Sociability Deficits and Altered Amygdala Circuits in Mice Lacking Pcdh10, an Autism Associated Gene

Schoch, Hannah; Kreibich, Arati S.; Ferri, Sarah L.; White, Rachel S.; Bohorquez, Dominique; Banerjee, Anamika; Port, Russell G.; Dow, Holly C.; Cordero, Lucero; Pallathra, Ashley A.; Kim, Hyong; Li, Hongzhe; Bilker, Warren B.; Hirano, Shinji; Schultz, Robert T.; Borgmann-Winter, Karin; Hahn, Chang-Gyu; Feldmeyer, Dirk; Carlson, Gregory C.; Abel, Ted; Brodkin, Edward S.

doi:10.1016/j.biopsych.2016.06.008

Cited by 92Autism Spectrum Disorder ResearchGenetics and Neurodevelopmental DisordersNeuroscience and Neuropharmacology Research

Sociability Deficits and Altered Amygdala Circuits in Mice Lacking Pcdh10, an Autism Associated Gene

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Schoch, Hannah, Kreibich, Arati S., Ferri, Sarah L., White, Rachel S., Bohorquez, Dominique, Banerjee, Anamika, Port, Russell G., Dow, Holly C., Cordero, Lucero, Pallathra, Ashley A., Kim, Hyong, Li, Hongzhe, Bilker, Warren B., Hirano, Shinji, Schultz, Robert T., Borgmann-Winter, Karin, Hahn, Chang-Gyu, Feldmeyer, Dirk, Carlson, Gregory C., Abel, Ted, Brodkin, Edward S.·2017·Biological Psychiatry

DOI 10.1016/j.biopsych.2016.06.008PMC PMC5161717

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Abstract

Background Behavioral symptoms in individuals with autism spectrum disorder (ASD) have been attributed to abnormal neuronal connectivity, but the molecular bases of these behavioral and brain phenotypes are largely unknown. Human genetic studies have implicated PCDH10, a member of the δ2 subfamily of nonclustered protocadherin genes, in ASD. PCDH10 expression is enriched in the basolateral amygdala, a brain region implicated in the social deficits of ASD. Previous reports indicate that Pcdh10 plays a role in axon outgrowth and glutamatergic synapse elimination, but its roles in social behaviors and amygdala neuronal connectivity are unknown. We hypothesized that haploinsufficiency of Pcdh10 would reduce social approach behavior and alter the structure and function of amygdala circuits. Methods Mice lacking one copy of Pcdh10 (Pcdh10+/-) and wild-type littermates were assessed for social approach and other behaviors. The lateral/basolateral amygdala was assessed for dendritic spine number and morphology, and amygdala circuit function was studied using voltage-sensitive dye imaging. Expression of Pcdh10 and N-methyl-D-aspartate receptor (NMDAR) subunits was assessed in postsynaptic density fractions of the amygdala. Results Male Pcdh10+/- mice have reduced social approach behavior, as well as impaired gamma synchronization, abnormal spine morphology, and reduced levels of NMDAR subunits in the amygdala. Social approach deficits in Pcdh10+/- male mice were rescued with acute treatment with the NMDAR partial agonist d-cycloserine. Conclusions Our studies reveal that male Pcdh10+/- mice have synaptic and behavioral deficits, and establish Pcdh10+/- mice as a novel genetic model for investigating neural circuitry and behavioral changes relevant to ASD.

