Dissertations, Theses, and Capstone Projects

Date of Degree

9-2024

Document Type

Dissertation

Degree Name

Ph.D.

Program

Biology

Advisor

Guillem Esber

Committee Members

Andrew Delamater

Susana Mingote

Jon Horvitz

Anjali Krishnan

Subject Categories

Behavioral Neurobiology | Cognitive Neuroscience

Keywords

credit assignment, cue competition, Temporal Difference Reinforcement Learning, electrophysiology, optogenetics, individual difference

Abstract

This dissertation investigates the mechanisms underlying variations in credit assignment to reward cues, with a focus on the lateral orbitofrontal cortex (lOFC). The lOFC has long been implicated in signaling reward expectancies, with controversy as to whether it signals the economic value of future outcomes, their sensory features to guide behavior or both. However, whether the lOFC signals the relative (competition-dependent) or absolute (contiguity-dependent) credit of cues is unknown. To address this, I employed a combination of novel behavioral assays, in-vivo electrophysiological recordings and optogenetic stimulation in rats. In Chapter 2, I tested the suitability of a self-initiating variant of the magazine approach procedure to examine the mechanisms of cue competition. The results show for the first time that agency over trial initiation promotes competitive credit assignment under conditions that normally attenuate it. In Chapter 3, I recorded neural activity in lOFC while rats performed in a novel relative-absolute validity contrast task. Results showed that lOFC neurons encode predictive credit along a competitive-noncompetitive learning continuum, with noncompetitive learning dominating the early stages of training and competitive learning taking increasing control over training. Moreover, encoding of competitive credit emerges late in the cue epoch and gradually migrates to the beginning of the cue as training progresses. This gradual backpropagation pattern, which is predicted by temporal difference reinforcement learning models, had hitherto eluded researchers. In Chapter 4, I report persistent individual differences in credit assignment along the v competitive-noncompetitive continuum and show that these differences correlate with neural activity in lOFC. These findings suggest that some individuals may remain vulnerable to maladaptive responses triggered by incidental cues, which has implications for understanding reward disorders. Finally, in Chapter 5, I examined the causal role of lOFC in credit assignment and discovered that optogenetic inhibition of this region causes paradoxical effects on credit assignment. Specifically, lOFC inhibition makes credit assignment less competitive early in training, but more competitive after extended training. Taken together, these findings underscore the need for further exploration of the neural substrates and clinical implications of the competitive-noncompetitive learning continuum.

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