Dopamine Is Required for the Neural Representation and Control of Movement Vigor

Panigrahi, Babita; Martin, Kathleen A.; Li, Yang; Graves, Austin R; Vollmer, Alison; Olson, Lar̀s; Mensh, Brett D.; Karpova, Alla Y.; Dudman, Joshua T.

doi:10.1016/j.cell.2015.08.014

Cited by 264 publications

(353 citation statements)

References 47 publications

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“…For example, rodents may be trained to manipulate a lever by automatically rewarding them for correct movements (Slutzky et al, 2010;Panigrahi et al, 2015). The outcomes of such tasks are not necessarily discrete (as in, for example, a lever press task), as the amplitude and direction of the movement can be monitored.…”

Section: Discussionmentioning

confidence: 99%

An automated rat single pellet reaching system with high-speed video capture

Ellens

Gaidica

Toader

et al. 2016

Journal of Neuroscience Methods

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Background Single pellet reaching is an established task for studying fine motor control in which rats reach for, grasp, and eat food pellets in a stereotyped sequence. Most incarnations of this task require constant attention, limiting the number of animals that can be tested and the number of trials per session. Automated versions allow more interventions in more animals, but must be robust and reproducible. New Method Our system automatically delivers single reward pellets for rats to grasp with their forepaw. Reaches are detected using real-time computer vision, which triggers video acquisition from multiple angles using mirrors. This allows us to record high-speed (>300 frames per second) video, and trigger interventions (e.g., optogenetics) with high temporal precision. Individual video frames are triggered by digital pulses that can be synchronized with behavior, experimental interventions, or recording devices (e.g., electrophysiology). The system is housed within a soundproof chamber with integrated lighting and ventilation, allowing multiple skilled reaching systems in one room. Results We show that rats acquire the automated task similarly to manual versions, that the task is robust, and can be synchronized with optogenetic interventions. Comparison with existing methods Existing skilled reaching protocols require high levels of investigator involvement, or, if ad libitum, do not allow for integration of high-speed, synchronized data collection. Conclusion This task will facilitate the study of motor learning and control by efficiently recording large numbers of skilled movements. It can be adapted for use with modern neurophysiology, which demands high temporal precision.

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Section: Discussionmentioning

confidence: 99%

An automated rat single pellet reaching system with high-speed video capture

Ellens

Gaidica

Toader

et al. 2016

Journal of Neuroscience Methods

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“…Modulatory actions of DA mediate longer time-scale control of motivational salience, vigor and social behavior (52 Gunaydin, 2014, 1535–1551, 53). However, DA neurons mediate faster, discrete DA synaptic responses, in addition to volume transmission.…”

Section: Synaptic Dopamine Signaling In the Striatummentioning

confidence: 99%

Heterogeneity in Dopamine Neuron Synaptic Actions Across the Striatum and Its Relevance for Schizophrenia

Chuhma

Mingote

Kalmbach

et al. 2017

Biological Psychiatry

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Brain imaging has revealed alterations in dopamine uptake, release and receptor levels in patients with schizophrenia that have been resolved at the scale of striatal subregions. However, the underlying synaptic mechanisms are at a finer scale. Dopamine neuron synaptic actions vary across the striatum, involving not only variations in dopamine release, but also in dopamine neuron connectivity, cotransmission, modulation and activity. Optogenetic studies have revealed that dopamine neurons release dopamine in a synaptic signal mode, and that the neurons also release glutamate and GABA as cotransmitters, with striking regional variation. Fast glutamate and GABA cotransmission convey discrete patterns of dopamine neuron activity to striatal neurons. Glutamate may function not only in a signaling role at a subset of dopamine neuron synapses, but also in mediating vesicular synergy, contributing to regional differences in loading of dopamine into synaptic vesicles. Regional differences in dopamine neuron signaling are likely to be differentially involved in the schizophrenia disease process, and likely determine the subregional specificity of the action of psychostimulants that exacerbate the disorder, and antipsychotics that ameliorate the disorder. Elucidating dopamine neuron synaptic signaling offers the potential for achieving greater pharmacological specificity through intersectional pharmacological actions targeting subsets of dopamine neuron synapses.

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“…MitoPark mice, which have progressive loss of SN to DA dopamine neurons (Ekstrand et al, 2007), show impairments in this task, and optogenetic inhibition of the nigrostriatal pathway induced similar impairments such that subjects took longer to complete a criterion number of trials. Electrophysiological recording from the neurons in this region showed that DMS neurons appear to be both representing and controlling movement vigor in this task (Panigrahi et al, 2015). This is in line with another recent study which used a self-paced nose poking paradigm to demonstrate that overall reward payoff expectancy as well as response vigor appear to be represented in the DS (A.…”

Section: Activational Components Of Motivationmentioning

confidence: 99%

“…Drui et al, 2014). Specifically, recent experiments which monitor in vivo activity within the dorsal striatum in awake behaving animals performing motivated operant behavioral tasks have demonstrated that this region appears to be important for representing and modulating response vigor (Panigrahi et al, 2015; A. Y. Wang et al, 2013).…”

Section: Activational Components Of Motivationmentioning

confidence: 99%

Neural substrates underlying effort, time, and risk-based decision making in motivated behavior

Bailey

Simpson

Balsam

2016

Neurobiology of Learning and Memory

103

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All mobile organisms rely on adaptive motivated behavior to overcome the challenges of living in an environment in which essential resources may be limited. A variety of influences ranging from an organism’s environment, experiential history, and physiological state all influence a cost-benefit analysis which allows motivation to energize behavior and direct it toward specific goals. Here we review the substantial amount of research aimed at discovering the interconnected neural circuits which allow organisms to carry-out the cost-benefit computations which allow them to behave in adaptive ways. We specifically focus on how the brain deals with different types of costs, including effort requirements, delays to reward and payoff riskiness. An examination of this broad literature highlights the importance of the extended neural circuits which enable organisms to make decisions about these different types of costs. This involves Cortical Structures, including the Anterior Cingulate Cortex (ACC), the Orbital Frontal Cortex (OFC), the Infralimbic Cortex (IL), and prelimbic Cortex (PL), as well as the Baso-Lateral Amygdala (BLA), the Nucleus Accumbens (Nacc), the Ventral Pallidal (VP), the Sub Thalamic Nucleus (STN) among others. Some regions are involved in multiple aspects of cost-benefit computations while the involvement of other regions is restricted to information relating to specific types of costs.

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Dopamine Is Required for the Neural Representation and Control of Movement Vigor

Cited by 264 publications

References 47 publications

An automated rat single pellet reaching system with high-speed video capture

An automated rat single pellet reaching system with high-speed video capture

Heterogeneity in Dopamine Neuron Synaptic Actions Across the Striatum and Its Relevance for Schizophrenia

Neural substrates underlying effort, time, and risk-based decision making in motivated behavior

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