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Vehicle-treated mice exhibited behavior statistically equivalent to historical never-injected control mice for social preference at ~PN30 and 24 hr fear memory at ~PN60.
“veh-treated mice exhibited behavior statistically equivalent to historical data of ours with mice that were undisturbed as neonates (no neonatal injection)”
From Excess Neonatal Testosterone Causes Male-Specific Social and Fear Memory Deficits in Wild-Type Mice (2025) · cites this paper as Schoch et al., 2017
The Methods and Materials > Behavior section describes social-approach testing at 28–32 days and a separate cohort injected with saline or d-cycloserine 30 minutes before testing. Our copy does not report a statistical comparison with historical never-injected mice, neonatal vehicle injections, or 24-hour fear memory at approximately PN60 (searched those terms and their paraphrases). (LLM, conf=0.77)
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Suppression of Sprouting: An Early Function of NMDA Receptors in the Absence of AMPA/Kainate Receptor Activity
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Gamma Activation in Young People with Autism Spectrum Disorders and Typically-Developing Controls When Viewing Emotions on Faces
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d-Cycloserine improves sociability in the BTBR T+ Itpr3tf/J mouse model of autism spectrum disorders with altered Ras/Raf/ERK1/2 signaling
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Distribution of OL-protocadherin protein in correlation with specific neural compartments and local circuits in the postnatal mouse brain
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Development of home cage social behaviors in BALB/cJ vs. C57BL/6J mice
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Rapid WAVE dynamics in dendritic spines of cultured hippocampal neurons is mediated by actin polymerization
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Emotion-elicited gamma synchrony in patients with first-episode schizophrenia: a neural correlate of social cognition outcomes
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Deconstructing Sociability, An Autism‐Relevant Phenotype, in Mouse Models
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“…as neonates (no neonatal injection); both social preference indices at ∼ PN30 and 24 h fear memory results at ∼ PN60 were comparable between mice administered veh and never-injected control mice we have collected over various experiments (Schoch et al., 2017; Ferri et al., 2016, 2020, 2021).”
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Review of: "Excitatory synapses and gap junctions cooperate to improve Pv neuronal burst firing and cortical social cognition in Shank2-mutant mice"
Aroniadou‐Anderjaska, V. (2021) · doi:10.32388/dqegpk
Additional file 16 of Innovative mouse models for the tumor suppressor activity of Protocadherin-10 isoforms
Kleinberger, I., Sanders, E., Staes, K., Troys, M. V., Hirano, S., Hochepied, T., Lemeire, K., Martens, L., Ampè, C., & Van Roy, F. (2022) · Figshare · doi:10.6084/m9.figshare.19654314
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Additional file 31 of Innovative mouse models for the tumor suppressor activity of Protocadherin-10 isoforms
Kleinberger, I., Sanders, E., Staes, K., Troys, M. V., Hirano, S., Hochepied, T., Lemeire, K., Martens, L., Ampè, C., & Van Roy, F. (2022) · Figshare · doi:10.6084/m9.figshare.19654371
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Additional file 24 of Innovative mouse models for the tumor suppressor activity of Protocadherin-10 isoforms
