Multimodal Interactions between Proprioceptive and Cutaneous Signals in Primary Somatosensory Cortex

Kim, Sung Soo; Gomez‐Ramirez, Manuel; Thakur, Pramodsingh H.; Hsiao, Steven S.

doi:10.1016/j.neuron.2015.03.020

Cited by 101 publications

(110 citation statements)

References 63 publications

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“…However, mounting evidence suggests that signals from distinct somatosensory submodalities are in fact combined in the CNS, and that most tactile percepts rely on multiple submodalities (Saal and Bensmaia, 2014). For example, a recent study found that all areas of somatosensory cortex receive input from both touch and proprioceptive neurons (Kim et al, 2015). …”

Section: Discussionmentioning

confidence: 99%

Parallel Transformation of Tactile Signals in Central Circuits of Drosophila

Tuthill

Wilson

2016

Cell

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SUMMARY To distinguish between complex somatosensory stimuli, central circuits must combine signals from multiple peripheral mechanoreceptor types, as well as mechanoreceptors at different sites in the body. Here, we investigate the first stages of somatosensory integration in Drosophila using in vivo recordings from genetically labeled central neurons, in combination with mechanical and optogenetic stimulation of specific mechanoreceptor types. We identify three classes of central neurons that process touch: one compares touch signals on different parts of the same limb, one compares touch signals on right and left limbs, and the third compares touch and proprioceptive signals. Each class encodes distinct features of somatosensory stimuli. The axon of an individual touch receptor neuron can diverge to synapse onto all three classes, meaning that these computations occur in parallel, not hierarchically. Representing a stimulus as a set of parallel comparisons is a fast and efficient way to deliver somatosensory signals to motor circuits.

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Section: Discussionmentioning

confidence: 99%

Parallel Transformation of Tactile Signals in Central Circuits of Drosophila

Tuthill

Wilson

2016

Cell

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“…Consistent with this idea, this analysis revealed significant activation in the frontal eye field contralateral to the pathological direction, and, in the opposite hemisphere, the ipsilateral postcentral sulcus, and supramarginal gyrus (Figure 4). Although proprioceptive information is processed in all subfields of primary somatosensory cortex, Brodmann’s area 3a (in the depth of the central sulcus) seems to be most important, followed by Brodmann’s area 1 and 2 (the latter located in the postcentral sulcus) (49). The middle cingulate gyrus is activated primarily in relation to movement execution, while the regions surrounding the frontal eye fields are premotor areas involved in motor planning (46).…”

Section: Discussionmentioning

confidence: 99%

A Functional Magnetic Resonance Imaging Study of Head Movements in Cervical Dystonia

et al. 2016

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Cervical dystonia (CD) is a neurological disorder characterized by abnormal movements and postures of the head. The brain regions responsible for these abnormal movements are not well understood, because most imaging techniques for assessing regional brain activity cannot be used when the head is moving. Recently, we mapped brain activation in healthy individuals using functional magnetic resonance imaging during isometric head rotation, when muscle contractions occur without actual head movements. In the current study, we used the same methods to explore the neural substrates for head movements in subjects with CD who had predominantly rotational abnormalities (torticollis). Isometric wrist extension was examined for comparison. Electromyography of neck and hand muscles ensured compliance with tasks during scanning, and any head motion was measured and corrected. Data were analyzed in three steps. First, we conducted within-group analyses to examine task-related activation patterns separately in subjects with CD and in healthy controls. Next, we directly compared task-related activation patterns between participants with CD and controls. Finally, considering that the abnormal head movements in CD occur in a consistently patterned direction for each individual, we conducted exploratory analyses that involved normalizing data according to the direction of rotational CD. The between-group comparisons failed to reveal any significant differences, but the normalization procedure in subjects with CD revealed that isometric head rotation in the direction of dystonic head rotation was associated with more activation in the ipsilateral anterior cerebellum, whereas isometric head rotation in the opposite direction was associated with more activity in sensorimotor cortex. These findings suggest that the cerebellum contributes to abnormal head rotation in CD, whereas regions in the cerebral cortex are involved in opposing the involuntary movements.

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“…Examinations of widespread and multidigit interactions in area 3b have added to our understanding of early stages of somatosensory processing to incorporate neurons with larger response fields that show reductions as well as increases in firing rate when discrete regions of skin are touched (DiCarlo et al 1998;Fitzgerald et al 2006b;Friedman et al 2008;Kim et al 2015;Reed et al 2008Reed et al , 2011Thakur et al 2006Thakur et al , 2012. Still, little information is available about the inhibitory components of the receptive field (RF) of neurons related to the hand and arm in primary somatosensory cortex in primates.…”

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confidence: 99%

Chronic recordings reveal tactile stimuli can suppress spontaneous activity of neurons in somatosensory cortex of awake and anesthetized primates

Reed

Franca

et al. 2016

Journal of Neurophysiology

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Qi HX, Reed JL, Franca JG, Jain N, Kajikawa Y, Kaas JH. Chronic recordings reveal tactile stimuli can suppress spontaneous activity of neurons in somatosensory cortex of awake and anesthetized primates. J Neurophysiol 115: 2105-000, 2016. First published February 24, 2016 doi:10.1152/jn.00634.2015.-In somatosensory cortex, tactile stimulation within the neuronal receptive field (RF) typically evokes a transient excitatory response with or without postexcitatory inhibition. Here, we describe neuronal responses in which stimulation on the hand is followed by suppression of the ongoing discharge. With the use of 16-channel microelectrode arrays implanted in the hand representation of primary somatosensory cortex of New World monkeys and prosimian galagos, we recorded neuronal responses from single units and neuron clusters. In 66% of our sample, neuron activity tended to display suppression of firing when regions of skin outside of the excitatory RF were stimulated. In a small proportion of neurons, single-site indentations suppressed firing without initial increases in response to any of the tested sites on the hand. Latencies of suppressive responses to skin indentation (usually 12-34 ms) were similar to excitatory response latencies. The duration of inhibition varied across neurons. Although most observations were from anesthetized animals, we also found similar neuron response properties in one awake galago. Notably, suppression of ongoing neuronal activity did not require conditioning stimuli or multi-site stimulation. The suppressive effects were generally seen following single-site skin indentations outside of the neuron's minimal RF and typically on different digits and palm pads, which have not often been studied in this context. Overall, the characteristics of widespread suppressive or inhibitory response properties with and without initial facilitative or excitatory responses add to the growing evidence that neurons in primary somatosensory cortex provide essential processing for integrating sensory stimulation from across the hand. inhibitory period; latency; area 3b; area 3a; monkeys AMONG THEIR COMMON TRAITS, primates, to varying degrees, rely on remarkable sensory and motor functions of the hand and arm. The cortical representations of the hand and associated neuron properties have long been studied to understand normal and impaired processing of somatosensory stimuli, with emphasis on developing strategies to promote recovery when processing is impaired. Examinations of widespread and multidigit interactions in area 3b have added to our understanding of early stages of somatosensory processing to incorporate neurons with larger response fields that show reductions as well as increases in firing rate when discrete regions of skin are touched (DiCarlo et al. 1998;

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Multimodal Interactions between Proprioceptive and Cutaneous Signals in Primary Somatosensory Cortex

Cited by 101 publications

References 63 publications

Parallel Transformation of Tactile Signals in Central Circuits of Drosophila

Parallel Transformation of Tactile Signals in Central Circuits of Drosophila

A Functional Magnetic Resonance Imaging Study of Head Movements in Cervical Dystonia

Chronic recordings reveal tactile stimuli can suppress spontaneous activity of neurons in somatosensory cortex of awake and anesthetized primates

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