scholarly journals Unveiling the neural correlates of habit in the dorsal striatum

2021 ◽  
Author(s):  
Youna Vandaele ◽  
Patricia H Janak

We have recently reported sustained inhibition in the dorsomedial striatum (DMS) and sustained excitation in the dorsolateral striatum (DLS) during execution of a lever press sequence in a discrete-trials task promoting habit. This sustained dorsostriatal activity was present early on, and did not clearly change in step with improved performance over ten training sessions. Early onset of sequence-related neural activity could have resulted from rapid habitual learning promoted by presentation of lever cues, predicting reward availability and delivery. To test this hypothesis, we compared DLS and DMS spiking activity in the discrete trials habit-promoting task with two task variants that promote goal-directed behavior. Comparison of the three tasks revealed that mean neuronal spiking activity was generally sustained across the lever press sequence in the task promoting habit and characterized by overall excitation in DLS and inhibition in DMS relative to baseline. In contrast, mean activity differences in DLS and DMS were much less prominent, and most changes occurred transiently around individual lever presses, in the tasks promoting goal-directed behavior. These results indicate that sequence delineation cues, such as the lever cues in these studies, promote habitual behavior and that this habitual behavior is encoded in the striatum by cue-triggered sustained DLS excitation and DMS inhibition that likely reflects cue-elicited behavioral chunking.

2021 ◽  
Vol 12 (1) ◽  
Author(s):  
Meizhu Huang ◽  
Dapeng Li ◽  
Xinyu Cheng ◽  
Qing Pei ◽  
Zhiyong Xie ◽  
...  

AbstractAppetitive locomotion is essential for animals to approach rewards, such as food and prey. The neuronal circuitry controlling appetitive locomotion is unclear. In a goal-directed behavior—predatory hunting, we show an excitatory brain circuit from the superior colliculus (SC) to the substantia nigra pars compacta (SNc) to enhance appetitive locomotion in mice. This tectonigral pathway transmits locomotion-speed signals to dopamine neurons and triggers dopamine release in the dorsal striatum. Synaptic inactivation of this pathway impairs appetitive locomotion but not defensive locomotion. Conversely, activation of this pathway increases the speed and frequency of approach during predatory hunting, an effect that depends on the activities of SNc dopamine neurons. Together, these data reveal that the SC regulates locomotion-speed signals to SNc dopamine neurons to enhance appetitive locomotion in mice.


2015 ◽  
Vol 112 (30) ◽  
pp. 9472-9477 ◽  
Author(s):  
David E. Moorman ◽  
Gary Aston-Jones

The prefrontal cortex (PFC) guides execution and inhibition of behavior based on contextual demands. In rodents, the dorsal/prelimbic (PL) medial PFC (mPFC) is frequently considered essential for execution of goal-directed behavior (“go”) whereas ventral/infralimbic (IL) mPFC is thought to control behavioral suppression (“stop”). This dichotomy is commonly seen for fear-related behaviors, and for some behaviors related to cocaine seeking. Overall, however, data for reward-directed behaviors are ambiguous, and few recordings of PL/IL activity have been performed to demonstrate single-neuron correlates. We recorded neuronal activity in PL and IL during discriminative stimulus driven sucrose seeking followed by multiple days of extinction of the reward-predicting stimulus. Contrary to a generalized PL-go/IL-stop hypothesis, we found cue-evoked activity in PL and IL during reward seeking and extinction. Upon analyzing this activity based on resultant behavior (lever press or withhold), we found that neurons in both areas encoded contextually appropriate behavioral initiation (during reward seeking) and withholding (during extinction), where context was dictated by response–outcome contingencies. Our results demonstrate that PL and IL signal contextual information for regulation of behavior, irrespective of whether that involves initiation or suppression of behavioral responses, rather than topographically encoding go vs. stop behaviors. The use of context to optimize behavior likely plays an important role in maximizing utility-promoting exertion of activity when behaviors are rewarded and conservation of energy when not.


2011 ◽  
Vol 23 (5) ◽  
pp. 1218-1229 ◽  
Author(s):  
Sanne de Wit ◽  
Roger A. Barker ◽  
Anthony D. Dickinson ◽  
Roshan Cools

This study presents the first direct investigation of the hypothesis that dopamine depletion of the dorsal striatum in mild Parkinson disease leads to impaired stimulus–response habit formation, thereby rendering behavior slow and effortful. However, using an instrumental conflict task, we show that patients are able to rely on direct stimulus–response associations when a goal-directed strategy causes response conflict, suggesting that habit formation is not impaired. If anything our results suggest a disease severity–dependent deficit in goal-directed behavior. These results are discussed in the context of Parkinson disease and the neurobiology of habitual and goal-directed behavior.


2006 ◽  
Vol 120 (1) ◽  
pp. 196-200 ◽  
Author(s):  
Siobhan Robinson ◽  
Bethany N. Sotak ◽  
Matthew J. During ◽  
Richard D. Palmiter

2011 ◽  
Vol 23 (11) ◽  
pp. 3620-3636 ◽  
Author(s):  
David B. Miele ◽  
Tor D. Wager ◽  
Jason P. Mitchell ◽  
Janet Metcalfe

Judgments of agency refer to people's self-reflective assessments concerning their own control: their assessments of the extent to which they themselves are responsible for an action. These self-reflective metacognitive judgments can be distinguished from action monitoring, which involves the detection of the divergence (or lack of divergence) between observed states and expected states. Presumably, people form judgments of agency by metacognitively reflecting on the output of their action monitoring and then consciously inferring the extent to which they caused the action in question. Although a number of previous imaging studies have been directed at action monitoring, none have assessed judgments of agency as a potentially separate process. The present fMRI study used an agency paradigm that not only allowed us to examine the brain activity associated with action monitoring but that also enabled us to investigate those regions associated with metacognition of agency. Regarding action monitoring, we found that being “out of control” during the task (i.e., detection of a discrepancy between observed and expected states) was associated with increased brain activity in the right TPJ, whereas being “in control” was associated with increased activity in the pre-SMA, rostral cingulate zone, and dorsal striatum (regions linked to self-initiated action). In contrast, when participants made self-reflective metacognitive judgments about the extent of their own control (i.e., judgments of agency) compared with when they made judgments that were not about control (i.e., judgments of performance), increased activity was observed in the anterior PFC, a region associated with self-reflective processing. These results indicate that action monitoring is dissociable from people's conscious self-attributions of control.


