Primate ventromedial prefrontal cortex neurons continuously encode the willingness to engage in reward directed behavior

Abstract

To survive in their complex environment, primates must integrate information over time and adjust their actions beyond immediate events. The underlying neurobiological processes, however, remain unclear. Here, we assessed the contribution of the ventromedial prefrontal cortex (VMPFC), a brain region important for value-based decision making. We recorded single VMPFC neurons in monkeys performing a task where obtaining fluid rewards required squeezing a grip. The willingness to perform the action was modulated not only by visual information about Effort and Reward levels, but also by contextual factors such as Trial Number (i.e fatigue and/or satiety) or behavior in recent trials. A greater fraction of VMPFC neurons encoded contextual information, compared to visual stimuli. Moreover, the dynamics of VMPFC firing was more closely related to slow changes in motivational states driven by these contextual factors rather than rapid responses to individual task events. Thus, the firing of VMPFC neurons continuously integrated contextual information and reliably predicted the monkeys's willingness to perform the task. This function might be critical when animals forage in a complex environment and need to integrate information over time. Its relation with motivational states also resonates with the VMPFC's implication in the 'default mode' or in mood disorders.

The Subjective Value of Cognitive Effort is Encoded by a Domain-General Valuation Network

“…Specifically, low-load choices were anticipated by below-average vmPFC signal during the valuation period, and this was particularly true on when offers biased high-load offer selection. This finding is consistent with the hypothesis that state variation in SV, as encoded by the vmPFC, determines momentary preference (Hare et al, 2009(Hare et al, , 2011(Hare et al, , 2014Rudebeck and Murray, 2014), current motivational state (Bouret and Richmond, 2010), and willingness to perform effortful instrumental tasks (San-Galli et al, 2018).…”

“…To test for such effects, we examined whether trialwise variation in SV representations predicted choice; specifically, whether valuation period signal predicted choice behavior, above and beyond the bias (␥) imposed by the second offer. We focused our analysis on the VS and vmPFC, given clear SV tracking in these regions, and also prior literature implicating vmPFC both in state incentive motivation, and causally determining choice (Hare et al, 2009(Hare et al, , 2011(Hare et al, , 2014Rudebeck and Murray, 2014;San-Galli et al, 2018).…”

Orbitofrontal Cortex: A Neural Circuit for Economic Decisions

“…These include in particular recent studies that focused on signals associated with individual goods or options (Howard et al, 2015; Howard and Kahnt, 2017; Klein-Flugge et al, 2013). Furthermore, a distinction recently drawn by San Galli et al (2016) seems potentially revealing. In their experiments, monkeys had to squeeze a bar (3 effort levels) to obtain a juice reward (3 quantity levels).…”

“…Most strikingly, firing rates were highly correlated with the willingness to work. In other words, neuronal activity in vmPFC seemed best explained in terms of the overall engagement in the task, as opposed to the values available for choice on any given trial (San Galli et al, 2016). Corroborating this perspective, vmPFC activity has also been linked to affective regulation (Delgado et al, 2016), and vmPFC dysfunction has been implicated in mood disorders including major depression (Price and Drevets, 2010; Ressler and Mayberg, 2007).…”

A Basal Forebrain-Cingulate Circuit in Macaques Decides It Is Time to Act

“…It is not clear why animals sometimes refrain from responding in an experimental task when any task-related response is usually likely to increase the likelihood of reward. Nevertheless, it is well known that they often do so (San-Galli et al, 2018;Stoll et al, 2016a). One way to interpret the results is that the animals doing so are avoiding paying a cost that is entailed by performing the trial.…”