Normative development of ventral striatal resting state connectivity in humans

Abstract

Incentives play a crucial role in guiding behavior throughout our lives, but perhaps no more so than during the early years of life. The ventral striatum is a critical piece of an incentive-based learning circuit, sharing robust anatomical connections with subcortical (e.g., amygdala, hippocampus) and cortical structures (e.g., medial prefrontal cortex (mPFC), insula) that collectively support incentive valuation and learning. Resting-state functional connectivity (rsFC) is a powerful method that provides insight into the development of the functional architecture of these connections involved in incentive-based learning. We employed a seed-based correlation approach to investigate ventral striatal rsFC in a cross-sectional sample of typically developing individuals between the ages of 4.5 and 23-years old (n=66). Ventral striatal rsFC with the mPFC showed regionally specific linear age-related changes in connectivity that were associated with age-related increases in circulating testosterone levels. Further, ventral striatal connectivity with the posterior hippocampus and posterior insula demonstrated quadratic age-related changes characterized by negative connectivity in adolescence. Finally, across this age range, the ventral striatum demonstrated positive coupling with the amygdala beginning during childhood and remaining consistently positive across age. In sum, our findings suggest normative ventral striatal rsFC development is dynamic and characterized by early establishment of connectivity with medial prefrontal and limbic structures supporting incentive-based learning, as well as substantial functional reorganization with later developing regions during transitions into and out of adolescence.

Toward a Personalized Science of Emotion Regulation

“…These findings have at least two possible explanations. One explanation is that developing neurobiology allows for prefrontal regulation of subcortical structures involved in generating appetitive responses before regulation of regions involved in generating aversive responses (see Fareri et al, in press; Gabard‐Durnam et al, ). Another possible explanation is that children have more experience interpreting food cues than they do with negative social situations and this experience facilitates better regulation (i.e., children eat food every day of their lives but encounter negative social situations less frequently).…”

Stress and the adolescent brain

“…The amygdala has strong bidirectional projections with the PFC (Barbas, Saha, Rempel-Clower, & Ghashghaei, 2003), while the ventral striatum receives unidirectional projections from the amygdala and PFC, including excitatory projections that facilitate reward learning (Stuber et al, 2011), and sends indirect projections back to the PFC (Cardinal, Parkinson, Hall, & Everitt, 2002; Casey, 2015; Cho, Ernst, & Fudge, 2013). The strong connectivity from the amygdala to the ventral striatum (Cho et al, 2013) has been observed during human development starting as early as early childhood as measured by resting state functional connectivity (Fareri et al, 2015). However, what will be clear in this review is that to date, the functional significance of these amygdala-ventral striatum connections has not been thoroughly examined in human development, and much of the extant human developmental work has approached the function of these two regions in parallel rather than in coordination.…”

A three‐wave longitudinal study of subcortical–cortical resting‐state connectivity in adolescence: Testing age‐ and puberty‐related changes

“…Previous RS studies already observed developmental changes in functional connectivity between subcortical regions and prefrontal circuitry. Whereas the functional coupling between the amygdala and medial PFC has been found to increase (Gabard‐Durnam et al, ) or show minimal changes (Peters, Peper, Duijvenvoorde, Braams, & Crone, ) across adolescence, studies also found a developmental decrease in connectivity strength for other subcortical–cortical connections, such as connectivity between the ventral striatum and PFC (Fareri et al, ; Padmanabhan, Lynn, Foran, Luna, & O'Hearn, ; Porter et al, ; van Duijvenvoorde, Achterberg, Braams, Peters, & Crone, ). This decrease in functional coupling between subcortical and prefrontal circuitries has been interpreted as a maturation of brain networks, and linked to a developmental decrease in risky behavior and reward valuation (van Duijvenvoorde, Achterberg, et al, ) across adolescence, but also to individual differences in risky behavior.…”