Neural determinants of human goal-directed vs. habitual action control and their relation to trait motivation

Abstract

Instrumental learning is mediated by goal-directed and habit systems in the brain. While rodent studies implicate distinct prefrontal/striatal regions in goal-directed and habit learning, neural systems underpinning these two processes in humans remain poorly understood. Here, using a validated discrimination learning task that distinguishes goal-directed learning from habit learning in 72 subjects in fMRI, we investigated the corticostriatal correlates of goal-directed learning and tested whether brain activation during learning is associated with trait motivation and behavioral performance in the post-learning test phase. Participants showed enhanced activation in medial prefrontal and posterior cingulate cortices during goal-directed action selection in the training phase, whereas habitual action selection activated bilateral insula, bilateral dorsal caudate and left precentral gyrus. In addition, early phase of learning was associated with increased activation in the frontoparietal control network and dorsal striatum, whereas default mode regions depicted increased activation in the late phase. Finally, avoidance motivation scores measured by Behavioral Inhibition/Activation System (BIS/BAS) correlated with accuracy during goal-directed learning and showed a nominally significant correlation with activation in dorsomedial prefrontal cortex during goal-directed acquisition of stimuli. These findings reveal the temporal dynamics of instrumental behavior and suggest that avoidance motivation predicts performance and brain activity during goal-directed learning.

Conflicted between Goal-Directed and Habitual Control, an fMRI Investigation

“…In everyday life we need to override habitual response tendencies (triggered by familiar contexts) to behave flexibly. We show that this competition between goal-directed and habitual action relates to activation of brain regions previously implicated in conflict monitoring, rule learning and response inhibition as observed in the stop signal task ( Verbruggen and Logan, 2008 ), reversal learning ( Hampshire et al, 2012 ), instrumental discrimination tasks ( de Wit et al, 2009 ; de Wit et al, 2012 ; Sjoerds et al, 2013 ; Eryilmaz et al, 2017 ), and switch tasks ( Walton et al, 2010 ). The activation observed in ACC is similar to previous studies using a similar instrumental discrimination task, where response competition arises between O-R and S-R processes ( de Wit et al, 2009, 2012 ; Eryilmaz et al, 2017 ).…”

“…We show that this competition between goal-directed and habitual action relates to activation of brain regions previously implicated in conflict monitoring, rule learning and response inhibition as observed in the stop signal task ( Verbruggen and Logan, 2008 ), reversal learning ( Hampshire et al, 2012 ), instrumental discrimination tasks ( de Wit et al, 2009 ; de Wit et al, 2012 ; Sjoerds et al, 2013 ; Eryilmaz et al, 2017 ), and switch tasks ( Walton et al, 2010 ). The activation observed in ACC is similar to previous studies using a similar instrumental discrimination task, where response competition arises between O-R and S-R processes ( de Wit et al, 2009, 2012 ; Eryilmaz et al, 2017 ). Traditionally, fMRI activation in the (dorsal) ACC was attributed to this region’s role in top-down control processes, monitoring for response conflict and assigning cognitive resources as required when task difficulty increases ( Milham et al, 2003 ; Botvinick et al, 2004 ; Shenhav and Botvinick, 2015 ; Shenhav et al, 2016 ).…”

“…The putamen has been consistently reported in functional and structure MRI studies using outcome devaluation and sequential-decision-making (model based/model free) paradigms ( de Wit et al, 2012 ; Delorme et al, 2016 ; for meta-analysis, see Patterson and Knowlton, 2018 ). Likewise, vmPFC activation is often observed when contrasting O-R and S-R conditions ( Valentin et al, 2007 ; McNamee et al, 2015 ; Eryilmaz et al, 2017 ). There are a number of possible explanations for why the current study did not find activation in these regions.…”

Investigating resting brain perfusion abnormalities and disease target-engagement by intranasal oxytocin in women with bulimia nervosa and binge-eating disorder and healthy controls

“…In contrast to our hypotheses, we could not find any resting rCBF alterations in the ventral or dorsal striatum in patients with BN/BED. This is surprising, given the pivotal role of the striatal circuits in cognitive processes known to be disrupted in BN/BED (such as incentive and habitual behaviours 93 , impulsivity 94 and self-regulation 95 ) and previous neuroimaging studies demonstrating functional and structural abnormalities in these areas (see refs. 7,8 for detailed reviews).…”

Investigating resting brain perfusion abnormalities and target-engagement by intranasal oxytocin in women with bulimia nervosa and binge-eating disorder and healthy controls

“…In contrast to our hypotheses, we could not find any resting rCBF alterations in the ventral or dorsal striatum in patients with BN/BED. This is surprising, given the pivotal role of the striatal circuits in cognitive processes known to be disrupted in BN/BED (such as incentive and habitual behaviours 84 , impulsivity 85 and self-regulation 86 ) and previous neuroimaging studies demonstrating functional and structural abnormalities in these areas (see 7,8 for detailed reviews).…”