REF]. Expected longitudinal links between both maternal unresponsiveness and lack of sensitivity in infancy with child disorganization at 42 months further established convergent validity [START_REF] Miljkovitch | Maternal interactive behaviour as a predictor of preschoolers' attachment representations among full term and premature samples[END_REF]. In addition, in a preliminary study [START_REF] Vanwalleghem | L'enfant porteur d'une trisomie 21 et ses relations aux autres[END_REF], the narratives of 96 subjects were coded using two coding methods, the one proposed by [START_REF] Granot | Attachment security and adjustment to school in middle childhood[END_REF] and the Q-Sort [START_REF] Miljkovitch | Les représentations d'attachement du jeune enfant. Développement d'un système de codage pour les histoires à compléter[END_REF]. The distributions of children in the 4 attachment categories, including disorganization, were compared. There was no significant difference between the two distributions. This also shows the validity of the Q-sort coding system. Coders were trained and supervised by one of the authors of the coding system. Regular meetings were held to build consensus among coders.

Socio-economic status

The socio-economic status (SES) was estimated using Barratt's simplified measure of social status (BSMSS, [START_REF] Barratt | Barratt simplified measure social status (BSMSS)[END_REF]. BSMSS score is based on both the level of education and the profession of each parent and on family status (married parents, separated, single parent families, etc.). BSMSS scores vary from 8 (lower SES) to 66 (higher SES).

Participants

The study population consisted of a clinical sample, participants with ID, and two control samples. Participants from one control group had the same mental age as participants with ID; mental age was assessed by the level of reasoning. Participants from the second control group had the same chronological age as participants with ID. Control children were randomly recruited in schools. The level of reasoning of children with ID was assessed with the Similarities and Matrix reasoning subtests of Wechsler Scales (WISC-4/WPPSI-3); the estimation has given an age range of 4-6 years.

The clinical sample included 54 children with ID, 34 boys and 20 girls, aged 8-12 years (M = 10.8 years, SD = 1.2 year). Thirty children presented an ID linked with Down syndrome (DS) and 24 a non-specific ID. The presence of an ID was attested by significant limitations in intellectual functioning and adaptive functioning, in accordance with DSM-5 criteria (APA, 2013). The control group of the same level of reasoning, included 54 typically developing children, 27 boys, 27 girls, aged 4-6 years (M = 5.1 years, SD = 0.5 year). The control group of the same chronological age included 54 typically developing children, 28 boys, 26 girls, of 8-12 years of age (M = 10.5 years, SD = 1.5 year).

Participation rate in this study was about 35 % for controls aged 8-12 years, 50 % for controls aged 4-6 years, and 20 % for children with ID. Some parents of children with ID found participation to be an additional burden given the numerous appointments their children already had for medical follow-up and psychosocial care. Others were not in favor of psychological study. A few parents refused for fear that the experimental protocol would set their child up for failure. Some did not give an explanation.

Data analysis

To compare attachment security and disorganization between children with ID and typically developing children, the Welch's ANOVA method was used and was followed by post-hoc Scheffé tests. Then, to explore the links between levels of intellectual and adaptive functioning and attachment among children with ID, partial correlations were used. Finally differences in security and disorganization between children with DS and children with non-specific ID were examined using a MANCOVA.

Results

Preliminary analyses

The proportions of girls and boys in the three groups were comparable: X 2 = 2.14, p > .30. Concerning socio-economic status, the BSMSS score of the ID subgroup was lower than that of control children aged 4-6 years, t(82) = -3.40, p = .001, and of control children Aged 8-12 years, t(88) = -3.08, p = .003. The BSMSS score of the non-specific ID subgroup was lower than that of children with DS, t (52) = 8.72, p < .001. The BSMSS score was therefore controlled in the main analyses. The BSMSS scores are presented in Tables 1 and2.

Among children with ID, the IQ short-form (IQs) was lower in children with Down Syndrome (DS) than in children with nonspecific ID, t(52) = -8.31, p < .001. The Vineland Adaptive Behaviour Composite score was also lower in children with DS than in children with non-specific ID, t(52) = -4.19, p < .001). These two scores were therefore controlled in the statistical analyses comparing these two subgroups. The BSMSS scores, IQ scores and Adaptive Behaviour Composite of children with DS and with nonspecific ID are presented in Table 2.

Main analyses

Comparisons of attachment scores between children with ID and control children

The ASCT scores for the three groups are presented in Table 3. A Welch's ANOVA aimed at testing the effect of the group on the secure dimension indicated a significant group effect, F(2, 98) = 75.94, p = .004. Post-hoc Scheff´e tests showed that children with ID were significantly less secure than controls aged 8-12 years (p = .011) but did not differ from controls aged 4-6 years (p > .10). No significant difference was found between the two control groups on the secure dimension (p > .50) and the two groups were statistically equivalent to 0 according to a two-one-sided-t-tests (TOST) procedure, t(105.78) = 2.38, p = .009, given equivalence bounds of -28.83 and 28.83 (on a raw scale) and an alpha of .05.

