Robust and distributed neural representation of action values

Abstract

Studies in rats, monkeys, and humans have found action-value signals in multiple regions of the brain. These findings suggest that action-value signals encoded in these brain structures bias choices toward higher expected rewards. However, previous estimates of action-value signals might have been inflated by serial correlations in neural activity and also by activity related to other decision variables. Here, we applied several statistical tests based on permutation and surrogate data to analyze neural activity recorded from the striatum, frontal cortex, and hippocampus. The results show that previously identified action-value signals in these brain areas cannot be entirely accounted for by concurrent serial correlations in neural activity and action value. We also found that neural activity related to action value is intermixed with signals related to other decision variables. Our findings provide strong evidence for broadly distributed neural signals related to action value throughout the brain.

Widespread coding of navigational variables in prefrontal cortex

“…The modular approach to understanding functional neuroanatomy has been challenged by a growing set of studies that highlight the broad distribution of variables otherwise thought to be more narrowly circumscribed. These include motor signals (Musall et al, 2019a and b; Stringer et al, 2019; Steinmetz et al, 2019) and reward signals (Vickery et al, 2011; Shin et al, 2021; Ottenheimer et al, 2022). These findings raise the possibility that like other cognitive functions, navigation may also be more distributed than previously assumed, perhaps as part of a gradient characterized by gradual untangling rather than strict functional borders (Fine et al, 2022; Fuster, 2000 and 2001; Yoo et al, 2018).…”

A neural substrate of sex-dependent modulation of motivation by value

“…Similar results emerged from considering only the neurons with significantly different activity on rewarded and unrewarded trials ( Figure 4e-f ). We classified neurons as outcome-encoding based on whether including the type of outcome (rewarded vs. unrewarded) improved the fit of a linear encoding model for each neuron, compared to a null distribution generated from fitting the same models to randomly shifted fluorescence data (see Methods for details) 64, 65 . In females compared to males, a significantly larger proportion of outcome-encoding neurons were preferentially active on unrewarded trials, while a significantly smaller proportion were preferentially active on rewarded trials ( Figure 4e-f ; χ 2 −test comparing the proportions of outcome-encoding neurons in males and females, χ 2 (2, n=756) = 24.16, p = 5.67x10 -6 ; the Marascuilo procedure with alpha=0.01 was used for comparisons between proportions of reward- and no reward-preferring outcome-encoding neurons in females and males; see Supplementary Figure 13b for definition of reward- and no reward-preferring neurons).…”

Motor Plans under Uncertainty Reflect a Trade-Off between Maximizing Reward and Success

“…While some amount of effort has been made to investigate the neural underpinnings of direct and intermediate movements ( Cisek and Kalaska, 2002 ; Cisek, 2007 ; Dekleva et al, 2018 ), much of this work thus far has focused on premotor cortex. In contrast, efforts to study the representation of subjective value and relative choice desirability have largely investigated midbrain structures including the basal ganglia and ventral tegmenal area, and associated areas of frontal cortex ( Samejima et al, 2005 ; Trepel et al, 2005 ; Croxson et al, 2009 ; Fox and Poldrack, 2009 ; Levy et al, 2010 ; Schmidt et al, 2012 ; Klein-Flügge et al, 2016 ; Doi et al, 2020 ; Shin et al, 2021 ). Intriguingly, however, there is some suggestion that parietal reach region in the posterior parietal cortex might be a potential area where information about motor goals and goal desirability converge ( Trepel et al, 2005 ).…”