Competitive integration of time and reward explains value-sensitive foraging decisions and frontal cortex ramping dynamics.


Journal

bioRxiv : the preprint server for biology
Titre abrégé: bioRxiv
Pays: United States
ID NLM: 101680187

Informations de publication

Date de publication:
05 Sep 2023
Historique:
pubmed: 21 9 2023
medline: 21 9 2023
entrez: 21 9 2023
Statut: epublish

Résumé

The ability to make advantageous decisions is critical for animals to ensure their survival. Patch foraging is a natural decision-making process in which animals decide when to leave a patch of depleting resources to search for a new one. To study the algorithmic and neural basis of patch foraging behavior in a controlled laboratory setting, we developed a virtual foraging task for head-fixed mice. Mouse behavior could be explained by ramp-to-threshold models integrating time and rewards antagonistically. Accurate behavioral modeling required inclusion of a slowly varying "patience" variable, which modulated sensitivity to time. To investigate the neural basis of this decision-making process, we performed dense electrophysiological recordings with Neuropixels probes broadly throughout frontal cortex and underlying subcortical areas. We found that decision variables from the reward integrator model were represented in neural activity, most robustly in frontal cortical areas. Regression modeling followed by unsupervised clustering identified a subset of neurons with ramping activity. These neurons' firing rates ramped up gradually in single trials over long time scales (up to tens of seconds), were inhibited by rewards, and were better described as being generated by a continuous ramp rather than a discrete stepping process. Together, these results identify reward integration via a continuous ramping process in frontal cortex as a likely candidate for the mechanism by which the mammalian brain solves patch foraging problems.

Identifiants

pubmed: 37732217
doi: 10.1101/2023.09.05.556267
pmc: PMC10508756
pii:
doi:

Types de publication

Preprint

Langues

eng

Subventions

Organisme : NIMH NIH HHS
ID : F32 MH126505
Pays : United States
Organisme : NINDS NIH HHS
ID : U19 NS113201
Pays : United States

Déclaration de conflit d'intérêts

Competing Interests The authors declare no competing interests.

Auteurs

Michael Bukwich (M)

Department of Molecular and Cellular Biology, Harvard University, Cambridge, MA, 02138.
Center for Brain Science, Harvard University, Cambridge, MA, 02138.
Current address: Sainsbury Wellcome Centre, University College London, London, W1T 4JG, UK.

Malcolm G Campbell (MG)

Department of Molecular and Cellular Biology, Harvard University, Cambridge, MA, 02138.
Center for Brain Science, Harvard University, Cambridge, MA, 02138.

David Zoltowski (D)

Department of Statistics, Stanford University, Stanford, CA, 94305.
Wu Tsai Neurosciences Institute, Stanford University, Stanford, CA 94305.

Lyle Kingsbury (L)

Department of Molecular and Cellular Biology, Harvard University, Cambridge, MA, 02138.
Center for Brain Science, Harvard University, Cambridge, MA, 02138.

Momchil S Tomov (MS)

Department of Molecular and Cellular Biology, Harvard University, Cambridge, MA, 02138.
Center for Brain Science, Harvard University, Cambridge, MA, 02138.
Current address: Motional AD LLC, Boston, MA 02210.

Joshua Stern (J)

Department of Molecular and Cellular Biology, Harvard University, Cambridge, MA, 02138.
Center for Brain Science, Harvard University, Cambridge, MA, 02138.

HyungGoo R Kim (HR)

Department of Molecular and Cellular Biology, Harvard University, Cambridge, MA, 02138.
Center for Brain Science, Harvard University, Cambridge, MA, 02138.
Center for Neuroscience Imaging Research, Institute for Basic Science, Suwon 16419, Republic of Korea.
Department of Biomedical Engineering, Sungkyunkwan University, Suwon 16419, Republic of Korea.

Jan Drugowitsch (J)

Department of Neurobiology, Harvard Medical School, Boston, MA, 02115.

Scott W Linderman (SW)

Department of Statistics, Stanford University, Stanford, CA, 94305.
Wu Tsai Neurosciences Institute, Stanford University, Stanford, CA 94305.

Naoshige Uchida (N)

Department of Molecular and Cellular Biology, Harvard University, Cambridge, MA, 02138.
Center for Brain Science, Harvard University, Cambridge, MA, 02138.

Classifications MeSH