Dissociable roles of central striatum and anterior lateral motor area in initiating and sustaining naturalistic behavior

Victoria L Corbit; Sean C Piantadosi; Jesse Wood; Srividhya S Madireddy; Clare J Y Choi; Ilana B Witten; Aryn H Gittis; Susanne E Ahmari

doi:10.1016/j.celrep.2024.115181

Dissociable roles of central striatum and anterior lateral motor area in initiating and sustaining naturalistic behavior

Cell Rep. 2025 Jan 8;44(1):115181. doi: 10.1016/j.celrep.2024.115181. Online ahead of print.

Authors

Victoria L Corbit¹, Sean C Piantadosi², Jesse Wood³, Srividhya S Madireddy⁴, Clare J Y Choi⁵, Ilana B Witten⁵, Aryn H Gittis⁶, Susanne E Ahmari⁷

Affiliations

¹ Center for the Neural Basis of Cognition, Carnegie Mellon University, Pittsburgh, PA, USA; Center for Neuroscience, University of Pittsburgh, Pittsburgh, PA, USA; Department of Biological Sciences, Carnegie Mellon University, Pittsburgh, PA, USA; Translational Neuroscience Program, Department of Psychiatry, University of Pittsburgh, Pittsburgh, PA, USA; Princeton Neuroscience Institute, Princeton University, Princeton, NJ, USA.
² Center for Neuroscience, University of Pittsburgh, Pittsburgh, PA, USA; Translational Neuroscience Program, Department of Psychiatry, University of Pittsburgh, Pittsburgh, PA, USA; Department of Anesthesiology and Pain Medicine, University of Washington, Seattle, WA, USA.
³ Translational Neuroscience Program, Department of Psychiatry, University of Pittsburgh, Pittsburgh, PA, USA.
⁴ Center for Neuroscience, University of Pittsburgh, Pittsburgh, PA, USA; Translational Neuroscience Program, Department of Psychiatry, University of Pittsburgh, Pittsburgh, PA, USA.
⁵ Princeton Neuroscience Institute, Princeton University, Princeton, NJ, USA.
⁶ Center for the Neural Basis of Cognition, Carnegie Mellon University, Pittsburgh, PA, USA; Department of Biological Sciences, Carnegie Mellon University, Pittsburgh, PA, USA.
⁷ Center for the Neural Basis of Cognition, Carnegie Mellon University, Pittsburgh, PA, USA; Center for Neuroscience, University of Pittsburgh, Pittsburgh, PA, USA; Translational Neuroscience Program, Department of Psychiatry, University of Pittsburgh, Pittsburgh, PA, USA. Electronic address: ahmarise@upmc.edu.

PMID: 39786992
DOI: 10.1016/j.celrep.2024.115181

Abstract

Understanding how corticostriatal circuits mediate behavioral selection and initiation in a naturalistic setting is critical to understanding behavior choice and execution in unconstrained situations. The central striatum (CS) is well poised to play an important role in these spontaneous processes. Using fiber photometry and optogenetics, we identify a role for CS in grooming initiation. However, CS-evoked movements resemble short grooming fragments, suggesting additional input is required to appropriately sustain behavior once initiated. Consistent with this idea, the anterior lateral motor area (ALM) demonstrates a slow ramp in activity that peaks at grooming termination, supporting a potential role for ALM in encoding grooming bout length. Furthermore, optogenetic stimulation of ALM-CS terminals generates sustained grooming responses. Finally, dual-region photometry indicates that CS activation precedes ALM during grooming. Taken together, these data support a model in which CS is involved in grooming initiation, while ALM may encode grooming bout length.

Keywords: CP: Neuroscience; SLEAP; anterior lateral motor area; calcium imaging; grooming; optogenetics; photometry; ramping activity; spontaneous behavior; striatum.