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

Biol Psychiatry. 2017 Feb 1;81(3):193-202. doi: 10.1016/j.biopsych.2016.06.008. Epub 2016 Jun 16.

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.

Keywords: Amygdala; Autism; Gene; NMDA; Protocadherin; Synapse.

MeSH terms

  • Amygdala / metabolism
  • Amygdala / pathology
  • Amygdala / physiopathology*
  • Animals
  • Autism Spectrum Disorder / genetics*
  • Autism Spectrum Disorder / physiopathology*
  • Autism Spectrum Disorder / psychology
  • Behavior, Animal / physiology
  • Cadherins / genetics
  • Cadherins / physiology*
  • Dendritic Spines / pathology
  • Disease Models, Animal
  • Electric Stimulation
  • Female
  • Gamma Rhythm
  • Haploinsufficiency
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Mutant Strains
  • Nerve Tissue Proteins / metabolism
  • Post-Synaptic Density / metabolism
  • Protocadherins
  • Receptors, N-Methyl-D-Aspartate / metabolism
  • Receptors, N-Methyl-D-Aspartate / physiology
  • Social Behavior*
  • Vocalization, Animal

Substances

  • Cadherins
  • Gprin1 protein, mouse
  • Nerve Tissue Proteins
  • Pcdh10 protein, mouse
  • Protocadherins
  • Receptors, N-Methyl-D-Aspartate
  • N-methyl D-aspartate receptor subtype 2A