Kleinberger, I., Sanders, E., Staes, K., Troys, M. V., Hirano, S., Hochepied, T., Lemeire, K., Martens, L., Ampè, C., & Van Roy, F. (2022) · Figshare · doi:10.6084/m9.figshare.19654341
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Additional file 6 of Innovative mouse models for the tumor suppressor activity of Protocadherin-10 isoforms
Kleinberger, I., Sanders, E., Staes, K., Troys, M. V., Hirano, S., Hochepied, T., Lemeire, K., Martens, L., Ampè, C., & Van Roy, F. (2022) · Figshare · doi:10.6084/m9.figshare.19654413
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Additional file 14 of Innovative mouse models for the tumor suppressor activity of Protocadherin-10 isoforms
Kleinberger, I., Sanders, E., Staes, K., Troys, M. V., Hirano, S., Hochepied, T., Lemeire, K., Martens, L., Ampè, C., & Van Roy, F. (2022) · Figshare · doi:10.6084/m9.figshare.19654308
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Additional file 7 of Innovative mouse models for the tumor suppressor activity of Protocadherin-10 isoforms
Kleinberger, I., Sanders, E., Staes, K., Troys, M. V., Hirano, S., Hochepied, T., Lemeire, K., Martens, L., Ampè, C., & Van Roy, F. (2022) · Figshare · doi:10.6084/m9.figshare.19654416
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Additional file 30 of Innovative mouse models for the tumor suppressor activity of Protocadherin-10 isoforms
Kleinberger, I., Sanders, E., Staes, K., Troys, M. V., Hirano, S., Hochepied, T., Lemeire, K., Martens, L., Ampè, C., & Van Roy, F. (2022) · Figshare · doi:10.6084/m9.figshare.19654365
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Additional file 32 of Innovative mouse models for the tumor suppressor activity of Protocadherin-10 isoforms
Kleinberger, I., Sanders, E., Staes, K., Troys, M. V., Hirano, S., Hochepied, T., Lemeire, K., Martens, L., Ampè, C., & Van Roy, F. (2022) · Figshare · doi:10.6084/m9.figshare.19654377
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Additional file 22 of Innovative mouse models for the tumor suppressor activity of Protocadherin-10 isoforms
Kleinberger, I., Sanders, E., Staes, K., Troys, M. V., Hirano, S., Hochepied, T., Lemeire, K., Martens, L., Ampè, C., & Van Roy, F. (2022) · Figshare · doi:10.6084/m9.figshare.19654335
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Additional file 12 of Innovative mouse models for the tumor suppressor activity of Protocadherin-10 isoforms
Kleinberger, I., Sanders, E., Staes, K., Troys, M. V., Hirano, S., Hochepied, T., Lemeire, K., Martens, L., Ampè, C., & Van Roy, F. (2022) · Figshare · doi:10.6084/m9.figshare.19654302
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Additional file 27 of Innovative mouse models for the tumor suppressor activity of Protocadherin-10 isoforms
Kleinberger, I., Sanders, E., Staes, K., Troys, M. V., Hirano, S., Hochepied, T., Lemeire, K., Martens, L., Ampè, C., & Van Roy, F. (2022) · Figshare · doi:10.6084/m9.figshare.19654350
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Additional file 23 of Innovative mouse models for the tumor suppressor activity of Protocadherin-10 isoforms
Kleinberger, I., Sanders, E., Staes, K., Troys, M. V., Hirano, S., Hochepied, T., Lemeire, K., Martens, L., Ampè, C., & Van Roy, F. (2022) · Figshare · doi:10.6084/m9.figshare.19654338
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Additional file 29 of Innovative mouse models for the tumor suppressor activity of Protocadherin-10 isoforms
Kleinberger, I., Sanders, E., Staes, K., Troys, M. V., Hirano, S., Hochepied, T., Lemeire, K., Martens, L., Ampè, C., & Van Roy, F. (2022) · Figshare · doi:10.6084/m9.figshare.19654356
