Simultaneous Top-down Modulation of the Primary Somatosensory Cortex and Thalamic Nuclei during Active Tactile Discrimination

Departments of Neurobiology, Biomedical Engineering, and Psychology and Neuroscience and Center for Neuroengineering, Duke University, Durham, North Carolina 27710, Neuroscience Program, Wellesley College, Wellesley, Massachusetts 02481, and Edmond and Lily Safra International Institute for Neuroscience of Natal, 59066-060 Natal, Brazil.
The Journal of Neuroscience : The Official Journal of the Society for Neuroscience (Impact Factor: 6.34). 02/2013; 33(9):4076-93. DOI: 10.1523/JNEUROSCI.1659-12.2013
Source: PubMed


The rat somatosensory system contains multiple thalamocortical loops (TCLs) that altogether process, in fundamentally different ways, tactile stimuli delivered passively or actively sampled. To elucidate potential top-down mechanisms that govern TCL processing in awake, behaving animals, we simultaneously recorded neuronal ensemble activity across multiple cortical and thalamic areas while rats performed an active aperture discrimination task. Single neurons located in the primary somatosensory cortex (S1), the ventroposterior medial, and the posterior medial thalamic nuclei of the trigeminal somatosensory pathways exhibited prominent anticipatory firing modulations before the whiskers touching the aperture edges. This cortical and thalamic anticipatory firing could not be explained by whisker movements or whisker stimulation, because neither trigeminal ganglion sensory-evoked responses nor EMG activity were detected during the same period. Both thalamic and S1 anticipatory activity were predictive of the animal's discrimination accuracy. Inactivation of the primary motor cortex (M1) with muscimol affected anticipatory patterns in S1 and the thalamus, and impaired the ability to predict the animal's performance accuracy based on thalamocortical anticipatory activity. These findings suggest that neural processing in TCLs is launched in anticipation of whisker contact with objects, depends on top-down effects generated in part by M1 activity, and cannot be explained by the classical feedforward model of the rat trigeminal system.

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    • "As used here, the term ''emulation'' describes a single entity made up of the linked representations of a potential action and its expected sensory result. Empirical support for the link between potential actions and predicted outcome comes from a recent study that found anticipatory activity from single cell discharges in rat thalamus, and primary sensory and motor cortex, when rats explored the size of an aperture (Pais-Vieira et al., 2013). This anticipatory activity was disrupted when motor cortex was de-activated with muscimol, indicating that motor cortical activity was important for maintaining predictive representations in thalamus and sensory cortex. "
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    • "The changes in the wavelets coefficient start increasing after a delay of approx. 1 s, to reach a stationary state in a few more seconds. shorter intervals were observed following active sensory shifts (Pais-Vieira et al., 2013), in line with the conclusions by Winter et al. (2008) based on a stimulus timing-matching paradigm, who found no advantage on the perceived timing of an active over a passive touch. Latencies of EMG and postural changes were the shortest on removal of haptic information. "
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    • "(D–F) same as (A–C) but during photosuppression of layer VI, and using a cell from layer IV as example; scale bar in (D) 50 spikes/s; population tuning curve in (F) is the average of n = 52 units. (Reprinted from Olsen et al., 2012 "
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