Combined Social and Spatial Coding in a Descending Projection from the Prefrontal Cortex

Malavika Murugan, Hee Jae Jang, Michelle Park, Ellia M. Miller, Julia Cox, Joshua P. Taliaferro, Nathan F. Parker, Varun Bhave, Hong Hur, Yupu Liang, Alexander R. Nectow, Jonathan W. Pillow, Ilana B. Witten*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

210 Scopus citations

Abstract

Social behaviors are crucial to all mammals. Although the prelimbic cortex (PL, part of medial prefrontal cortex) has been implicated in social behavior, it is not clear which neurons are relevant or how they contribute. We found that PL contains anatomically and molecularly distinct subpopulations that target three downstream regions that have been implicated in social behavior: the nucleus accumbens (NAc), amygdala, and ventral tegmental area. Activation of NAc-projecting PL neurons (PL-NAc), but not the other subpopulations, decreased the preference for a social target. To determine what information PL-NAc neurons convey, we selectively recorded from them and found that individual neurons were active during social investigation, but only in specific spatial locations. Spatially specific manipulation of these neurons bidirectionally regulated the formation of a social-spatial association. Thus, the unexpected combination of social and spatial information within the PL-NAc may contribute to social behavior by supporting social-spatial learning. Prefrontal neurons that project to the accumbens encode a combination of social and spatial information and bidirectionally modulate social-spatial learning.

Original languageEnglish (US)
Pages (from-to)1663-1677.e16
JournalCell
Volume171
Issue number7
DOIs
StatePublished - Dec 14 2017

Funding

We thank B. Engelhard, S. Bolkan, and the rest of the Witten lab for comments and advice on this work; E. Kremer and E. Engel for reagents; and B. Patel for technical assistance. This work was funded by Pew , McKnight , and Sloan Foundation grants to I.B.W., the NIH ( DP2 DA035149-01 and 5R01MH106689-02 to I.B.W. and 1F32MH112320-01A1 to J.C.), SCGB ( 412733 to M.M.), NSF GRFP (to N.F.P.), NARSAD Young Investigator Awards (to A.R.N. and I.B.W.), and NCATS NIH CTSA program ( UL1 TR001866 to Y.L. and H.H.). I.B.W. is a New York Stem Cell Foundation—Robertson Investigator. J.W.P. was supported by grants from the McKnight Foundation , Simons Collaboration on the Global Brain ( SCGB AWD1004351 ), and the NSF CAREER Award ( IIS-1150186 ).

Keywords

  • calcium imaging
  • medial prefrontal cortex
  • nucleus accumbens
  • optogenetics
  • social behavior

ASJC Scopus subject areas

  • General Biochemistry, Genetics and Molecular Biology

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