Changes in the Proportion of Inhibitory Interneuron Types from Sensory to Executive Areas of the Primate Neocortex: Implications for the Origins of Working Memory Representations

Santiago Torres-Gomez, Jackson D. Blonde, Diego Mendoza-Halliday, Eric Kuebler, Michelle Everest, Xiao Jing Wang, Wataru Inoue, Michael O. Poulter, Julio Martinez-Trujillo

Research output: Contribution to journalArticlepeer-review

Abstract

Neuronal spiking activity encoding working memory (WM) is robust in primate association cortices but weak or absent in early sensory cortices. This may be linked to changes in the proportion of neuronal types across areas that influence circuits' ability to generate recurrent excitation. We recorded neuronal activity from areas middle temporal (MT), medial superior temporal (MST), and the lateral prefrontal cortex (LPFC) of monkeys performing a WM task and classified neurons as narrow (NS) and broad spiking (BS). The ratio NS/BS decreased from MT > MST > LPFC. We analyzed the Allen Institute database of ex vivo mice/human intracellular recordings to interpret our data. Our analysis suggests that NS neurons correspond to parvalbumin (PV) or somatostatin (SST) interneurons while BS neurons are pyramidal (P) cells or vasoactive intestinal peptide (VIP) interneurons. We labeled neurons in monkey tissue sections of MT/MST and LPFC and found that the proportion of PV in cortical layers 2/3 decreased, while the proportion of CR cells increased from MT/MST to LPFC. Assuming that primate CR/CB/PV cells perform similar computations as mice VIP/SST/PV cells, our results suggest that changes in the proportion of CR and PV neurons in layers 2/3 cells may favor the emergence of activity encoding WM in association areas.

Original languageEnglish (US)
Pages (from-to)4544-4562
Number of pages19
JournalCerebral Cortex
Volume30
Issue number8
DOIs
StatePublished - Jun 30 2020

Keywords

  • CR interneurons
  • PV interneurons
  • inhibition-excitation balance
  • medial superior temporal
  • middle temporal
  • narrow and broad spiking
  • prefrontal cortex
  • working memory (WM)

ASJC Scopus subject areas

  • Cognitive Neuroscience
  • Cellular and Molecular Neuroscience

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