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Additional file 19 of Innovative mouse models for the tumor suppressor activity of Protocadherin-10 isoforms
Kleinberger, I., Sanders, E., Staes, K., Troys, M. V., Hirano, S., Hochepied, T., Lemeire, K., Martens, L., Ampè, C., & Van Roy, F. (2022) · Figshare · doi:10.6084/m9.figshare.19654323
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Additional file 18 of Innovative mouse models for the tumor suppressor activity of Protocadherin-10 isoforms
Kleinberger, I., Sanders, E., Staes, K., Troys, M. V., Hirano, S., Hochepied, T., Lemeire, K., Martens, L., Ampè, C., & Van Roy, F. (2022) · Figshare · doi:10.6084/m9.figshare.19654320
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Additional file 3 of Innovative mouse models for the tumor suppressor activity of Protocadherin-10 isoforms
Kleinberger, I., Sanders, E., Staes, K., Troys, M. V., Hirano, S., Hochepied, T., Lemeire, K., Martens, L., Ampè, C., & Van Roy, F. (2022) · Figshare · doi:10.6084/m9.figshare.19654401
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Additional file 17 of Innovative mouse models for the tumor suppressor activity of Protocadherin-10 isoforms
Kleinberger, I., Sanders, E., Staes, K., Troys, M. V., Hirano, S., Hochepied, T., Lemeire, K., Martens, L., Ampè, C., & Van Roy, F. (2022) · Figshare · doi:10.6084/m9.figshare.19654317
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Additional file 35 of Innovative mouse models for the tumor suppressor activity of Protocadherin-10 isoforms
Kleinberger, I., Sanders, E., Staes, K., Troys, M. V., Hirano, S., Hochepied, T., Lemeire, K., Martens, L., Ampè, C., & Van Roy, F. (2022) · Figshare · doi:10.6084/m9.figshare.19654395
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Additional file 25 of Innovative mouse models for the tumor suppressor activity of Protocadherin-10 isoforms
Kleinberger, I., Sanders, E., Staes, K., Troys, M. V., Hirano, S., Hochepied, T., Lemeire, K., Martens, L., Ampè, C., & Van Roy, F. (2022) · Figshare · doi:10.6084/m9.figshare.19654344
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Additional file 33 of Innovative mouse models for the tumor suppressor activity of Protocadherin-10 isoforms
Kleinberger, I., Sanders, E., Staes, K., Troys, M. V., Hirano, S., Hochepied, T., Lemeire, K., Martens, L., Ampè, C., & Van Roy, F. (2022) · Figshare · doi:10.6084/m9.figshare.19654383
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Additional file 4 of Innovative mouse models for the tumor suppressor activity of Protocadherin-10 isoforms
Kleinberger, I., Sanders, E., Staes, K., Troys, M. V., Hirano, S., Hochepied, T., Lemeire, K., Martens, L., Ampè, C., & Van Roy, F. (2022) · Figshare · doi:10.6084/m9.figshare.19654404
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Additional file 20 of Innovative mouse models for the tumor suppressor activity of Protocadherin-10 isoforms
Kleinberger, I., Sanders, E., Staes, K., Troys, M. V., Hirano, S., Hochepied, T., Lemeire, K., Martens, L., Ampè, C., & Van Roy, F. (2022) · Figshare · doi:10.6084/m9.figshare.19654329
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Additional file 26 of Innovative mouse models for the tumor suppressor activity of Protocadherin-10 isoforms
Kleinberger, I., Sanders, E., Staes, K., Troys, M. V., Hirano, S., Hochepied, T., Lemeire, K., Martens, L., Ampè, C., & Van Roy, F. (2022) · Figshare · doi:10.6084/m9.figshare.19654347
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Additional file 5 of Innovative mouse models for the tumor suppressor activity of Protocadherin-10 isoforms
