Spike frequency adaptation in primate lateral prefrontal cortex neurons results from interplay between intrinsic properties and circuit dynamics

Nils A Koch; Benjamin W Corrigan; Michael Feyerabend; Roberto A Gulli; Michelle S Jimenez-Sosa; Mohamad Abbass; Julia K Sunstrum; Sara Matovic; Megan Roussy; Rogelio Luna; Samuel A Mestern; Borna Mahmoudian; Susheel Vijayraghavan; Hiroyuki Igarashi; Kartik S Pradeepan; William J Assis; J Andrew Pruszynski; Shreejoy Tripathy; Jochen F Staiger; Guillermo Gonzalez-Burgos; Andreas Neef; Stefan Treue; Stefan Everling; Wataru Inoue; Anmar Khadra; Julio C Martinez-Trujillo

doi:10.1016/j.celrep.2024.115159

Spike frequency adaptation in primate lateral prefrontal cortex neurons results from interplay between intrinsic properties and circuit dynamics

Cell Rep. 2025 Jan 6;44(1):115159. doi: 10.1016/j.celrep.2024.115159. Online ahead of print.

Authors

Nils A Koch¹, Benjamin W Corrigan², Michael Feyerabend³, Roberto A Gulli⁴, Michelle S Jimenez-Sosa⁵, Mohamad Abbass⁶, Julia K Sunstrum⁷, Sara Matovic⁸, Megan Roussy⁹, Rogelio Luna¹⁰, Samuel A Mestern⁸, Borna Mahmoudian¹¹, Susheel Vijayraghavan⁹, Hiroyuki Igarashi¹², Kartik S Pradeepan¹³, William J Assis¹⁴, J Andrew Pruszynski¹³, Shreejoy Tripathy¹⁵, Jochen F Staiger¹⁶, Guillermo Gonzalez-Burgos¹⁷, Andreas Neef¹⁸, Stefan Treue¹⁹, Stefan Everling¹³, Wataru Inoue¹¹, Anmar Khadra²⁰, Julio C Martinez-Trujillo³

Affiliations

¹ Integrated Program in Neuroscience, McGill University, Montreal, QC, Canada.
² Department of Biology, York University, Toronto, ON, Canada; Department of Clinical Neurological Sciences, London Health Sciences Centre, Western University, London, ON, Canada; Department of Physiology and Pharmacology, Schulich School of Medicine and Dentistry, Western University, London, ON, Canada.
³ Department of Clinical Neurological Sciences, London Health Sciences Centre, Western University, London, ON, Canada; Department of Physiology and Pharmacology, Schulich School of Medicine and Dentistry, Western University, London, ON, Canada; Western Institute for Neuroscience, Western University, London, ON, Canada.
⁴ Integrated Program in Neuroscience, McGill University, Montreal, QC, Canada; Robarts Research Institute, University of Western Ontario, London, ON, Canada.
⁵ Robarts Research Institute, University of Western Ontario, London, ON, Canada.
⁶ Department of Clinical Neurological Sciences, London Health Sciences Centre, Western University, London, ON, Canada; Western Institute for Neuroscience, Western University, London, ON, Canada; Robarts Research Institute, University of Western Ontario, London, ON, Canada.
⁷ Western Institute for Neuroscience, Western University, London, ON, Canada; Robarts Research Institute, University of Western Ontario, London, ON, Canada; Neuroscience Graduate Program, Western University, London, ON, Canada.
⁸ Western Institute for Neuroscience, Western University, London, ON, Canada; Robarts Research Institute, University of Western Ontario, London, ON, Canada.
⁹ Department of Physiology and Pharmacology, Schulich School of Medicine and Dentistry, Western University, London, ON, Canada.
¹⁰ Department of Physiology and Pharmacology, Schulich School of Medicine and Dentistry, Western University, London, ON, Canada; Robarts Research Institute, University of Western Ontario, London, ON, Canada.
¹¹ Department of Physiology and Pharmacology, Schulich School of Medicine and Dentistry, Western University, London, ON, Canada; Western Institute for Neuroscience, Western University, London, ON, Canada; Robarts Research Institute, University of Western Ontario, London, ON, Canada.
¹² Department of Physiology and Pharmacology, Schulich School of Medicine and Dentistry, Western University, London, ON, Canada; Robarts Research Institute, University of Western Ontario, London, ON, Canada; Department of Pharmacology, Graduate School of Pharmaceutical Sciences, Tohoku University, Sendai, Miyagi, Japan.
¹³ Department of Physiology and Pharmacology, Schulich School of Medicine and Dentistry, Western University, London, ON, Canada; Western Institute for Neuroscience, Western University, London, ON, Canada.
¹⁴ Western Institute for Neuroscience, Western University, London, ON, Canada.
¹⁵ Krembil Centre for Neuroinformatics, Centre for Addiction and Mental Health, Toronto, ON, Canada; Department of Psychiatry, University of Toronto, Toronto, ON, Canada; Institute of Medical Sciences, University of Toronto, Toronto, ON, Canada; Department of Physiology, University of Toronto, Toronto, ON, Canada.
¹⁶ Department of Neuroanatomy, University Medical Center, Georg-August-University, Göttingen, Germany.
¹⁷ Department of Psychiatry, University of Pittsburgh, Pittsburgh, PA, USA.
¹⁸ Campus Institute for Dynamics of Biological Networks, Göttingen, Germany; Max Planck Institute for Dynamics and Self-Organization, Göttingen, Germany; Bernstein Center for Computational Neuroscience, Göttingen, Germany.
¹⁹ Cognitive Neuroscience Laboratory, German Primate Center - Leibniz Institute for Primate Research, Göttingen, Germany; Faculty for Biology and Psychology, University of Göttingen, Göttingen, Germany; Leibniz ScienceCampus, Primate Cognition, Göttingen, Germany.
²⁰ Integrated Program in Neuroscience, McGill University, Montreal, QC, Canada; Department of Physiology, McGill University, Montreal, QC, Canada. Electronic address: anmar.khadra@mcgill.ca.

PMID: 39772396
DOI: 10.1016/j.celrep.2024.115159

Abstract

Cortical neurons in brain slices display intrinsic spike frequency adaptation (I-SFA) to constant current inputs, while extracellular recordings show extrinsic SFA (E-SFA) during sustained visual stimulation. Inferring how I-SFA contributes to E-SFA during behavior is challenging due to the isolated nature of slice recordings. To address this, we recorded macaque lateral prefrontal cortex (LPFC) neurons in vivo during a visually guided saccade task and in vitro in brain slices. Broad-spiking (BS) putative pyramidal cells and narrow-spiking (NS) putative inhibitory interneurons exhibit both E-SFA and I-SFA. Developing a data-driven hybrid circuit model comprising NS model neurons receiving BS input reveals that NS model neurons exhibit longer SFA than observed in vivo; however, adding feedforward inhibition corrects this in a manner dependent on I-SFA. Identification of this circuit motif shaping E-SFA in LPFC highlights the roles of both intrinsic and network mechanisms in neural activity underlying behavior.

Keywords: CP: Neuroscience; broad-spiking and narrow-spiking neurons; circuit motif; computational modeling; extrinsic and intrinsic spike frequency adaptation; hybrid model; inhibition of inhibition; in vivo and in vitro slice recordings; lateral prefrontal cortex; macaque monkeys; visually guided saccade.