Pyramidal cell types drive functionally distinct cortical activity patterns during decision-making

Nature Neuroscience, vol. 26, pp. 495–505

Abstract

Understanding how cortical circuits generate complex behavior requires investigating the cell types that comprise them. Functional differences across pyramidal neuron (PyN) types have been observed within cortical areas, but it is not known whether these local differences extend throughout the cortex, nor whether additional differences emerge when larger-scale dynamics are considered. We used genetic and retrograde labeling to target pyramidal tract, intratelencephalic and corticostriatal projection neurons and measured their cortex-wide activity. Each PyN type drove unique neural dynamics, both at the local and cortex-wide scales. Cortical activity and optogenetic inactivation during an auditory decision task revealed distinct functional roles. All PyNs in parietal cortex were recruited during perception of the auditory stimulus, but, surprisingly, pyramidal tract neurons had the largest causal role. In frontal cortex, all PyNs were required for accurate choices but showed distinct choice tuning. Our results reveal that rich, cell-type-specific cortical dynamics shape perceptual decisions.

Authors 12

1. Simon Musall corresponding Aachen Department of Systems Neurophysiology Institute for Zoology

   Forschungszentrum Jülich · RWTH Aachen University

   Affiliation as printed

   Department of Systems Neurophysiology, Institute for Zoology, RWTH Aachen University, Aachen, Germany. s.musall@fz-juelich.de

   Institute of Biological Information Processing (IBI-3), Forschungszentrum Jülich, Jülich, Germany. s.musall@fz-juelich.de

   Institute of Biological Information Processing (IBI-3), Forschungszentrum Jülich, Jülich, Germany

2. Xiaonan Richard Sun

   Cold Spring Harbor Laboratory · Donald & Barbara Zucker School of Medicine at Hofstra/Northwell

   Affiliation as printed

   Cold Spring Harbor Laboratory, Neuroscience, Cold Spring Harbor, New York, NY, USA

   Department of Neurosurgery, Zucker School of Medicine at Hofstra/Northwell, Hempstead, NY, USA

3. Hemanth Mohan

   Cold Spring Harbor Laboratory · Duke Medical Center

   Affiliation as printed

   Cold Spring Harbor Laboratory, Neuroscience, Cold Spring Harbor, New York, NY, USA

   Department of Neurobiology, Duke University Medical Center, Durham, NC, USA

4. Xu An

   Cold Spring Harbor Laboratory · Duke Medical Center

   Affiliation as printed

   Cold Spring Harbor Laboratory, Neuroscience, Cold Spring Harbor, New York, NY, USA

   Department of Neurobiology, Duke University Medical Center, Durham, NC, USA

5. Steven Gluf

   Cold Spring Harbor Laboratory

   Affiliation as printed

   Cold Spring Harbor Laboratory, Neuroscience, Cold Spring Harbor, New York, NY, USA

6. Shu-Jing Li

   Cold Spring Harbor Laboratory

   Affiliation as printed

   Cold Spring Harbor Laboratory, Neuroscience, Cold Spring Harbor, New York, NY, USA

7. Rhonda Drewes

   Cold Spring Harbor Laboratory

   Affiliation as printed

   Cold Spring Harbor Laboratory, Neuroscience, Cold Spring Harbor, New York, NY, USA

8. Emma Cravo Aachen Department of Systems Neurophysiology Institute for Zoology

   RWTH Aachen University

   Affiliation as printed

   Department of Systems Neurophysiology, Institute for Zoology, RWTH Aachen University, Aachen, Germany

9. Irene Lenzi Aachen Department of Systems Neurophysiology Institute for Zoology

   Forschungszentrum Jülich · RWTH Aachen University

   Affiliation as printed

   Department of Systems Neurophysiology, Institute for Zoology, RWTH Aachen University, Aachen, Germany

   Institute of Biological Information Processing (IBI-3), Forschungszentrum Jülich, Jülich, Germany

10. Chaoqun Yin

    University of California, Los Angeles

    Affiliation as printed

    Department of Neurobiology, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, CA, USA

11. Björn M. Kampa Aachen Department of Systems Neurophysiology Institute for Zoology

    Forschungszentrum Jülich · Jülich Aachen Research Alliance · RWTH Aachen University

    Affiliation as printed

    Department of Systems Neurophysiology, Institute for Zoology, RWTH Aachen University, Aachen, Germany

    JARA Brain, Institute for Neuroscience and Medicine (INM-10), Forschungszentrum Jülich, Jülich, Germany

12. Anne K. Churchland corresponding

    University of California, Los Angeles · Cold Spring Harbor Laboratory

    Affiliation as printed

    Cold Spring Harbor Laboratory, Neuroscience, Cold Spring Harbor, New York, NY, USA. achurchland@mednet.ucla.edu

    Department of Neurobiology, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, CA, USA. achurchland@mednet.ucla.edu

    Cold Spring Harbor Laboratory, Neuroscience, Cold Spring Harbor, New York, NY, USA