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Abstract
Error detection is critical to the shaping of goal-oriented behavior. Recent studies in non-human primates delineated a circuit involving the lateral habenula (LH) and ventral tegmental area (VTA) in error detection. Neurons in the LH increased activity, preceding decreased activity in the VTA, to a missing reward, indicating a feedforward signal from the LH to VTA. In the current study we used connectivity analyses to reveal this pathway in humans. In 59 adults performing a stop signal task during functional magnetic resonance imaging, we identified brain regions showing greater psychophysiological interaction with the habenula during stop error as compared to stop success trials. These regions included a cluster in the VTA/substantia nigra (SN), internal segment of globus pallidus, bilateral amygdala, and insula. Furthermore, using Granger causality and mediation analyses, we showed that the habenula Granger caused the VTA/SN, establishing the direction of this interaction, and that the habenula mediated the functional connectivity between the amygdala and VTA/SN during error processing. To our knowledge, these findings are the first to demonstrate a feedforward influence of the habenula on the VTA/SN during error detection in humans.
Highlights
Using Granger causality and mediation analyses, we showed that the habenula Granger caused the ventral tegmental area (VTA)/substantia nigra (SN), establishing the direction of this interaction, and that the habenula mediated the functional connectivity between the amygdala and VTA/SN during error processing
The stop signal delay (SSD) – the time interval between the go and stop signal – started at 200 ms and varied from one stop trial to the according to a staircase procedure: if the subject succeeded in withholding the response, the SSD increased by 64 ms; if they failed, SSD decreased by 64 ms (Levitt, 1971)
The application of multivariate autoregressive (MAR) modeling required that each region of interest (ROI) time series was covariance stationary, which we examined with the Augmented Dickey Fuller (ADF) test (Hamilton, 1994)
Summary
Many studies in non-human primates described the role of the saliency/ reward pathway, involving the ventral tegmental area (VTA) and substantia nigra (SN), in outcome and error processing (Montague et al, 1996; Schultz et al, 1997; Holroyd and Coles, 2002; Schultz, 2002; Fiorillo et al, 2003; Bayer and Glimcher, 2005). Neurons in the VTA/SN increase activity to an unexpected reward and decrease activity to a missing reward. These roles of VTA/SN in error-related cognitive processes have recently been substantiated in humans (D’Ardenne et al, 2008; Carter et al, 2009; Duzel et al, 2009). Neurons in the habenula and midbrain were each excited and inhibited by no-reward-predicting targets; and electrical stimulation of lateral habenula (LH) decreased activity in the dopaminergic neurons (Matsumoto and Hikosaka, 2007)
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