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Encoding externally and internally accredited value in prefrontal cortex

Abstract

Given the prefrontal cortex (PFC) is involved in tracking consequences from both one's environment and actions, this work attempts to characterize the involved neuronal processes. In the first portion of this thesis, we focus on internally accredited value, namely the value of actions. We recorded the spiking activity from single neurons of two subjects while they performed a task that required them to monitor relationships between their actions and resulting outcomes on a trial-by-trial basis. We contrasted the activity from two brain areas known to have projections to motor areas but different limbic and attentional roles: dorsolateral prefrontal cortex (PFdl) and medial prefrontal cortex, dorsal to the cingulate sulcus (PFcs). During the epoch after the first action-outcome (AO) association was revealed to the subject, nearly twice as many PFdl neurons encoded the action compared to the outcome. Conversely, more PFcs neurons encoded the outcome as compared to the action. In both brain areas, information about action and outcome were separated in two populations: few neurons encoded action and outcome. When the subjects learned a subsequent AO association, that outcome was encoded relative to the first, i.e., better or worse, rather than as the identity of the outcome, i.e., apple juice or quinine. Again, PFcs had more reward encoding than PFdl at this time. These data support past studies that implicate PFcs in monitoring the value of actions for value-based decision making.

The second portion of this work contrasts neuronal representations of AO associations with that of stimulus-outcome (SO) associations. Lesion and imaging studies have suggested that AO encoding relies on PFcs and SO encoding on orbitofrontal cortex (PFo). We hypothesized similar dissociation at the neuronal level. To test this idea, we trained the same two subjects on two tasks, one that relied on AO associations to solve and another that relied on SO associations. The SO task was analogous to the aforementioned AO task, except that pictures, rather than actions, were associated with the delivery of juice rewards. While the subjects performed these tasks, we recorded the neuronal activity from PFcs and PFo. Both areas had neurons encoding stimuli, actions, and outcomes across the tasks. There was only a subtle bias for PFo neurons preferring the SO task. Most notable was the prominent action selectivity in PFo for the action the subject would perform to select his more preferred reward in the SO task. No such bias was seen in the AO task. Collectively, this work implicates PFcs and PFo as key regions in goal-directed behavior given their ability to flexibly represent value as it is attributed to either external cues or internally generated motor actions.

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