The role of the substantia nigra in posture control

Barter, Joseph W.; Castro, Stephen; Sukharnikova, Tatyana; Rossi, Mark A.; Yin, Henry H.

doi:10.1111/ejn.12540

Cited by 52 publications

(46 citation statements)

References 39 publications

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“…However, recent reports suggest that the firing of putative dopaminergic neurons in both rodents and primates is altered during trained movements (12)(13)(14)(15). Our data show that the activity of identified dopaminergic neurons (in the SNc, VTA, and SNL) also changes around the spontaneous movements made by untrained mice in the absence of any overt cues or reward.…”

Section: Discussionsupporting

confidence: 46%

“…For example, some dopaminergic neurons respond to novel or salient events or during cognitive processes such as decision making and working memory (6,(8)(9)(10). Moreover, although the firing of these dopaminergic neurons generally has been thought not to vary consistently with movement (3,11), there is evidence that the activity of putatively classified dopaminergic neurons can change during movement execution in a heterogeneous manner (12)(13)(14)(15)(16). This evidence, in turn, raises the possibilities that at least some types of movement might be differentially encoded by the firing of distinct populations of dopaminergic neuron and that dysregulation of such activity might contribute to motor impairment in PD before, or commensurate with, frank neurodegeneration.…”

mentioning

confidence: 99%

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Representation of spontaneous movement by dopaminergic neurons is cell-type selective and disrupted in parkinsonism

Dodson

Dreyer

Jennings

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

167

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Midbrain dopaminergic neurons are essential for appropriate voluntary movement, as epitomized by the cardinal motor impairments arising in Parkinson's disease. Understanding the basis of such motor control requires understanding how the firing of different types of dopaminergic neuron relates to movement and how this activity is deciphered in target structures such as the striatum. By recording and labeling individual neurons in behaving mice, we show that the representation of brief spontaneous movements in the firing of identified midbrain dopaminergic neurons is cell-type selective. Most dopaminergic neurons in the substantia nigra pars compacta (SNc), but not in ventral tegmental area or substantia nigra pars lateralis, consistently represented the onset of spontaneous movements with a pause in their firing. Computational modeling revealed that the movement-related firing of these dopaminergic neurons can manifest as rapid and robust fluctuations in striatal dopamine concentration and receptor activity. The exact nature of the movement-related signaling in the striatum depended on the type of dopaminergic neuron providing inputs, the striatal region innervated, and the type of dopamine receptor expressed by striatal neurons. Importantly, in aged mice harboring a genetic burden relevant for human Parkinson's disease, the precise movement-related firing of SNc dopaminergic neurons and the resultant striatal dopamine signaling were lost. These data show that distinct dopaminergic cell types differentially encode spontaneous movement and elucidate how dysregulation of their firing in early Parkinsonism can impair their effector circuits.opamine is vital for normal motor function, as exemplified by the motor deficits arising from the dysfunction/degeneration of midbrain dopaminergic neurons in Parkinson's disease (PD). One prevailing view is that midbrain dopaminergic neurons guide purposeful actions through encoding value, for example, by conveying the difference between expected and actual reward (1-3). Although this function has been ascribed to all midbrain dopaminergic neurons, there is considerable functional heterogeneity across different cell populations in the ventral tegmental area (VTA; A10) and the substantia nigra pars compacta (SNc; A9) (4-7). For example, some dopaminergic neurons respond to novel or salient events or during cognitive processes such as decision making and working memory (6,(8)(9)(10). Moreover, although the firing of these dopaminergic neurons generally has been thought not to vary consistently with movement (3, 11), there is evidence that the activity of putatively classified dopaminergic neurons can change during movement execution in a heterogeneous manner (12-16). This evidence, in turn, raises the possibilities that at least some types of movement might be differentially encoded by the firing of distinct populations of dopaminergic neuron and that dysregulation of such activity might contribute to motor impairment in PD before, or commensurate with, frank neurodegeneration.To ...

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Section: Discussionsupporting

confidence: 46%

mentioning

confidence: 99%

Representation of spontaneous movement by dopaminergic neurons is cell-type selective and disrupted in parkinsonism

Dodson

Dreyer

Jennings

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

167

View full text Add to dashboard Cite

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“…The standard rate model conflates movement amplitude and speed, claiming that the excessively high firing rate of SNr/GPi neurons is responsible for parkinsonian symptoms like bradykinesia (slowed movement) and akinesia (Albin et al, 1989;DeLong, 1990). According to our model, these symptoms cannot be explained by excessive BG output; rather, they are attributed to a reduction in the rate of change in the firing rate of BG output nuclei.…”

Section: Bg Output and Transition Controlmentioning

confidence: 84%

“…According to the most popular model of BG function, a decrease in the inhibitory BG output enables movements, whereas an increase in the output prevents movements (Albin et al, 1989;DeLong, 1990;Hikosaka et al, 2000). Although this model is supported by a number of studies (Hikosaka et al, 2000), other observations seem to be incompatible with the disinhibition hypothesis.…”

Section: Introductionmentioning

confidence: 99%

Basal Ganglia Outputs Map Instantaneous Position Coordinates during Behavior

Barter

Li²,

Sukharnikova³

et al. 2015

J. Neurosci.

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The basal ganglia (BG) are implicated in many movement disorders, yet how they contribute to movement remains unclear. Using wireless in vivo recording, we measured BG output from the substantia nigra pars reticulata (SNr) in mice while monitoring their movements with video tracking. The firing rate of most nigral neurons reflected Cartesian coordinates (either x-or y-coordinates) of the animal's head position during movement. The firing rates of SNr neurons are either positively or negatively correlated with the coordinates. Using an egocentric reference frame, four types of neurons can be classified: each type increases firing during movement in a particular direction (left, right, up, down), and decreases firing during movement in the opposite direction. Given the high correlation between the firing rate and the x and y components of the position vector, the movement trajectory can be reconstructed from neural activity. Our results therefore demonstrate a quantitative and continuous relationship between BG output and behavior. Thus, a steady BG output signal from the SNr (i.e., constant firing rate) is associated with the lack of overt movement, when a stable posture is maintained by structures downstream of the BG. Any change in SNr firing rate is associated with a change in position (i.e., movement). We hypothesize that the SNr output quantitatively determines the direction, velocity, and amplitude of voluntary movements. By changing the reference signals to downstream position control systems, the BG can produce transitions in body configurations and initiate actions.

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“…The substantia nigra is an important player in particular for control of eye movement, motor planning, reward seeking, or learning. Moreover, as the thalamus can be considered as a relay between the sensory systems and the cortex, indirect impairment of the thalamus caused by the dysfunction of the substantia nigra alters sensory perceptions Barter et al, 2014).…”

Section: E Parkinson's Diseasementioning

confidence: 99%