Run on the disorganized dimension, a Welch's ANOVA indicated a significant group effect, F(2, 89) = 14.3, p < .001, children with ID being significantly more disorganized than controls aged 4-6 years (post-hoc Scheffé test, p < .001) and than controls aged 8-12 years (p < .001). No significant difference was found between the two control groups (post-hoc Scheffé test, p > .40) and the two groups were statistically equivalent to 0 according to the TOST procedure, t(105.97) = -2.23, p = .014, given equivalence bounds of -21.62 and 21.62 (on a raw scale) and an alpha of .05.

Level of intellectual and adaptive functioning and attachment in children with ID

Partial correlations controlling for BSMSS between the ASCT secure and disorganized dimensions and, respectively, IQs, Vineland Adaptive Behaviour Composite scores, and the three Vineland subscores (socialization, daily living skills, and communication) are presented in Table 4. Partial correlations between the ASCT scales and IQs were non-significant (all |rs| < .14). Revealing that IQs scores were not linked to ASCT scores. Negative correlations were found between the disorganization dimension and, respectively, the Vineland adaptive behaviour composite score, r = -.31, p = .026, and the daily living skills sub-score, r = -.29, p = .035.

Attachment and ID subgroups

The results of the MANCOVA comparing children with Down syndrome (DS) to children with non-specific ID showed that there was no group effect on attachment: F(2, 48) = 0.25; p > .70). There was also no effect of BSMSS on attachment: F(2, 48) = 0.81; p > .40 nor on IQs: F(2, 48) = 0.10; p > .90. However, a significant effect of the Vineland adaptive behaviour composite score on attachment was found: F(2, 48) = 3.62, p = .003. Univariate analyses specified that the effect of the Vineland adaptive behaviour composite score concerned the disorganized dimension only: F(1, 49) = 6.78, p = .012, consistent with the negative correlation between the Vineland adaptive behaviour composite score and disorganization.

Discussion

Attachment among school-age children with ID

The first objective of this study was to compare secure and disorganized attachment representations among children with ID aged 8-12 years with typically developing children. Results showed that children with ID had less secure attachment representations than controls of the same chronological age (8-12 years old) but did not differ from controls of the same mental age (4-6 years old). They also that children with ID had more disorganized attachment representations than controls of the same chronological age or of the same mental age.

Concerning security, results involving the ID group may at first suggest that security scores vary according to mental age given that a significant difference was found with typically developing children of the same age but not with those of the same mental age. It must noted however that the mean score for the control group of the same mental age was intermediate to that for the control group of the same chronological age and that for the ID group and was not significantly different from either. The fact that no difference was found between the two control groups thus invalidates this hypothesis. This corroborates the assumption that other factors, such as contextual factors [START_REF] Schuengel | Attachment, intellectual disabilities and mental health: Research, assessment and intervention[END_REF], may be involved in the difference in security between children with ID and typically developing children of the same age. In particular, Feniger-Schaal and Joels (2018) showed that maternal sensitivity was negatively associated with security in infants with ID. Likewise, lack of caregiver sensitivity may lead to greater insecurity in the school years as well.

Results concerning disorganization are unequivocal as children with ID obtained scores that were higher than those of the two control groups, whereas the two latter did not differ from one another. This finding is consistent with previous studies [START_REF] Atkinson | Maternal sensitivity, child functional level, and attachment in Down syndrome[END_REF][START_REF] Feniger-Schaal | Attachment quality of children with ID and its link to maternal sensitivity and structuring[END_REF][START_REF] Vaughn | Quality of toddler-mother attachment in children with Down syndrome: Limits to interpretation of strange situation behavior[END_REF] showing more disorganized or unclassifiable attachment behavior patterns among infants and preschoolers with ID (14-75 months). Interestingly, disorganization at the level of representation in our sample of children with ID was negatively associated with adaptive functioning. The disorganization scale is characterized by an inability to find solutions for the story beginnings. Perhaps then, below a minimum level of adaptive functioning, children with ID have more difficulty solving stressful situations. Of the three Vineland sub-scores, only the daily living skills sub-score was related to disorganization. This subscale reflects the person's level of autonomy in daily life and is composed of items related to taking care of oneself (e.g., eating, dressing, taking care of one's appearance), taking care of one's home (e.g., being careful with hot things, putting away one's belongings, feeding animals) and living in the community (e.g., making phone calls, understanding rules, laws, safety, understanding the value of money, understanding how a clock works etc.). It could have been expected that the other two Vineland subscales relative to quality of communication and quality of socialization be linked to quality of attachment because attachment involves intersubjective emotional sharing between children and their caregivers [START_REF] Atkinson | Maternal sensitivity, child functional level, and attachment in Down syndrome[END_REF].

