Optimal Balance of the Striatal Medium Spiny Neuron Network

Ponzi, Adam; Wickens, Jeffery R.

doi:10.1371/journal.pcbi.1002954

Cited by 45 publications

(104 citation statements)

References 140 publications

(152 reference statements)

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“…Computational studies suggest that networks of inhibitory neurons with realistic connectivity regimes for lateral inhibition reduce the level of activity, increase the contrast of responses, i.e., decorrelate striatal input [79,80], and can cause transitioning between striatal cell assemblies [32,81]. Although lateral inhibition is not the only mechanism by which neuronal network activity can be decorrelated [82], it can greatly enhance pattern decorrelation, as recently shown in a computational network model of neurons with threshold nonlinearities [33].…”

Section: Discussionmentioning

confidence: 99%

A Low-Correlation Resting State of the Striatum during Cortical Avalanches and Its Role in Movement Suppression

Klaus

Plenz

2016

PLoS Biol

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During quiet resting behavior, involuntary movements are suppressed. Such movement control is attributed to cortico-basal ganglia loops, yet population dynamics within these loops during resting and their relation to involuntary movements are not well characterized. Here, we show by recording cortical and striatal ongoing population activity in awake rats during quiet resting that intrastriatal inhibition maintains a low-correlation striatal resting state in the presence of cortical neuronal avalanches. Involuntary movements arise from disturbed striatal resting activity through two different population dynamics. Nonselectively reducing intrastriatal γ-aminobutyric acid (GABA) receptor-A inhibition synchronizes striatal dynamics, leading to involuntary movements at low rate. In contrast, reducing striatal interneuron (IN)-mediated inhibition maintains decorrelation and induces intermittent involuntary movements at high rate. This latter scenario was highly effective in modulating cortical dynamics at a subsecond timescale. To distinguish intrastriatal processing from loop dynamics, cortex-striatum-midbrain cultures, which lack feedback to cortex, were used. Cortical avalanches in vitro were accompanied by low-correlated resting activity in the striatum and nonselective reduction in striatal inhibition synchronized striatal neurons similar to in vivo. Importantly, reduction of inhibition from striatal INs maintained low correlations in the striatum while reorganizing functional connectivities among striatal neurons. Our results demonstrate the importance of two major striatal microcircuits in distinctly regulating striatal and cortical resting state dynamics. These findings suggest that specific functional connectivities of the striatum that are maintained by local inhibition are important in movement control.

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Section: Discussionmentioning

confidence: 99%

A Low-Correlation Resting State of the Striatum during Cortical Avalanches and Its Role in Movement Suppression

Klaus

Plenz

2016

PLoS Biol

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“…5), located in the striatum of the BG loop [96]. The sophisticated properties of the striatum include spiny projection neurons (SPNs) endowed with bistability and nonlinear amplification [102] and a sparse inhibitory network expressing complex dynamics [103]. Furthermore, the learning and performance of SPNs is modulated by reward prediction signals (purple diamond) sent from dopamine (DA) neurons in the midbrain.…”

Section: The Dpm Architecture For Learning and Control (J Houk)mentioning

confidence: 99%

Consensus Paper: Towards a Systems-Level View of Cerebellar Function: the Interplay Between Cerebellum, Basal Ganglia, and Cortex

et al. 2016

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Despite increasing evidence suggesting the cerebellum works in concert with the cortex and basal ganglia, the nature of the reciprocal interactions between these three brain regions remains unclear. This consensus paper gathers diverse recent views on a variety of important roles played by the cerebellum within the cerebello-basal ganglia-thalamo-cortical system across a range of motor and cognitive functions. The paper includes theoretical and empirical contributions, which cover the following topics: recent evidence supporting the dynamical interplay between cerebellum, basal ganglia, and cortical areas in humans and other animals; theoretical neuroscience perspectives and empirical evidence on the reciprocal influences between cerebellum, basal ganglia, and cortex in learning and control processes; and data suggesting possible roles of the cerebellum in basal ganglia movement disorders. Although starting from different backgrounds and dealing with different topics, all the contributors agree that viewing the cerebellum, basal ganglia, and cortex as an integrated system enables us to understand the function of these areas in radically different ways. In addition, there is unanimous consensus between the authors that future experimental and computational work is needed to understand the function of cerebellar-basal ganglia circuitry in both motor and non-motor functions. The paper reports the most advanced perspectives on the role of the cerebellum within the cerebello-basal ganglia-thalamo-cortical system and illustrates other elements of consensus as well as disagreements and open questions in the field.

