Covert valuation for information sampling and choice

Abstract

We use our eyes to assess the value of objects around us and carefully fixate options that we are about to choose. Neurons in the prefrontal cortex reliably encode the value of fixated options, which is essential for decision making. Yet as a decision unfolds, it remains unclear how prefrontal regions determine which option should be fixated next. Here we show that anterior cingulate cortex (ACC) encodes the value of options in the periphery to guide subsequent fixations during economic choice. In an economic decision-making task involving four simultaneously presented cues, we found rhesus macaques evaluated cues using their peripheral vision. This served two distinct purposes: subjects were more likely to fixate valuable peripheral cues, and more likely to choose valuable options whose cues were never even fixated. ACC, orbitofrontal cortex, dorsolateral pre-frontal cortex, and ventromedial prefrontal cortex neurons all encoded cue value post-fixation. ACC was unique, however, in also encoding the value of cues before fixation and even cues that were never fixated. This pre-saccadic value encoding by ACC predicted which cue was next fixated during the decision process. ACC therefore conducts simultaneous processing of peripheral information to guide information sampling and choice during decision making.

Anterior cingulate cortex causally supports flexible learning under motivationally challenging and cognitively demanding conditions

“…Our main findings suggest extensions to theoretical accounts of the overarching function of the ACC for adaptive behavior. First, the finding of prolonged information sampling after ACC-TUS supports recent electrophysiological and imaging studies showing that activity in the ACC predicts information sampling of visual objects and attention to maximize reward outcomes [17,18,25,42]. However, we found a functional deficit of information sampling only in the gain-loss learning context in which subjects expected lower payoff, suggesting that the ACC contributes to information sampling, particularly in motivationally challenging conditions.…”

“…These studies found that neurons in the ACC encoded the pre-learned value of objects when they were fixated [18] or peripherally attended [16,19]. Moreover, subpopulations of ACC neurons also encode the value of objects that are not yet fixated but are possible future targets for fixations [17]. Disrupting these signals with TUS in our study is a plausible reason causing uncertainty about the value of objects and for prolonging information sampling durations.…”

“…These results suggest that TUS might disrupt or modulate the activity of neuronal circuitries in ACC that would have responded to the demand for information about the feature values by controlling the duration of gaze fixations on available objects. Such activity has been documented to be encoded in ACC [16][17][18][19]. These studies found that neurons in the ACC encoded the pre-learned value of objects when they were fixated [18] or peripherally attended [16,19].…”

“…These findings suggest that the ACC or striatum may be functionally important to learn expected values of objects' specific visual features and thereby mediate information-seeking behavior and visual attention [17,[21][22][23][24][25]. There are at least 3 possible ways how feature-specific value information in these areas may support flexible learning.…”

“…Succeeding with these tasks requires computing probabilities of action-reward associations. However, recent studies have documented neurons in ACC and striatum that not only tracked action-reward association probabilities, but also the expected reward value of specific features of chosen objects [11,[15][16][17][18][19]. Neuronal information about the value object features emerged slightly earlier in ACC than in striatum [15,16,19] and rapidly synchronized between both structures suggesting they are available across the frontostriatal network at similar times [20].…”