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

Abstract

Anterior cingulate cortex (ACC) and striatum (STR) contain neurons encoding not only the expected values of actions, but also the value of stimulus features irrespective of actions. Values about stimulus features in ACC or STR might contribute to adaptive behavior by guiding fixational information sampling and biasing choices toward relevant objects, but they might also have indirect motivational functions by enabling subjects to estimate the value of putting effort into choosing objects. Here, we tested these possibilities by modulating neuronal activity in ACC and STR of nonhuman primates using transcranial ultrasound stimulation while subjects learned the relevance of objects in situations with varying motivational and cognitive demands. Motivational demand was indexed by varying gains and losses during learning, while cognitive demand was varied by increasing the uncertainty about which object features could be relevant during learning. We found that ultrasound stimulation of the ACC, but not the STR, reduced learning efficiency and prolonged information sampling when the task required averting losses and motivational demands were high. Reduced learning efficiency was particularly evident at high cognitive demands and immediately after subjects experienced a loss of already attained tokens. These results suggest that the ACC supports flexible learning of feature values when loss experiences impose a motivational challenge and when uncertainty about the relevance of objects is high. Taken together, these findings provide causal evidence that the ACC facilitates resource allocation and improves visual information sampling during adaptive behavior.

Noradrenergic alpha-2a Receptor Stimulation Enhances Prediction Error Signaling in Anterior Cingulate Cortex and Striatum

“…We found the neural correlates of enhanced set shifting in those neural circuits in the ACC and striatum of NHPs that are known to activate during guided exploratory behavior and information seeking (Bromberg-Martin and Monosov, 2020; Boroujeni et al, 2022; Jahn et al, 2023). Activity in the ACC, in particular, correlates with successfully exploring alternative options and gathering information about the value of options (Jahn et al, 2023).…”

The Medial Frontal Cortex, Performance Monitoring, Cognitive Control, and Decision Making

“…Moreover, feedback-related aMCC activity during a probabilistic learning task was associated with performance in a delayed memory task (Klein et al, 2007). In addition, ultrasound stimulation of the aMCC-homolog during a learning task in non-human primates reduced learning efficiency and prolonged information sampling (Banaie Boroujeni et al, 2022). Third, results from functional connectivity analyses revealed stronger aMCC connectivity with hippocampus and ventral striatum during early learning when feedback is highly informative, compared to later stages in learning (Klein et al, 2007).…”

Effects of the motor cortical theta‐burst transcranial‐focused ultrasound stimulation on the contralateral motor cortex

“…Low‐intensity transcranial‐focused ultrasound stimulation (TUS) is gaining increasing attention due to the advantages of high spatial resolution and ability to target deep brain structures such as the basal ganglia (Nakajima et al., 2022), thalamus (Legon et al., 2018), anterior cingulate cortex and striatum (Banaie Boroujeni et al., 2022). Recent work has demonstrated that TUS could induce aftereffects at the stimulated site that persist beyond the period of stimulation (Nakajima et al., 2022; Samuel et al., 2022; Zeng et al., 2022; Zhang et al., 2021).…”