The association between level of adaptive functioning and disorganized attachment may be interpreted as follows: Disorganized attachment representations may contribute to maladaptive social behaviors and thus hinder the development of adaptive functioning. Insecure attachment is associated with sub-optimal socio-emotional development [START_REF] Girard | La sécurité d'attachement durant la deuxième année de vie en tant que facteur prédictif des habiletés sociales en milieu scolaire[END_REF][START_REF] Groh | Attachment in the early life course: Meta-analytic evidence for its role in socioemotional development[END_REF]. Notably disorganized children eventually have more behavior problems [START_REF] Mccartney | Testing a maternal attachment model of behavior problems in early childhood[END_REF]NICHD, 2006). Knowing that people with ID are at greater risk for emotional and behavioral problems [START_REF] Emerson | Prevalence of psychiatric disorders in children and adolescents with and without intellectual disability[END_REF], more studies are needed to investigate whether insecure or disorganized attachment account for this increased risk.

Environmental factors may also explain the link between attachment and level of adaptive functioning. It is likely that families in which disorganized attachment develops provide poor support for adaptive development as well. Adjusting to the needs of children with ID can be challenging and requires the provision of interactions which are neither too controlling, nor under-stimulating or lacking constant responsiveness. Inadequate co-adaptive processes and affective communication errors may lead to disorganized attachment [START_REF] Beebe | On the origins of disorganized attachment and internal working models: Paper II. An empirical microanalysis of 4-month mother-Infant interaction[END_REF][START_REF] Lyons-Ruth | Chapter IV. Maternal frightened, frightening, or atypical behavior and disorganized infant attachment patterns[END_REF][START_REF] Solomon | The disorganized attachment-caregiving system: Dysregulation of adaptive processes at multiple levels[END_REF] and contribute to limit the development of adaptive skills. Little is known about the way environmental factors impact both attachment and adaptive functioning in children with ID. More research is needed to determine the specific factors at play and whether those identified among typically developing children also apply to children with ID.

Although the present study established a link between level of adaptive functioning and attachment, no relationship was found with IQ. It is noteworthy that most of the children with Down syndrome from our sample had very low scores on the WISC-4 (the lowest score on the WISC-4 is 35 whereas the mean score of the DS sample was 36). Thus, it is possible that the failure to reveal an effect was related to a floor effect and insufficient sensitivity of the IQ measure. The study of a link between cognitive resources and attachment would require further investigation using an instrument that makes it possible to discriminate more finely the levels of overall cognitive functioning of children with ID. Moreover, during the interviews, we observed that children with ID whose attachment was disorganized often showed perseverations in the various assessments (e.g., repeating the same action during the ASCT, always pointing to the picture proposed last in a reasoning test where one must choose one answer among several ones). These perseverations indicate lack of cognitive flexibility, which may impact children's ability to adapt to attachment-related situations and develop organized attachment strategies. Some studies show that executive functions are often highly impaired in children with ID [START_REF] Carney | Executive function in Williams and Down syndromes[END_REF][START_REF] Daunhauer | Profiles of everyday executive functioning in young children with Down syndrome[END_REF] and are associated with adaptive behavior [START_REF] Sabat | Different abilities needed at home and school: The relation between executive function and adaptive behaviour in adolescents with Down syndrome[END_REF]. Future studies that include a specific assessment of executive functions could be useful to determine whether lack of cognitive flexibility could be a specific risk factor for disorganization among children with ID.

Attachment and etiology of ID

In order to ascertain that the results from this study accurately reflect the mutual influence between ID and attachment rather than the effect of a confounding factor related to the etiology of ID (i.e. genetic syndrome), attachment security and disorganization scores of children with DS were compared to those of children with non-specific ID. No significant differences were found between the two groups, thus further confirming the role of ID per se in explaining the specifics of attachment among children with ID.

ASCT: a valid test to assess attachment within children with ID?

Pipp-Siegel, Siegel, and Dean (1999) have shown that some signs of attachment disorganization during the SSP could reflect neurological impairments rather than actual attachment-related behaviors, this raises the question of the validity of the disorganization scale of the SSP for children with ID. Likewise, in the present study, the question arises as to whether certain verbal and non-verbal behaviors that characterize play among children with ID during the ASCT actually reflect neurocognitive limitations rather than attachment questioning the validity of the ASCT to assess attachment representations among children with ID.

