Motor Control by Sensory Cortex

Mátyás, Ferenc; Sreenivasan, Varun; Marbach, Fred; Wacongne, Catherine; Barsy, Boglárka; Matéo, Céline; Aronoff, Rachel; Petersen, Carl C. H.

doi:10.1126/science.1195797

Cited by 345 publications

(323 citation statements)

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“…To test this, we generated a dendritic plateau potential by activating the clustered excitatory inputs within a short time window using the model SPN. Then a group of 20 synapses, in addition to spontaneous synaptic background noise, were randomly distributed in the dendrites and each synapse activated independently with high-frequency activity (10 Hz in a Poisson distribution) to mimic cortical activity (38). To avoid potential biases on the spatial locations of the synapses, which may perturb statistics, we generated a large sample pool with 1,000 unbiased distribution patterns ( Fig.…”

Section: Dendritic Plateau Potentials Broaden the Spatiotemporal Windmentioning

confidence: 99%

Cell-type–specific inhibition of the dendritic plateau potential in striatal spiny projection neurons

Lindroos

et al. 2017

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

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Striatal spiny projection neurons (SPNs) receive convergent excitatory synaptic inputs from the cortex and thalamus. Activation of spatially clustered and temporally synchronized excitatory inputs at the distal dendrites could trigger plateau potentials in SPNs. Such supralinear synaptic integration is crucial for dendritic computation. However, how plateau potentials interact with subsequent excitatory and inhibitory synaptic inputs remains unknown. By combining computational simulation, two-photon imaging, optogenetics, and dualcolor uncaging of glutamate and GABA, we demonstrate that plateau potentials can broaden the spatiotemporal window for integrating excitatory inputs and promote spiking. The temporal window of spiking can be delicately controlled by GABAergic inhibition in a celltype-specific manner. This subtle inhibitory control of plateau potential depends on the location and kinetics of the GABAergic inputs and is achieved by the balance between relief and reestablishment of NMDA receptor Mg 2+ block. These findings represent a mechanism for controlling spatiotemporal synaptic integration in SPNs.O ne of the principal functions of neurons is to integrate excitatory and inhibitory synaptic inputs and transform subthreshold membrane potential fluctuations into suprathreshold spiking activities. Both theoretical and experimental works have proposed that a single neuron can process inputs as a multilayer computational device in which individual dendritic branches function as a computational unit and can generate dendritic spikes or plateau potentials (1-4). In vivo studies have demonstrated that dendritic plateau potentials evoked by coincident inputs can amplify excitatory signals and enhance the capacity of learning and information storage at a specific branch (5-7). However, a majority of the understanding of dendritic computation is based on studies focusing on pyramidal cells of hippocampal and cortical areas. It is relatively less known whether these conclusions apply to the striatal neurons (8).The striatum, the main input nucleus of the basal ganglia, receives convergent glutamatergic inputs from the cortex and thalamus (9-11). The integration of these functionally distinct inputs is critical for fine movement control and action selection (12, 13). The principal neurons in the striatum-spiny projection neurons (SPNs)-display hyperpolarized membrane potentials (∼−80 mV) at rest, often referred to as the "down-state" (14, 15). It is generally believed that coherent cortical inputs can effectively depolarize SPNs and promote membrane potential transitions from a hyperpolarized down-state to a depolarized "up-state" (∼−55 mV), at which point action potentials can be generated (14-16). To achieve this ∼20-to 30-mV state transition, it has been estimated that a large number (hundreds to thousands) of active inputs would be required (14-17). Interestingly, striatal SPNs are capable of producing long-lasting plateau potentials following activation of spatially clustered and temporally synchronized excit...

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Section: Dendritic Plateau Potentials Broaden the Spatiotemporal Windmentioning

confidence: 99%

Cell-type–specific inhibition of the dendritic plateau potential in striatal spiny projection neurons

Lindroos

et al. 2017

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

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“…This central observation complements a large body of physiological studies in the rodent vibrissal system on the integration of touch and movement (e.g., Ferezou et al 2007;Lee et al 2013;Matyas et al 2010;Zagha et al 2013) by demonstrating a clear functional consequence of such integration in healthy humans.…”

Section: Discussionmentioning

confidence: 85%

“…Whereas the existence of several pathways for somatosensory processing in humans had previously been reported (see Dijkerman and de Haan 2007), we were particularly inspired by recent physiological evidence in rodents supporting additional, more direct, pathways between somatosensory and motor areas of the brain (see Ferezou et al 2007;Lee et al 2013;Matyas et al 2010;Zagha et al 2013). We hypothesized that through state changes propagating along these pathways (see Maris 2013 andZagha et al 2013) tactile input may automatically influence the corresponding motor areas and thereby facilitate movements of the stimulated effector.…”

Section: Discussionmentioning

confidence: 99%

“…For example, stimulation of rodent primary motor cortex (M1) influences the physiological state of the primary somatosensory cortex (S1) through a direct pathway from M1 to S1, and this improves sensory processing (Lee et al 2013;Zagha et al 2013). Likewise, sensory responses and state changes in S1 propagate to M1 (Ferezou et al 2007) as well as the spinal cord (van Ede and Maris 2013) and may even contribute to motor control directly (Coulter and Jones 1977;Matyas et al 2010). To date, however, the behavioral consequences of such tactile-induced state changes of the motor system have remained largely unexplored.…”

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confidence: 99%

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Touch automatically upregulates motor readiness in humans

