Concerted roles of LRRTM1 and SynCAM 1 in organizing prefrontal cortex synapses and cognitive functions

Karen Perez Arce, Adema Ribic, Dhrubajyoti Chowdhury, Katherine Watters, Garth J. Thompson, Basavaraju G. Sanganahalli, Elizabeth T. C. Lippard, Astrid Rohlmann, Stephen M. Strittmatter, Markus Missler, Fahmeed Hyder and Thomas Biederer ()
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Karen Perez Arce: Tufts University School of Medicine
Adema Ribic: Tufts University School of Medicine
Dhrubajyoti Chowdhury: Yale School of Medicine
Katherine Watters: Tufts University School of Medicine
Garth J. Thompson: Yale School of Medicine
Basavaraju G. Sanganahalli: Yale School of Medicine
Elizabeth T. C. Lippard: Yale School of Medicine
Astrid Rohlmann: Westfälische Wilhelms-University
Stephen M. Strittmatter: Yale School of Medicine
Markus Missler: Westfälische Wilhelms-University
Fahmeed Hyder: Yale School of Medicine
Thomas Biederer: Tufts University School of Medicine

Nature Communications, 2023, vol. 14, issue 1, 1-18

Abstract: Abstract Multiple trans-synaptic complexes organize synapse development, yet their roles in the mature brain and cooperation remain unclear. We analyzed the postsynaptic adhesion protein LRRTM1 in the prefrontal cortex (PFC), a region relevant to cognition and disorders. LRRTM1 knockout (KO) mice had fewer synapses, and we asked whether other synapse organizers counteract further loss. This determined that the immunoglobulin family member SynCAM 1 controls synapse number in PFC and was upregulated upon LRRTM1 loss. Combined LRRTM1 and SynCAM 1 deletion substantially lowered dendritic spine number in PFC, but not hippocampus, more than the sum of single KO impairments. Their cooperation extended presynaptically, and puncta of Neurexins, LRRTM1 partners, were less abundant in double KO (DKO) PFC. Electrophysiology and fMRI demonstrated aberrant neuronal activity in DKO mice. Further, DKO mice were impaired in social interactions and cognitive tasks. Our results reveal concerted roles of LRRTM1 and SynCAM 1 across synaptic, network, and behavioral domains.

Date: 2023
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DOI: 10.1038/s41467-023-36042-w

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