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Atypical perineuronal nets in the CA2 region interfere with social memory in a mouse model of social dysfunction

Molecular Psychiatry volume 27, pages 3520–3531 (2022)Cite this article

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A Correction to this article was published on 22 April 2022

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Abstract

Social memory dysfunction is an especially devastating symptom of many neuropsychiatric disorders, which makes understanding the cellular and molecular processes that contribute to such abnormalities important. Evidence suggests that the hippocampus, particularly the CA2 region, plays an important role in social memory. We sought to identify potential mechanisms of social memory dysfunction in the hippocampus by investigating features of neurons, glia, and the extracellular matrix (ECM) of BTBR mice, an inbred mouse strain with deficient social memory. The CA2 is known to receive inputs from dentate gyrus adult-born granule cells (abGCs), neurons known to participate in social memory, so we examined this cell population and found fewer abGCs, as well as fewer axons from abGCs in the CA2 of BTBR mice compared to controls. We also found that BTBR mice had fewer pyramidal cell dendritic spines, in addition to fewer microglia and astrocytes, in the CA2 compared to controls. Along with diminished neuronal and glial elements, we found atypical perineuronal nets (PNNs), specialized ECM structures that regulate plasticity, in the CA2 of BTBR mice. By diminishing PNNs in the CA2 of BTBR mice to control levels, we observed a partial restoration of social memory. Our findings suggest that the CA2 region of BTBR mice exhibits multiple cellular and extracellular abnormalities and identify atypical PNNs as one mechanism producing social memory dysfunction, although the contribution of reduced abGC afferents, pyramidal cell dendritic spine, and glial cell numbers remains unexplored.

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Fig. 1: BTBR mice have impairments in sociability and social memory.
Fig. 2: BTBR mice have fewer mossy fibers from abGCs to the CA2.
Fig. 3: BTBR mice have a smaller CA2 region as well as fewer pyramidal cell dendritic spines, microglia, and astrocytes.
Fig. 4: BTBR mice have high WFA+ volume and intensity in the CA2 but not the vCA1.
Fig. 5: Reducing CA2 PNNs in control mice impairs social memory, while reducing PNNs in BTBR mice to control values partially rescues social memory impairment.

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Acknowledgements

This work was supported by the National Institutes of Health, NIMH 1R01 MH118631-01 to EG and NIH Training Fellowship T32MH065214 to ECC. The authors thank Biorender for assistance with the figure schematics, Sahana Murthy and Brandy A. Briones for helpful comments on the project, and Carla G. Dias, Kristen A. Pagliai, and Amelia Windorski for assistance with histological analyses.

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  1. Princeton Neuroscience Institute, Princeton University, Princeton, NJ, USA

    Elise C. Cope, Anna D. Zych, Nicole J. Katchur, Renée C. Waters, Blake J. Laham, Emma J. Diethorn, Christin Y. Park, William R. Meara & Elizabeth Gould

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Cope, E.C., Zych, A.D., Katchur, N.J. et al. Atypical perineuronal nets in the CA2 region interfere with social memory in a mouse model of social dysfunction. Mol Psychiatry 27, 3520–3531 (2022). https://doi.org/10.1038/s41380-021-01174-2

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