Spatiotemporal Properties of Neuron Response Suppression in Owl Monkey Primary Somatosensory Cortex When Stimuli Are Presented to Both Hands

Abstract

Despite the lack of ipsilateral receptive fields (RFs) for neurons in the hand representation of area 3b of primary somatosensory cortex, interhemispheric interactions have been reported to varying degrees. We investigated spatiotemporal properties of these interactions to determine the following: response types, timing between stimuli to evoke the strongest bimanual interactions, topographical distribution of effects, and their dependence on similarity of stimulus locations on the two hands. We analyzed response magnitudes and latencies of single neurons and multineuron clusters recorded from 100-electrode arrays implanted in one hemisphere of each of two anesthetized owl monkeys. Skin indentations were delivered to the two hands simultaneously and asynchronously at mirror locations (matched sites on each hand) and nonmirror locations. Since multiple neurons were recorded simultaneously, stimuli on the contralateral hand could be within or outside of the classical RFs of any given neuron. For most neurons, stimulation on the ipsilateral hand suppressed responses to stimuli on the contralateral hand. Maximum suppression occurred when the ipsilateral stimulus was presented 100 ms before the contralateral stimulus onset ( p Ͻ 0.0005). The longest stimulus onset delay tested (500 ms) allowed contralateral responses to recover to control levels ( p ϭ 0.428). Stimulation on mirror digits did not differ from stimulation on nonmirror locations ( p ϭ 1.000). These results indicate that interhemispheric interactions are common in area 3b, somewhat topographically diffuse, and maximal when the suppressing ipsilateral stimulus precedes the contralateral stimulus. Our findings point to a neurophysiological basis for "interference" effects found in human psychophysical studies of bimanual stimulation.

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

“…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.…”

“…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.…”

“…We examined cortical neurons in area 3b of primates to explore the nature of information processing in primary somatosensory cortex with emphasis on how stimuli outside of the excitatory RF modulate neuronal activity. Previously, we have reported (Reed et al 2010a(Reed et al , b, 2011) that area 3b neurons are modulated by stimuli presented outside of the minimal RFs (mRFs), such that stimulation on two different digit or palm sites can facilitate or suppress firing relative to single-site stimulation within the mRF. With the use of chronic microelectrode array recordings, here, we report suppression of baseline firing in response to single-site skin indentations and describe properties of responses related to types of suppression encountered in three different primate species.…”

Spatiotemporal Dynamics of Bimanual Integration in Human Somatosensory Cortex and Their Relevance to Bimanual Object Manipulation

“…Recent reports also showed suppressive interhemispheric interactions in area 3b of monkey SI during simultaneous tactile stimulation of both hands (Tommerdahl et al, 2006;Reed et al, 2011). Because of the lack of direct callosal connections between hand representations of area 3b in primates, it was suggested that the interhemispheric effects in area 3b involve indirect intrahemispheric feedback projections from other areas, such as area 2 of SI, SII, or PPC.…”

Testing Tactile Masking between the Forearms

“…This technique provides behavioural 5,7,8,[13][14][15] evidence to support neurophysiological [16][17][18] and neuroimaging data [19][20][21][22][23] that suggest that the integration of somatosensory inputs from the two sides of the body occurs in a somatotopic representation. In these experiments, the effect of arm location was briefly examined by comparing masking when the hands were touching or parallel.…”