Cell Reports (Jan 2025)
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
Affiliations
- Nils A. Koch
- Integrated Program in Neuroscience, McGill University, Montreal, QC, Canada
- Benjamin W. Corrigan
- 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
- Michael Feyerabend
- 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
- Roberto A. Gulli
- Integrated Program in Neuroscience, McGill University, Montreal, QC, Canada; Robarts Research Institute, University of Western Ontario, London, ON, Canada
- Michelle S. Jimenez-Sosa
- Robarts Research Institute, University of Western Ontario, London, ON, Canada
- Mohamad Abbass
- 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
- Julia K. Sunstrum
- 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
- Sara Matovic
- Western Institute for Neuroscience, Western University, London, ON, Canada; Robarts Research Institute, University of Western Ontario, London, ON, Canada
- Megan Roussy
- Department of Physiology and Pharmacology, Schulich School of Medicine and Dentistry, Western University, London, ON, Canada
- Rogelio Luna
- 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
- Samuel A. Mestern
- Western Institute for Neuroscience, Western University, London, ON, Canada; Robarts Research Institute, University of Western Ontario, London, ON, Canada
- Borna Mahmoudian
- 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
- Susheel Vijayraghavan
- Department of Physiology and Pharmacology, Schulich School of Medicine and Dentistry, Western University, London, ON, Canada
- Hiroyuki Igarashi
- 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
- Kartik S. Pradeepan
- 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
- William J. Assis
- Western Institute for Neuroscience, Western University, London, ON, Canada
- J. Andrew Pruszynski
- 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
- Shreejoy Tripathy
- 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
- Jochen F. Staiger
- Department of Neuroanatomy, University Medical Center, Georg-August-University, Göttingen, Germany
- Guillermo Gonzalez-Burgos
- Department of Psychiatry, University of Pittsburgh, Pittsburgh, PA, USA
- Andreas Neef
- 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
- Stefan Treue
- 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
- Stefan Everling
- 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
- Wataru Inoue
- 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
- Anmar Khadra
- Integrated Program in Neuroscience, McGill University, Montreal, QC, Canada; Department of Physiology, McGill University, Montreal, QC, Canada; Corresponding author
- Julio C. Martinez-Trujillo
- 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
- Journal volume & issue
-
Vol. 44,
no. 1
p. 115159
Abstract
Summary: 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.
