The behavioral signature of stepwise learning strategy in male rats and its neural correlate in the basal forebrain

Hachi E. Manzur, Ksenia Vlasov, You-Jhe Jhong, Hung-Yen Chen and Shih-Chieh Lin ()
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Hachi E. Manzur: National Institute on Aging, National Institutes of Health
Ksenia Vlasov: National Institute on Aging, National Institutes of Health
You-Jhe Jhong: National Yang Ming Chiao Tung University
Hung-Yen Chen: National Yang Ming Chiao Tung University
Shih-Chieh Lin: National Institute on Aging, National Institutes of Health

Nature Communications, 2023, vol. 14, issue 1, 1-15

Abstract: Abstract Studies of associative learning have commonly focused on how rewarding outcomes are predicted by either sensory stimuli or animals’ actions. However, in many learning scenarios, reward delivery requires the occurrence of both sensory stimuli and animals’ actions in a specific order, in the form of behavioral sequences. How such behavioral sequences are learned is much less understood. Here we provide behavioral and neurophysiological evidence to show that behavioral sequences are learned using a stepwise strategy. In male rats learning a new association, learning started from the behavioral event closest to the reward and sequentially incorporated earlier events. This led to the sequential refinement of reward-seeking behaviors, which was characterized by the stepwise elimination of ineffective and non-rewarded behavioral sequences. At the neuronal level, this stepwise learning process was mirrored by the sequential emergence of basal forebrain neuronal responses toward each event, which quantitatively conveyed a reward prediction error signal and promoted reward-seeking behaviors. Together, these behavioral and neural signatures revealed how behavioral sequences were learned in discrete steps and when each learning step took place.

Date: 2023
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DOI: 10.1038/s41467-023-40145-9

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