2006 ◽  
Vol 95 (2) ◽  
pp. 948-959 ◽  
Author(s):  
Masahiko Haruno ◽  
Mitsuo Kawato

To select appropriate behaviors leading to rewards, the brain needs to learn associations among sensory stimuli, selected behaviors, and rewards. Recent imaging and neural-recording studies have revealed that the dorsal striatum plays an important role in learning such stimulus-action-reward associations. However, the putamen and caudate nucleus are embedded in distinct cortico-striatal loop circuits, predominantly connected to motor-related cerebral cortical areas and frontal association areas, respectively. This difference in their cortical connections suggests that the putamen and caudate nucleus are engaged in different functional aspects of stimulus-action-reward association learning. To determine whether this is the case, we conducted an event-related and computational model–based functional MRI (fMRI) study with a stochastic decision-making task in which a stimulus-action-reward association must be learned. A simple reinforcement learning model not only reproduced the subject's action selections reasonably well but also allowed us to quantitatively estimate each subject's temporal profiles of stimulus-action-reward association and reward-prediction error during learning trials. These two internal representations were used in the fMRI correlation analysis. The results revealed that neural correlates of the stimulus-action-reward association reside in the putamen, whereas a correlation with reward-prediction error was found largely in the caudate nucleus and ventral striatum. These nonuniform spatiotemporal distributions of neural correlates within the dorsal striatum were maintained consistently at various levels of task difficulty, suggesting a functional difference in the dorsal striatum between the putamen and caudate nucleus during stimulus-action-reward association learning.


2015 ◽  
Vol 114 (3) ◽  
pp. 1399-1416 ◽  
Author(s):  
Paul S. Regier ◽  
Seiichiro Amemiya ◽  
A. David Redish

Goal-directed and habit-based behaviors are driven by multiple but dissociable decision making systems involving several different brain areas, including the hippocampus and dorsal striatum. On repetitive tasks, behavior transitions from goal directed to habit based with experience. Hippocampus has been implicated in initial learning and dorsal striatum in automating behavior, but recent studies suggest that subregions within the dorsal striatum have distinct roles in mediating habit-based and goal-directed behavior. We compared neural activity in the CA1 region of hippocampus with anterior dorsolateral and posterior dorsomedial striatum in rats on a spatial choice task, in which subjects experienced reward delivery changes that forced them to adjust their behavioral strategy. Our results confirm the importance of the hippocampus in evaluating predictive steps during goal-directed behavior, while separate circuits in the basal ganglia integrated relevant information during automation of actions and recognized when new behaviors were needed to continue obtaining rewards.


2009 ◽  
Vol 36 (11) ◽  
pp. 1141-1157 ◽  
Author(s):  
Katherine E. Shannon ◽  
Colin Sauder ◽  
Theodore P. Beauchaine ◽  
Lisa M. Gatzke-Kopp

Studies addressing the neural correlates of criminal behavior have focused primarily on the prefrontal cortex and the amygdala. However, few studies have examined dopaminergic inputs to these or other brain regions, despite the fact that central dopamine (DA) dysfunction is associated with both trait impulsivity and novelty seeking. Given long-standing associations between both of these personality traits and externalizing psychopathology, the authors examined effective connectivity between the caudate nucleus and the anterior cingulate cortex, two areas that rely on DA input to facilitate associative learning and goal directed behavior. Dysfunction in top-down and bottom-up processing within this dopaminergically mediated frontostriatal circuit may be an important biological vulnerability that increases one’s likelihood of engaging in delinquent and criminal behavior. When compared with controls, reduced effective connectivity between these regions among adolescents with externalizing psychopathology was found, suggesting deficiencies in frontostriatal circuitry.


2021 ◽  
Vol 11 (3) ◽  
pp. 368
Author(s):  
Jae-Hwan Kang ◽  
Junsuk Kim ◽  
Yang Seok Cho ◽  
Sung-Phil Kim

The human brain carries out cognitive control for the inhibition of habitual behaviors by suppressing some familiar but inappropriate behaviors instead of engaging specific goal-directed behavior flexibly in a given situation. To examine the characteristics of neural dynamics related to such inhibition of habitual behaviors, we used a modified rock–paper–scissors (RPS) task that consisted of a basic, a lose-, and a win-conditioned game. Spectral and phase synchrony analyses were conducted to examine the acquired electroencephalogram signals across the entire brain during all RPS tasks. Temporal variations in frontal theta power activities were directly in line with the stream of RPS procedures in accordance with the task conditions. The lose-conditioned RPS task gave rise to increases in the local frontal power and global phase-synchronized pairs of theta oscillations. The activation of the global phase-synchronized network preceded the activation of frontal theta power. These results demonstrate that the frontal regions play a pivotal role in the inhibition of habitual behaviors—stereotyped and ingrained stimulus–response mappings that have been established over time. This study suggests that frontal theta oscillations may be engaged during the cognitive inhibition of habitual behaviors and that these oscillations characterize the degree of cognitive load required to inhibit habitual behaviors.


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