Neural activity ramps in frontal cortex signal extended motivation during learning.

TitleNeural activity ramps in frontal cortex signal extended motivation during learning.
Publication TypeJournal Article
Year of Publication2024
AuthorsRegalado JM, Asensio ACorredera, Haunold T, Toader AC, Li YRan, Neal LA, Rajasethupathy P
JournalElife
Volume13
Date Published2024 Jul 22
ISSN2050-084X
KeywordsAnimals, Behavior, Animal, Cues, Gyrus Cinguli, Learning, Male, Mice, Mice, Inbred C57BL, Motivation, Neurons, Prefrontal Cortex, Reward
Abstract

Learning requires the ability to link actions to outcomes. How motivation facilitates learning is not well understood. We designed a behavioral task in which mice self-initiate trials to learn cue-reward contingencies and found that the anterior cingulate region of the prefrontal cortex (ACC) contains motivation-related signals to maximize rewards. In particular, we found that ACC neural activity was consistently tied to trial initiations where mice seek to leave unrewarded cues to reach reward-associated cues. Notably, this neural signal persisted over consecutive unrewarded cues until reward-associated cues were reached, and was required for learning. To determine how ACC inherits this motivational signal we performed projection-specific photometry recordings from several inputs to ACC during learning. In doing so, we identified a ramp in bulk neural activity in orbitofrontal cortex (OFC)-to-ACC projections as mice received unrewarded cues, which continued ramping across consecutive unrewarded cues, and finally peaked upon reaching a reward-associated cue, thus maintaining an extended motivational state. Cellular resolution imaging of OFC confirmed these neural correlates of motivation, and further delineated separate ensembles of neurons that sequentially tiled the ramp. Together, these results identify a mechanism by which OFC maps out task structure to convey an extended motivational state to ACC to facilitate goal-directed learning.

DOI10.7554/eLife.93983
Alternate JournalElife
PubMed ID39037775
PubMed Central IDPMC11262795
Grant ListDP2 AG058487 / AG / NIA NIH HHS / United States
Graduate Research Fellowship / / National Science Foundation /
Gilliam Fellowship / HHMI / Howard Hughes Medical Institute / United States
DP2AG058487 / NH / NIH HHS / United States

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