Kleinberger, I., Sanders, E., Staes, K., Troys, M. V., Hirano, S., Hochepied, T., Lemeire, K., Martens, L., Ampè, C., & Van Roy, F. (2022) · Figshare · doi:10.6084/m9.figshare.19654410
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Additional file 21 of Innovative mouse models for the tumor suppressor activity of Protocadherin-10 isoforms
Kleinberger, I., Sanders, E., Staes, K., Troys, M. V., Hirano, S., Hochepied, T., Lemeire, K., Martens, L., Ampè, C., & Van Roy, F. (2022) · Figshare · doi:10.6084/m9.figshare.19654332
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Additional file 15 of Innovative mouse models for the tumor suppressor activity of Protocadherin-10 isoforms
Kleinberger, I., Sanders, E., Staes, K., Troys, M. V., Hirano, S., Hochepied, T., Lemeire, K., Martens, L., Ampè, C., & Van Roy, F. (2022) · Figshare · doi:10.6084/m9.figshare.19654311
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Additional file 1 of Innovative mouse models for the tumor suppressor activity of Protocadherin-10 isoforms
Kleinberger, I., Sanders, E., Staes, K., Troys, M. V., Hirano, S., Hochepied, T., Lemeire, K., Martens, L., Ampè, C., & Van Roy, F. (2022) · Figshare · doi:10.6084/m9.figshare.19654326
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Additional file 28 of Innovative mouse models for the tumor suppressor activity of Protocadherin-10 isoforms
Kleinberger, I., Sanders, E., Staes, K., Troys, M. V., Hirano, S., Hochepied, T., Lemeire, K., Martens, L., Ampè, C., & Van Roy, F. (2022) · Figshare · doi:10.6084/m9.figshare.19654353
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Additional file 2 of Innovative mouse models for the tumor suppressor activity of Protocadherin-10 isoforms
Kleinberger, I., Sanders, E., Staes, K., Troys, M. V., Hirano, S., Hochepied, T., Lemeire, K., Martens, L., Ampè, C., & Van Roy, F. (2022) · Figshare · doi:10.6084/m9.figshare.19654362
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Additional file 8 of Innovative mouse models for the tumor suppressor activity of Protocadherin-10 isoforms
Kleinberger, I., Sanders, E., Staes, K., Troys, M. V., Hirano, S., Hochepied, T., Lemeire, K., Martens, L., Ampè, C., & Van Roy, F. (2022) · Figshare · doi:10.6084/m9.figshare.19654419
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Additional file 13 of Innovative mouse models for the tumor suppressor activity of Protocadherin-10 isoforms
Kleinberger, I., Sanders, E., Staes, K., Troys, M. V., Hirano, S., Hochepied, T., Lemeire, K., Martens, L., Ampè, C., & Van Roy, F. (2022) · Figshare · doi:10.6084/m9.figshare.19654305
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Additional file 34 of Innovative mouse models for the tumor suppressor activity of Protocadherin-10 isoforms
Kleinberger, I., Sanders, E., Staes, K., Troys, M. V., Hirano, S., Hochepied, T., Lemeire, K., Martens, L., Ampè, C., & Van Roy, F. (2022) · Figshare · doi:10.6084/m9.figshare.19654389
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Protocadherin 10, a member of cadherin superfamily, increases stress-susceptibility in chronic unpredictable stress-treated rats
Li, X.-M., Zhang, N., Zhang, X.-L., Liu, N., Xia, C., Yang, X., Wang, H., Xu, Y., Chu, S.-F., Chen, N., et al. (2026) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2026.174158
Canalization of neural dynamics by δ-protocadherins in the developing zebrafish optic tectum
Biswas, S., Emond, M. R., Philip, G. S., & Jontes, J. D. (2026) · PLoS Genetics · doi:10.1371/journal.pgen.1012171
Nonclustered Protocadherins in Autism: Integrating Cell Adhesion and Activity-Dependent Signalling
Miozzo, F. (2026) · The Neuroscientist · doi:10.1177/10738584261457052

