Nucleus accumbens, thalamus and insula connectivity during incentive anticipation in typical adults and adolescents

Abstract

Reward neurocircuitry links motivation with complex behavioral responses. Studies of incentive processing have repeatedly demonstrated activation of nucleus accumbens (NAc), thalamus, and anterior insula, three key components of reward neurocircuitry. The contribution of the thalamus to this circuitry in humans has been relatively ignored, a gap that needs to be filled, given the central role of this structure in processing and filtering information. This study aimed to understand how these three regions function as a network during gain or loss anticipation in adults and youth. Towards this goal, functional magnetic resonance imaging (fMRI) and dynamic causal modeling (DCM) were used to examine effective connectivity among these three nodes in healthy adults and adolescents who performed the monetary incentive delay (MID) task. Seven connectivity models, based on anatomic connections, were tested. They were estimated for incentive anticipation and underwent Bayesian Model Selection (BMS) to determine the best-fit model for each adult and adolescent group. Connection strengths were extracted from the best-fit model and examined for significance in each group. These variables were then entered into a linear mixed model to test between-group effects on effective connectivity in reward neurocircuitry. The best-fit model for both groups included all possible anatomic connections. Three main findings emerged: (1) Across the task, thalamus and insula significantly influenced NAc; (2) A broader set of significant connections was found for the loss-cue condition than the gain-cue condition in both groups; (3) Finally, between-group comparisons of connectivity strength failed to detect statistical differences, suggesting that adults and adolescents use this incentive-processing network in a similar manner. This study demonstrates the way in which the thalamus and insula influence the NAc during incentive processing in humans. Specifically, this is the first study to demonstrate in humans the key role of thalamus projections onto the NAc in support of reward processing. Our results suggest that anticipation of gain/loss involves an ‘alerting’ signal (thalamus) that converges with interoceptive information (insula) to shape action selection programs in the ventral striatum.

Identifying the neural substrates of intrinsic motivation during task performance

“…That is, AIC and striatum activities positively interacted more during the performance of intrinsically, relative to non-intrinsically, motivating tasks. This finding is consistent with previous neuroscientific findings showing functional connectivity between the AIC and striatum (Cho et al, 2013;Postuma & Dagher, 2006). This functional connectivity pattern is consistent with well-established anatomical connections between the AIC and striatum (Chikama et al, 1997;Singer, Critchley, & Preuschoff, 2009).…”

“…The basis of this prediction was the proposition that the AIC and striatum interact-or work together during the experience of intrinsic motivation-to constitute the intrinsic-motivation system. We based H3 on the well-known anatomical and functional connectivity between the AIC and striatum in the motivation circuitry (Chikama, McFarland, Amaral, & Haber, 1997;Cho et al, 2013). H3 would be confirmed by increased AIC-striatum interaction during the performance of the intrinsically, relative to non-intrinsically, motivating tasks.…”

Effect of GABRA2 Genotype on Development of Incentive-Motivation Circuitry in a Sample Enriched for Alcoholism Risk

“…In a group comparison between adolescents aged 12-17 years (n ¼ 24) and adults aged 22-42 years (n ¼ 24), reduced activation of the NAcc during anticipation of reward was found in adolescents (Bjork et al, 2010). However, a comparison of 10-to 17-year olds (n ¼ 24) with 22-to 48-year olds (n ¼ 30) found reduced activation in the putamen, but not the ventral striatum (Cho et al, 2012). Differences across these reports and the present work may be due in part to definition of age groups, which could introduce confounds (Galvan, 2010;Luna et al, 2010).…”

A cross-sectional and longitudinal analysis of reward-related brain activation: Effects of age, pubertal stage, and reward sensitivity

“…Instead, increased functional connectivity was found between VS and insula after rewards compared to losses, and the strength of this functional connectivity was related to individuals' risky decision-making. That is, greater connectivity was associated with an attenuated tendency to play, suggesting a potentially regulatory role of the insula (see also Cho et al, 2012). Indeed, insula activation has been implicated in saliency detection (Menon & Uddin, 2010), harm avoidance (Paulus, Rogalsky, Simmons, Feinstein, & Stein, 2003), and risk processing (Mohr, Biele, & Heekeren, 2010).…”