Mapping of functionally characterized cell classes onto canonical circuit operations in primate prefrontal cortex

Authors

Salva Ardid, Department of Biology, Centre for Vision Research, York University, Toronto, Ontario M6J 1P3, Canada, Center for Computational Neuroscience and Neural Technology (CompNet), Department of Mathematics and Statistics, Boston University, Boston, Massachusetts 02215, sardid@bu.edu thiwom@yorku.ca.
Martin Vinck, Department of Neurobiology, Yale University School of Medicine, New Haven, Connecticut 06510, and.
Daniel Kaping, Department of Biology, Centre for Vision Research, York University, Toronto, Ontario M6J 1P3, Canada.
Susanna Marquez, Department of Biology, Centre for Vision Research, York University, Toronto, Ontario M6J 1P3, Canada.
Stefan Everling, Department of Physiology and Pharmacology, University of Western Ontario, London, Ontario N6A 5K8, Canada.
Thilo Womelsdorf, Department of Biology, Centre for Vision Research, York University, Toronto, Ontario M6J 1P3, Canada, Department of Physiology and Pharmacology, University of Western Ontario, London, Ontario N6A 5K8, Canada sardid@bu.edu thiwom@yorku.ca.

Document Type

Article

Publication Date

2-18-2015

Journal

The Journal of neuroscience : the official journal of the Society for Neuroscience

Volume

35

Issue

7

First Page

2975

Last Page

91

URL with Digital Object Identifier

10.1523/JNEUROSCI.2700-14.2015

Abstract

Microcircuits are composed of multiple cell classes that likely serve unique circuit operations. But how cell classes map onto circuit functions is largely unknown, particularly for primate prefrontal cortex during actual goal-directed behavior. One difficulty in this quest is to reliably distinguish cell classes in extracellular recordings of action potentials. Here we surmount this issue and report that spike shape and neural firing variability provide reliable markers to segregate seven functional classes of prefrontal cells in macaques engaged in an attention task. We delineate an unbiased clustering protocol that identifies four broad spiking (BS) putative pyramidal cell classes and three narrow spiking (NS) putative inhibitory cell classes dissociated by how sparse, bursty, or regular they fire. We speculate that these functional classes map onto canonical circuit functions. First, two BS classes show sparse, bursty firing, and phase synchronize their spiking to 3-7 Hz (theta) and 12-20 Hz (beta) frequency bands of the local field potential (LFP). These properties make cells flexibly responsive to network activation at varying frequencies. Second, one NS and two BS cell classes show regular firing and higher rate with only marginal synchronization preference. These properties are akin to setting tonically the excitation and inhibition balance. Finally, two NS classes fired irregularly and synchronized to either theta or beta LFP fluctuations, tuning them potentially to frequency-specific subnetworks. These results suggest that a limited set of functional cell classes emerges in macaque prefrontal cortex (PFC) during attentional engagement to not only represent information, but to subserve basic circuit operations.