WHY PROTOCADHERIN11XY (PCDH11XY) AND NO OTHER GENE WILL EXPLAIN THE SEX DIFFERENCES IN PSYCHOSIS
Crow, T. J. (2010) · Schizophrenia Research · doi:10.1016/j.schres.2010.02.872
Age- and sex-specific fear conditioning deficits in mice lacking Pcdh10, an Autism Associated Gene
Ferri, S. L., Dow, H. C., Schoch, H., Lee, J. Y., Brodkin, E. S., & Abel, T. (2021) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2020.107364 · Cited by 51 · see citing works
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ASD/OCD-Linked Protocadherin-10 Regulates Synapse, But Not Axon, Development in the Amygdala and Contributes to Fear- and Anxiety-Related Behaviors
Hoshina, N., Johnson-Venkatesh, E. M., Rally, V. R., Sant, J., Hoshina, M., Seiglie, M. P., & Umemori, H. (2022) · Journal of Neuroscience · doi:10.1523/jneurosci.1843-21.2022 · Cited by 19 · see citing works
Dynamic connectivity analysis of selective serotonin reuptake inhibitor effects, a pharmacological PET/MR study
Gryglewski, G., Hahn, A. K., Berroterán-Infante, N., Klöbl, M., Klebermass, E., Hienert, M., Pichler, V., Vanicek, T., Nics, L., Rischka, L., et al. (2017) · European Neuropsychopharmacology · doi:10.1016/s0924-977x(17)31460-8
Protocadherin 10 alters γ oscillations, amino acid levels, and their coupling; baclofen partially restores these oscillatory deficits
Port, R. G., Gajewski, C. R., Krizman, E. N., Dow, H. C., Hirano, S., Brodkin, E. S., Carlson, G. C., Robinson, M. B., Roberts, T. P. L., & Siegel, S. J. (2017) · Neurobiology of Disease · doi:10.1016/j.nbd.2017.08.013 · Cited by 54 · see citing works
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Authors: Schoch, H., Kreibich, A. S., Ferri, S. L., White, R. S., Bohorquez, D., Banerjee, A., Port, R. G., Dow, H. C., Cordero, L., Pallathra, A. A., Kim, H., Li, H., Bilker, W. B., Hirano, S., Schultz, R. T., Borgmann-Winter, K., Hahn, C.-G., Feldmeyer, D., Carlson, G. C., Abel, T., & Brodkin, E. S.
Affiliations: University of Pennsylvania (US)
Kansai Medical University (JP)
Children's Hospital of Philadelphia (US)
Forschungszentrum Jülich (DE)
Corresponding author: Brodkin, Edward S.
ORCID: Schoch, Hannah
Ferri, Sarah L.
White, Rachel S.
Bohorquez, Dominique
Banerjee, Anamika
Port, Russell G.
Dow, Holly C.
Pallathra, Ashley A.
Li, Hongzhe
Bilker, Warren B.
Hirano, Shinji
Schultz, Robert T.
Feldmeyer, Dirk
Abel, Ted
Brodkin, Edward S.
Venue: Biological Psychiatry
Publisher: Elsevier BV
Published: 2017-02
Volume: 81
Issue: 3
Pages: 193-202
ISSN: 0006-3223 (ISSN-L)
DOI: 10.1016/j.biopsych.2016.06.008
PMC: PMC5161717
OpenAlex: W2433184682
Cited by: 92
References: 82
Citations by year: 2026: 4 · 2025: 5 · 2024: 3 · 2023: 5 · 2022: 38 · 2021: 8 · 2020: 7 · 2019: 5 · 2018: 9 · 2017: 6 · 2016: 2
FWCI: 4.67
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Biological Psychiatry (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
RWTH Publications (RWTH Aachen) (submittedVersion)
Funders: Pennsylvania Department of Health
National Institutes of Health (5t32mh017168-34)
Johnson and Johnson
National Institute of Mental Health (P50MH096891, R01MH080718, T32 MH-017168)
National Institute of Neurological Disorders and Stroke (T32NS007413)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Autism Spectrum Disorder Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords: PCDH10, autism spectrum disorder, social approach behavior, social dysfunction, basolateral amygdala, dendritic spines, NMDA receptor subunits, gamma oscillations, D-cycloserine, haploinsufficiency, mouse model, glutamatergic synapses, neuronal connectivity
MeSH terms: Autism Spectrum Disorder, Protocadherins, Amygdala, Animals, Behavior, Animal, Disease Models, Animal, Electric Stimulation, Female, Male, Mice, Inbred C57BL, Mice, Mutant Strains, Nerve Tissue Proteins, Social Behavior, Vocalization, Animal, Cadherins, Receptors, N-Methyl-D-Aspartate, Dendritic Spines, Mice, Haploinsufficiency, Post-Synaptic Density, Gamma Rhythm

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Sociability Deficits and Altered Amygdala Circuits in Mice Lacking Pcdh10, an Autism Associated Gene

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