Recent evidence suggests that the learning processes that underlie the acquisition of goal-directed actions and that support their transition into habits are encoded within distinct regions of the dorsal striatum and involve distinct cortio-striatal networks. Disorders of `voluntary'movement, e.g. Parkinson's disease, and involving intrusive involuntary movement, e.g. Tourette's syndrome, obsessive compulsive disorder and Huntingdon's disease, have also been found to involve damage to cortico-striatal networks and to result in severe cognitive deficits in choice, planning and executive processes generally. These cases make it clear that the capacity for goal-directed action is highly adaptive. Nevertheless, although research into the physiological systems that subserve learning processes in humans and other animals has been of ongoing concern to the neuroscience research community, the neural bases of both goal-directed and habit learning are still very poorly understood. The broad, long-term objective of the current project is, therefore, to understand the neural systems that control both goal-directed and habitual learning processes. In this project we will focus specifically on cortio-striatal networks involving the medial prefrontal cortex and its efferents to the dorsomedial striatum in goal-directed learning and sensorimotor cortex and its afferents to dorsolateral striatum in habit learning under three specific aims: (i) to examine the role of the dorsomedial striatum in goal-directed learning processes;(ii) to explore the role of cortico-dorsomedial striatal circuits in goal-directed learning;and (iii) to compare the role of dorsomedial and dorsolateral striatum in actions and habits. We plan to use behavioral manipulations and tests that allow direct assessment of the specific learning processes engaged under a number of circumstances and to establish the neural networks that support these learning processes using a series of molecular and cellular markers and interventions that, in recent years, have proven to be of value in studying neural circuits and systems.

Public Health Relevance

The learning processes that underlie the acquisition of goal-directed actions and that support their transition into habits are encoded within distinct regions of the dorsal striatum and involve distinct cortio-striatal networks. Disorders of `voluntary'movement, e.g. Parkinson's disease, and involving intrusive involuntary movement, e.g. Tourette's syndrome, obsessive compulsive disorder and Huntingdon's disease, have also been found to involve damage to cortico-striatal networks and to result in severe cognitive deficits in choice, planning and executive processes generally. These cases make it clear that the capacity for goal-directed action is highly adaptive. Nevertheless, the neural bases of both goal-directed and habit learning are still very poorly understood. The broad, long-term objective of the current project is, therefore, to understand the neural systems that control both goal-directed and habitual learning processes. In this project we will focus specifically on cortio-striatal networks involving the medial prefrontal cortex and the dorsomedial striatum in goal-directed learning and sensorimotor cortex and its afferents to dorsolateral striatum in habit learning. We plan to use behavioral manipulations and tests that allow direct assessment of the specific learning processes engaged under a number of circumstances and to establish the neural networks that support these learning processes using molecular and cellular approaches that have proven of value in studying neural circuits and systems.

Agency
National Institute of Health (NIH)
Institute
Eunice Kennedy Shriver National Institute of Child Health & Human Development (NICHD)
Type
Research Project (R01)
Project #
5R01HD059257-05
Application #
8072076
Study Section
Neurobiology of Learning and Memory Study Section (LAM)
Program Officer
Nitkin, Ralph M
Project Start
2008-04-01
Project End
2013-03-31
Budget Start
2011-04-01
Budget End
2012-03-31
Support Year
5
Fiscal Year
2011
Total Cost
$184,758
Indirect Cost
Name
University of Sydney
Department
Type
DUNS #
752389338
City
Sydney
State
Country
Australia
Zip Code
2006
Furlong, Teri M; Corbit, Laura H; Brown, Robert A et al. (2018) Methamphetamine promotes habitual action and alters the density of striatal glutamate receptor and vesicular proteins in dorsal striatum. Addict Biol 23:857-867
Dezfouli, Amir; Balleine, Bernard W (2013) Actions, action sequences and habits: evidence that goal-directed and habitual action control are hierarchically organized. PLoS Comput Biol 9:e1003364
Lingawi, Nura W; Balleine, Bernard W (2012) Amygdala central nucleus interacts with dorsolateral striatum to regulate the acquisition of habits. J Neurosci 32:1073-81
Shiflett, Michael W; Balleine, Bernard W (2011) Molecular substrates of action control in cortico-striatal circuits. Prog Neurobiol 95:1-13
Ostlund, Sean B; Wassum, Kate M; Murphy, Niall P et al. (2011) Extracellular dopamine levels in striatal subregions track shifts in motivation and response cost during instrumental conditioning. J Neurosci 31:200-7
Shiflett, Michael W; Balleine, Bernard W (2011) Contributions of ERK signaling in the striatum to instrumental learning and performance. Behav Brain Res 218:240-7
Balleine, Bernard W; O'Doherty, John P (2010) Human and rodent homologies in action control: corticostriatal determinants of goal-directed and habitual action. Neuropsychopharmacology 35:48-69
Shiflett, Michael W; Brown, Robert A; Balleine, Bernard W (2010) Acquisition and performance of goal-directed instrumental actions depends on ERK signaling in distinct regions of dorsal striatum in rats. J Neurosci 30:2951-9
Shiflett, Michael W; Balleine, Bernard W (2010) At the limbic-motor interface: disconnection of basolateral amygdala from nucleus accumbens core and shell reveals dissociable components of incentive motivation. Eur J Neurosci 32:1735-43
Ostlund, Sean B; Winterbauer, Neil E; Balleine, Bernard W (2009) Evidence of action sequence chunking in goal-directed instrumental conditioning and its dependence on the dorsomedial prefrontal cortex. J Neurosci 29:8280-7

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