Ede

Winner

Maris

2015

Journal of Neurophysiology

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van Ede F, Winner T, Maris E. Touch automatically upregulates motor readiness in humans. J Neurophysiol 114: 3121-3130, 2015. First published September 23, 2015 doi:10.1152/jn.00504.2015.-Goal-directed movements require effective integration of tactile input with ongoing movement. Here we investigated the functional consequences of such integration in healthy humans by probing the influence of spatially congruent and incongruent tactile stimuli on performance in a speeded button-press task. In addition, using magnetoencephalography (MEG), we evaluated whether the modulation of somato-motor beta (13-30 Hz) oscillations following tactile inputwhich has been shown to propagate to motor areas-could underlie this influence. We demonstrate that congruent tactile stimuli, despite being irrelevant to the motor task, lead to both faster and more accurate responses. We further show that this automatic upregulation of lateralized motor readiness 1) is specific to tactile input, 2) is independent of the spatial separation of the hands in peripersonal space, and 3) lasts (and remains facilitatory) for up to a second after the tactile input. This pattern of behavioral results is in line with recent physiological investigations showing that somatosensory and motor areas directly influence each other's processing capacity through joint changes in brain state. At the same time, however, the tactile-induced modulation of beta oscillations (one particular index of such a somatomotor state change) could not account for the observed movement facilitation, because it had a different time course. tactile stimuli; movement; sensorimotor integration; beta oscillations; automatic facilitation GOAL-DIRECTED MOVEMENTS require effective interactions between the brain's somatosensory and motor areas. Recent physiological studies have suggested that such interactions are facilitated by the direct influence of somatosensory areas on motor areas, and vice versa. For example, stimulation of rodent primary motor cortex (M1) influences the physiological state of the primary somatosensory cortex (S1) through a direct pathway from M1 to S1, and this improves sensory processing (Lee et al. 2013;Zagha et al. 2013). Likewise, sensory responses and state changes in S1 propagate to M1 (Ferezou et al. 2007) as well as the spinal cord (van Ede and Maris 2013) and may even contribute to motor control directly (Coulter and Jones 1977;Matyas et al. 2010). To date, however, the behavioral consequences of such tactile-induced state changes of the motor system have remained largely unexplored. Moreover, most previous inferences on the integration between touch and movement (including the involvement of somato-motor state changes) have been based on animal (i.e., rodent) models. In the present work, we therefore aimed at characterizing the influence of touch on movement in healthy humans. In particular, we investigated the influence of external tactile stimuli on motor readiness: the ability to respond quickly to an arbitrary response signal (imperative cue).Our...

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“…Observations between Medetomidine0.1 and Isoflurane1 as well as Mediso within the primary somatosensory barrel field cortex appear to support this. The somatosensory cortices play important roles in sensory information flow as well as movement planning and execution, while posterior areas include associative cortical functions (Matyas et al, 2010;Watson et al, 2011). Significantly reduced ReHo in the primary somatosensory barrel field cortex under Urethane1.5 in comparison to Isoflurane1 and Mediso led to consideration of the pharmacological mechanism mentioned above as one plausible explanation.…”

Section: Discussionmentioning

confidence: 99%

Functional network study on the wild type and DISC1 transgenic mice

Wu¹

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Major mental disorders such as schizophrenia (SZ), bipolar disorder and major depression create a heavy social burden and remain poorly treated. Recent reports examining the genetic and molecular structure of brain disorders discovered the gene Disrupted-in-Schizophrenia 1 (DISC1) to be significantly associated with these disorders and plays a substantial role in influencing a range of shared endophenotypes underlying these disorders. This has led to a powerful gateway to explore the underlying pathology and to achieve better diagnosis and treatments of major mental diseases. Characterising the phenotypes of DISC1 in brain functions would provide valuable insights into the mechanism of how this gene influences the brain.Resting-state fMRI (rs-fMRI) is a powerful technique being applied to more than 30 different kinds of brain disorders and different species. Findings from rs-fMRI studies on humans provide ample evidence of abnormal functional patterns in patients with mental illnesses. Specifically, altered functional connectivity (FC) and network topologies are proposed to be plausible imaging endophenotypes of psychotic disorders. However, little is known about the direct effects of gene dysfunction, such as DISC1 mutations, on restingstate brain activations. One aim of this thesis is to investigate the impacts of DISC1 on variations of resting-state functional networks (RSNs) in anaesthetized mouse brains using DISC1 transgenic mice and rs-fMRI.Before characterizing disease phenotypes in mouse models, it is necessary to understand how the mouse brain functions in normal states. Anaesthesia is currently an integrated part of most mouse rs-fMRI experiment. However, it influences blood-oxygenation-leveldependent (BOLD) fMRI signals via modulation of neurovascular coupling and brain metabolism, and therefore alters FC and topologies of RSNs. Investigating FC and its changes associated with genes therefore initially requires an understanding of the anaesthetics. Furthermore, various anaesthetic protocols are adopted by different labs leading to difficulties in result comparisons. The brain is a complex and hierarchical system, whereby its RSN architecture can be characterised from mutiple perspectives at regional or global levels. Previous mouse rs-fMRI studies have focused on long-distance FC, however, given the non-uniform influence of anaesthesia on the brain, mapping functional activations across scales in mice under different anaesthetics remain sparsely explored. Establishing this relationahsip would provide a reliable reference to study mouse brain functions in abnormal states and facilitate comparisons across laboratories. | P a g eIn the first aim of this thesis, I investigated the local connectivity in wide type (WT) mice under six commonly used anaesthetic regimens. I identified that the regional connectivity altered across the brain as a function of the expression density of receptors relative to specific agents. In addition, the depth of anaesthesia influences local synchronization.In the seco...

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Motor Control by Sensory Cortex

Cited by 345 publications

References 31 publications

Cell-type–specific inhibition of the dendritic plateau potential in striatal spiny projection neurons

Cell-type–specific inhibition of the dendritic plateau potential in striatal spiny projection neurons

Touch automatically upregulates motor readiness in humans

Functional network study on the wild type and DISC1 transgenic mice

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