Spike frequency adaptation in primate lateral prefrontal cortex neurons results from interplay between intrinsic properties and circuit dynamics
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...
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2025-01-01
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S2211124724015109 |
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| author | 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 |
| author_facet | 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 |
| author_sort | Nils A. Koch |
| collection | DOAJ |
| description | 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. |
| format | Article |
| id | doaj-art-82709a9440fa478a84d51f82958444a5 |
| institution | Kabale University |
| issn | 2211-1247 |
| language | English |
| publishDate | 2025-01-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Cell Reports |
| spelling | doaj-art-82709a9440fa478a84d51f82958444a52025-01-08T04:52:25ZengElsevierCell Reports2211-12472025-01-01441115159Spike frequency adaptation in primate lateral prefrontal cortex neurons results from interplay between intrinsic properties and circuit dynamicsNils A. Koch0Benjamin W. Corrigan1Michael Feyerabend2Roberto A. Gulli3Michelle S. Jimenez-Sosa4Mohamad Abbass5Julia K. Sunstrum6Sara Matovic7Megan Roussy8Rogelio Luna9Samuel A. Mestern10Borna Mahmoudian11Susheel Vijayraghavan12Hiroyuki Igarashi13Kartik S. Pradeepan14William J. Assis15J. Andrew Pruszynski16Shreejoy Tripathy17Jochen F. Staiger18Guillermo Gonzalez-Burgos19Andreas Neef20Stefan Treue21Stefan Everling22Wataru Inoue23Anmar Khadra24Julio C. Martinez-Trujillo25Integrated Program in Neuroscience, McGill University, Montreal, QC, CanadaDepartment 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, CanadaDepartment 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, CanadaIntegrated Program in Neuroscience, McGill University, Montreal, QC, Canada; Robarts Research Institute, University of Western Ontario, London, ON, CanadaRobarts Research Institute, University of Western Ontario, London, ON, CanadaDepartment 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, CanadaWestern 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, CanadaWestern Institute for Neuroscience, Western University, London, ON, Canada; Robarts Research Institute, University of Western Ontario, London, ON, CanadaDepartment of Physiology and Pharmacology, Schulich School of Medicine and Dentistry, Western University, London, ON, CanadaDepartment of Physiology and Pharmacology, Schulich School of Medicine and Dentistry, Western University, London, ON, Canada; Robarts Research Institute, University of Western Ontario, London, ON, CanadaWestern Institute for Neuroscience, Western University, London, ON, Canada; Robarts Research Institute, University of Western Ontario, London, ON, CanadaDepartment 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, CanadaDepartment of Physiology and Pharmacology, Schulich School of Medicine and Dentistry, Western University, London, ON, CanadaDepartment 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, JapanDepartment of Physiology and Pharmacology, Schulich School of Medicine and Dentistry, Western University, London, ON, Canada; Western Institute for Neuroscience, Western University, London, ON, CanadaWestern Institute for Neuroscience, Western University, London, ON, CanadaDepartment of Physiology and Pharmacology, Schulich School of Medicine and Dentistry, Western University, London, ON, Canada; Western Institute for Neuroscience, Western University, London, ON, CanadaKrembil 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, CanadaDepartment of Neuroanatomy, University Medical Center, Georg-August-University, Göttingen, GermanyDepartment of Psychiatry, University of Pittsburgh, Pittsburgh, PA, USACampus Institute for Dynamics of Biological Networks, Göttingen, Germany; Max Planck Institute for Dynamics and Self-Organization, Göttingen, Germany; Bernstein Center for Computational Neuroscience, Göttingen, GermanyCognitive 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, GermanyDepartment of Physiology and Pharmacology, Schulich School of Medicine and Dentistry, Western University, London, ON, Canada; Western Institute for Neuroscience, Western University, London, ON, CanadaDepartment 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, CanadaIntegrated Program in Neuroscience, McGill University, Montreal, QC, Canada; Department of Physiology, McGill University, Montreal, QC, Canada; Corresponding authorDepartment 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, CanadaSummary: 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.http://www.sciencedirect.com/science/article/pii/S2211124724015109CP: Neuroscience |
| spellingShingle | 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 Spike frequency adaptation in primate lateral prefrontal cortex neurons results from interplay between intrinsic properties and circuit dynamics Cell Reports CP: Neuroscience |
| title | Spike frequency adaptation in primate lateral prefrontal cortex neurons results from interplay between intrinsic properties and circuit dynamics |
| title_full | Spike frequency adaptation in primate lateral prefrontal cortex neurons results from interplay between intrinsic properties and circuit dynamics |
| title_fullStr | Spike frequency adaptation in primate lateral prefrontal cortex neurons results from interplay between intrinsic properties and circuit dynamics |
| title_full_unstemmed | Spike frequency adaptation in primate lateral prefrontal cortex neurons results from interplay between intrinsic properties and circuit dynamics |
| title_short | Spike frequency adaptation in primate lateral prefrontal cortex neurons results from interplay between intrinsic properties and circuit dynamics |
| title_sort | spike frequency adaptation in primate lateral prefrontal cortex neurons results from interplay between intrinsic properties and circuit dynamics |
| topic | CP: Neuroscience |
| url | http://www.sciencedirect.com/science/article/pii/S2211124724015109 |
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