Nucleus accumbens, thalamus and insula connectivity during incentive anticipation in typical adults and adolescents.
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.
Department of Neurobiology and Anatomy, University of Rochester Medical Center, NY, USA.
Youngsun T
YT
Cho
Section on Development and Affective Neuroscience Branch, National Institute of Mental Health, NIH, DHHS, MD, USA.
Stephen
S
Fromm
Center for Mind and Brain, University of California, Davis, CA, USA.
Amanda E
AE
Guyer
Section on Development and Affective Neuroscience Branch, National Institute of Mental Health, NIH, DHHS, MD, USA.
Allison
A
Detloff
Section on Development and Affective Neuroscience Branch, National Institute of Mental Health, NIH, DHHS, MD, USA.
Daniel S
DS
Pine
Department of Neurobiology and Anatomy, University of Rochester Medical Center, NY, USA.
Julie L
JL
Fudge
Section on Development and Affective Neuroscience Branch, National Institute of Mental Health, NIH, DHHS, MD, USA. Electronic address: ernstm@mail.nih.gov.
Monique
M
Ernst
D000293:Adolescent; D000328:Adult; D059031:Anticipation, Psychological / Q000502:physiology*; D001931:Brain Mapping; D002540:Cerebral Cortex / Q000033:anatomy & histology / Q000502:physiology*; D003463:Cues; D005260:Female; D006801:Humans; D007091:Image Processing, Computer-Assisted; D008279:Magnetic Resonance Imaging; D008297:Male; D008875:Middle Aged; D009434:Neural Pathways / Q000033:anatomy & histology / Q000502:physiology*; D009714:Nucleus Accumbens / Q000033:anatomy & histology / Q000502:physiology*; D012201:Reward; D013788:Thalamus / Q000033:anatomy & histology / Q000502:physiology*; D055815:Young Adult