Structure of the Excitatory Receptive Fields of Infragranular Forelimb Neurons in the Rat Primary Somatosensory Cortex Responding To Touch

Abstract

We quantitatively studied the excitatory receptive fields of 297 neurons recorded from the forelimb infragranular somatosensory cortex of the rat while touch stimuli were applied to discrete locations on the forelimbs. Receptive fields were highly heterogeneous, but they were regulated, on average, by an underlying spatio-temporal structure. We found the following. (i) Neurons responded with decreasing magnitude and increasing latency when the stimulus was moved from the primary location to secondary locations and to far ispilateral locations of their excitatory receptive fields, displaying smooth transitions from the primary location to secondary locations. (ii) Receptive field patterns revealed functional connectivity between the digits and ventral palm, which did not depend on whether the digits were stimulated dorsally or ventrally. (iii) The structure of the receptive fields (i.e. the neural responses to stimulation of secondary locations compared to the neural responses to stimulation of the primary location), reflected cortical (rather than body) distances. (iv) There was a functional separation between the forepaw and the rest of the forelimb. Namely: if the primary location was in the digits or palm, secondary locations were biased toward the digits and palm; if the primary location was in rest of the forelimb, secondary locations appeared equally distributed over forelimb, digits and palm. (v) More than 40% of neurons extended their receptive field to the ipsilateral forelimb, without any evident spatial organization. Overall, the stimuli evoked approximately 3 times more spikes from secondary responses than from primary responses. These results suggest that a rich repertoire of spatio-temporal responses is available for encoding tactile information. This highly distributed receptive field structure provides the electrophysiological architecture for studying organization and plasticity of cortical somatosensory processing.

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

“…Yet, we also found evidence consistent with cortical sources of inhibition (Davis et al 2003;Fitzpatrick et al 1999;Hubel and Wiesel 1965;Nelken and Young 1994;Shofner and Young 1985;Spirou and Young 1991;Walker et al 1999;Webb et al 2005;Wehr and Zador 2003). Thus our findings indirectly support recent views that suppressive response components arise from a combination of cortical and subcortical sources rather than from the traditional model of suppression from cortical sources only [e.g., Sachdev et al (2012) review].…”

“…Yet, similar to results for excitatory RFs, we revealed effects of single-site stimulation that occurred far from each neuron's excitatory mRF across distant digits or palm pads. As reported by Tutunculer et al (2006), we also found evidence to suggest that the response types to tactile stimuli were more closely related to cortical separations within the hand representation than to separations between contiguous surfaces of the physical hand. Furthermore, neuronal activity recorded from a selected cortical electrode in response to stimulation of sites across the hand suggested that lateral interactions involving firing suppression occur not only along the representation of a single digit (in the rostral-caudal dimension in cortex) but also between digits (across the medial-lateral dimension in cortex).…”

“…The extent of suppressive response components when single sites were stimulated across hand locations adds properties of firing suppression to the overall picture of RF structure and supports findings related to widespread excitatory response fields reported in the somatosensory cortex of primates (Friedman et al 2008;Lipton et al 2010;Reed et al 2008Reed et al , 2010aReed et al , b, 2011Reed et al , 2012Thakur et al 2012;Tutunculer et al 2006) and rodents (Tutunculer et al 2006). We believe that our findings reported here contribute to a better understanding of how primates process sensory stimuli on the hand for object perception and manipulation, which is fundamental for developing strategies to improve sensorimotor functions of the hand after impairments in patients with deficits due to nerve or spinal cord injury and disorders.…”

Spike Timing, Spike Count, and Temporal Information for the Discrimination of Tactile Stimuli in the Rat Ventrobasal Complex

“…Although our experimental anesthetized conditions represent a good model of passive unexpected stimuli during quiet behaviors (Krupa et al, 2004;Ferezou et al, 2006), it is important to remark that inferences about how stimuli are processed by behaving animals based on anesthetized data should be cautious. Nevertheless, the loss of spatial selectivity resulting from the large receptive fields-not only in the thalamus but also in the cortex (Ghazanfar and Nicolelis, 1999;Tutunculer et al, 2006;Moxon et al, 2008)-could be the price paid by sensory systems to fully benefit from the high information capacity of spike timing codes .…”

Biomimetic Brain Machine Interfaces for the Control of Movement

“…Recent studies in the Moxon laboratory examined how sensorimotor information is encoded in normal animals and how this encoding is affected by spinal cord injury. Before hemisection, cells within a single cortical column encode passive sensory information using large, heterogeneous receptive fields covering the digits and palm (Tutunculer et al, 2006), and the timing between spikes contributes to a distributed spatiotemporal code . In the awake animal, recorded neuronal activity can be used to encode the placement of footfalls on a treadmill with a sensitivity of Ͼ90%.…”