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“…Information from D1-and D2-MSNs is ultimately relayed to the thalamus and the motor cortex 25 . Coordinated activation of D1-and D2-MSNs is crucial for action selection and inhibition of unwanted behaviors as well as to control the overall level of activity in the CSTC pathway 26,27 . Accordingly, reduced activity of D1-MSNs and increased activity of D2-MSNs generate a powerful inhibition of the motor cortex.…”

Section: Discussionmentioning

confidence: 99%

Global and local excitation and inhibition shape the dynamics of the cortico-striatal-thalamo-cortical pathway

Rǎdulescu

Herron

Kennedy

et al. 2017

Preprint

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The cortico-striatal-thalamo-cortical (CSTC) pathway is a brain circuit that controls movement execution, habit formation and reward. Hyperactivity in the CSTC pathway is involved in obsessive compulsive disorder (OCD), a neuropsychiatric disorder characterized by the execution of repetitive involuntary movements. The striatum shapes the activity of the CSTC pathway through the coordinated activation of two classes of medium spiny neurons (MSNs) expressing D1 or D2 dopamine receptors. The exact mechanisms by which balanced excitation/inhibition (E/I) of these cells controls the network dynamics of the CSTC pathway remain unclear. Here we use non-linear modeling of neuronal activity and bifurcation theory to investigate how global and local changes in E/I of MSNs regulate the activity of the CSTC pathway. Our findings indicate that a global and proportionate increase in E/I pushes the system to states of generalized hyper-activity throughout the entire CSTC pathway. Certain disproportionate changes in global E/I trigger network oscillations. Local changes in the E/I of MSNs generate specific oscillatory behaviors in MSNs and in the CSTC pathway. These findings indicate that subtle changes in the relative strength of E/I of MSNs can powerfully control the network dynamics of the CSTC pathway in ways that are not easily predicted by its synaptic connections.The cortico-striatal-thalamo-cortical (CSTC) pathway is a neuronal circuit that controls movement selection and initiation, reinforcement and reward 1 . Our current understanding of the wiring diagram of the CSTC pathway, based on functional neuroimaging studies, indicate that this circuit has an equivalent organization in rodents and humans of either sex and age (Fig. 1A,B) 2 . In normal conditions, oscillations and synchronous activity in distinct domains of the CSTC pathway are crucial to ensure the execution of habitual actions [3][4][5] . In contrast, hyperactivity in specific domains or throughout the circuit are thought to underlie the manifestation of obsessive compulsive disorder (OCD) and Tourette's syndrome 2,6 . The basal ganglia nucleus of the striatum plays an important role in regulating the activity of the CSTC pathway through the coordinated interplay of two populations of long-projections GABAergic neurons: the D1 and D2 dopamine receptor expressing medium spiny neurons (D1-and D2-MSNs, respectively) 3,7 . D1-MSNs project directly to the internal capsule of the globus pallidus (GPi) and the substantia nigra pars reticulata (SNr; Fig. 1C), whereas D2-MSNs project indirectly to the SNr by way of intermediate synaptic connections in the external capsule of the globus pallidus (GPe) and the sub-thalamic nucleus (STN; Fig. 1C). Activation of D1-MSNs facilitates movement initiation and activation of D2-MSNs inhibits initiation of competing actions 8,9 . Recent findings indicate that repetitive optogenetic activation of cortico-striatal glutamatergic afferents to the striatum triggers OCD-like behaviors in mice 10 , whereas optogenetic stimulation of ...

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Optimal Balance of the Striatal Medium Spiny Neuron Network

Cited by 45 publications

References 140 publications

A Low-Correlation Resting State of the Striatum during Cortical Avalanches and Its Role in Movement Suppression

A Low-Correlation Resting State of the Striatum during Cortical Avalanches and Its Role in Movement Suppression

Consensus Paper: Towards a Systems-Level View of Cerebellar Function: the Interplay Between Cerebellum, Basal Ganglia, and Cortex

Global and local excitation and inhibition shape the dynamics of the cortico-striatal-thalamo-cortical pathway

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