A preliminary qualitative analysis of the stories of the 30 children with DS [START_REF] Vanwalleghem | Peut-on parler d'erreurs dans les histoires d'attachement `a compl´eter[END_REF]) highlighted low verbal emotional expressivity among all children, both secure and insecure. This parallels the results of [START_REF] Cicchetti | Interplay among behavioral systems: Illustrations from the study of attachment, affiliation, and wariness in young children with Down's syndrome[END_REF]: during the SSP, children with DS expressed their distress less intensely than control children, but the organization and sequence of their responses were comparable to those of controls. Similarly, during the ASCT, in spite of low verbal emotional expressivity, security signs appeared through structured, consistent stories, where solutions were provided to the problems presented. Regarding the dimension of disorganization, children with more disorganized representations showed distractibility, perseverations, inattention, or lack of inhibition. These manifestations may be the expression of disorganized attachment patterns or dysexecutive disorders: their indeterminate nature further questions the validity of the disorganization scale for children with ID. However, children also exhibited other specific signs of disorganization, such as lack of narrative coherence. Neurocognitive deficits may have increased the intensity of disorganization and conversely, disorganization may have increased the expression of attention and executive disturbances, which are frequent among children with DS [START_REF] Pritchard | Executive functions among youth with Down syndrome and co-existing neurobehavioural disorders[END_REF]. Given that children's narratives enable discrimination of different response patterns reflecting attachment, including secure and disorganized attachment representations in children with DS, the ASCT seems appropriate to assess attachment representations un these children. However, further research is needed to test the validity of the disorganization scale, particularly with children with ID, by testing convergent validity and the nomological network that includes known precursors of attachment disorganization.

The validity of the ASCT for measuring attachment representations in school-age children could also be questioned as this instrument was originally designed for children aged 3-7 years. To circumvent this problem, the stories were adapted to this age group, based on recommendations from [START_REF] Granot | Attachment security and adjustment to school in middle childhood[END_REF]. The absence of differences between the ASCT scores of the two control groups, aged 4-6 years and 8-12 years, respectively, suggests that the coding was valid for the 8-to 12-year-old group as well.

Conclusions

In conclusion, the present study showed that school-age children with ID were more vulnerable to insecure and disorganized attachment than typically developing children and this was linked to their level of adaptive functioning. More research is needed to (1) understand the factors underlying disorganized attachment representations in these children, (2) determine whether environmental factors impact both attachment and adaptive functioning and (3) whether attachment influences level of adaptive functioning, for example by increasing the risk that children with ID develop social problems as observed among children without ID [START_REF] Granqvist | Disorganized attachment in infancy: A review of the phenomenon and its implications for clinicians and policy-makers[END_REF], and (4) to confirm the validity of the ASCT for children with ID.

CRediT authorship contribution statement

Stéphanie Vanwalleghem :

 Vanwalleghem Conceptualization, Methodology, Project administration, Formal analysis, Writing-Original Draft. Raphaële Miljkovitch: Conceptualization, Methodology, Writing -Review & Editing, Supervision. Annie Vinter: Conceptualization, Review & Editing, Supervision.

Table 1

 1 BSMSS scores of children with ID, typically developing children of same mental age and of same chronological age.

		ID				Control 4-6 years			Control 8-12 years
		M	SD	Min	Max	M	SD	Min	Max	M	SD	Min	Max
	BSMSS	29.3	21.8	8.0	66.0	43.9	12.2	19.0	66.0	42.5	16.7	8.0	66.0

Note. BSMSS = socio-economic status score; ID = Intellectual Disability.

Table 2

 2 BSMSS scores of children with Down Syndrome and children with non-specific ID.

	DS

Table 3

 3 ASCT scores of children with ID, typically developing children of same mental age and of same chronological age.

		ID				Control 4-6 years			Control 8-12 years
		M	SD	Min	Max	M	SD	Min	Max	M	SD	Min	Max
	Secure	46.8	13.2	18.8	66.1	51.5	15.1	10.7	66.1	54.0	8.1	34.9	68.1
	Disorganized	57.0	16.8	33.2	92.7	47.3	12.3	32.8	76.5	44.2	5.9	35.3	73.4

Note. ASCT = Attachment Story Completion Task; ID = Intellectual Disability.

Table 4

 4 Partial correlations between ASCT secure and disorganized dimensions with IQs and VINELAND-II scores, controlled by BSMSS, for participants with ID.Note. ASCT = Attachment Story Completion Task; IQs = Intellectual Quotient short form; Composite = Adaptive Behaviour Composite.

		WISC-4	VINELAND-2
	ASCT	IQs	Composite	Communication	Daily Living Skills	Socialization
	Secure	.02	.20	.11	.14	.14
	Disorganized	-.04	-.31*	-.15	-.29*	-.16

* = p < .05.

Acknowledgements

There was no primary funders nor grants for this research. The Institut Lejeune and the Acodège association supported this research by informing families who met the study's inclusion criteria that they might participate in the study.

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Declaration of Competing Interest

None.