Effects of spatiotemporal stimulus properties on spike timing correlations in owl monkey primary somatosensory cortex.

The correlated discharges of cortical neurons in primary somatosensory cortex are a potential source of information about somatosensory stimuli. One aspect of neuronal correlations that has not been well studied is how the spatiotemporal properties of tactile stimuli affect the presence and magnitude of correlations. We presented single- and dual-point stimuli with varying spatiotemporal relationships to the hands of three anesthetized owl monkeys and recorded neuronal activity from 100-electrode arrays implanted in primary somatosensory cortex. Correlation magnitudes derived from joint peristimulus time histogram (JPSTH) analysis of single neuron pairs were used to determine the level of spike timing correlations under selected spatiotemporal stimulus conditions. Correlated activities between neuron pairs were commonly observed, and the proportions of correlated pairs tended to decrease with distance between the recorded neurons. Distance between stimulus sites also affected correlations. When stimuli were presented simultaneously at two sites, ∼37% of the recorded neuron pairs showed significant correlations when adjacent phalanges were stimulated, and ∼21% of the pairs were significantly correlated when nonadjacent digits were stimulated. Spatial proximity of paired stimuli also increased the average correlation magnitude. Stimulus onset asynchronies in the paired stimuli had small effects on the correlation magnitude. These results show that correlated discharges between neurons at the first level of cortical processing provide information about the relative locations of two stimuli on the hand.

Widespread spatial integration in primary somatosensory cortex.

Tactile discrimination depends on integration of information from the discrete receptive fields (RFs) of peripheral sensory afferents. Because this information is processed over a hierarchy of subcortical nuclei and cortical areas, the integration likely occurs at multiple levels. The current study presents results indicating that neurons across most of the extent of the hand representation in monkey primary somatosensory cortex (area 3b) interact, even when these neurons have separate RFs. We obtained simultaneous recordings by using a 100-electrode array implanted in the hand representation of primary somatosensory cortex of two anesthetized owl monkeys. During a series of 0.5-s skin indentations with single or dual probes, the distance between electrodes from which neurons with synchronized spike times were recorded exceeded 2 mm. The results provide evidence that stimuli on different parts of the hand influence the degree of synchronous firing among a large population of neurons. Because spike synchrony potentiates the activation of commonly targeted neurons, synchronous neural activity in primary somatosensory cortex can contribute to discrimination of complex tactile stimuli.

Response properties of neurons in primary somatosensory cortex of owl monkeys reflect widespread spatiotemporal integration.

Receptive fields of neurons in somatosensory area 3b of monkeys are typically described as restricted to part of a single digit or palm pad. However, such neurons are likely involved in integrating stimulus information from across the hand. To evaluate this possibility, we recorded from area 3b neurons in anesthetized owl monkeys with 100-electrode arrays, stimulating two hand locations with electromechanical probes simultaneously or asynchronously. Response magnitudes and latencies of single- and multiunits varied with stimulus conditions, and multiunit responses were similar to single-unit responses. The mean peak firing rate for single neurons stimulated within the preferred location was estimated to be ∼26 spike/s. Simultaneous stimulation with a second probe outside the preferred location slightly decreased peak firing rates to ∼22 spike/s. When the nonpreferred stimulus preceded the preferred stimulus by 10-500 ms, peak firing rates were suppressed with greatest suppression when the nonpreferred stimulus preceded by 30 ms (∼7 spike/s). The mean latency for single neurons stimulated within the preferred location was ∼23 ms, and latency was little affected by simultaneous paired stimulation. However, when the nonpreferred stimulus preceded the preferred stimulus by 10 ms, latencies shortened to ∼16 ms. Response suppression occurred even when stimuli were separated by long distances (nonadjacent digits) or long times (500 ms onset asynchrony). Facilitation, though rare, occurred most often when the stimulus onsets were within 0-30 ms of each other. These findings quantify spatiotemporal interactions and support the hypothesis that area 3b is involved in widespread stimulus integration.

Deconstruction of spatial integrity in visual stimulus detected by modulation of synchronized activity in cat visual cortex.

Spatiotemporal relationships among contour segments can influence synchronization of neural responses in the primary visual cortex. We performed a systematic study to dissociate the impact of spatial and temporal factors in the signaling of contour integration via synchrony. In addition, we characterized the temporal evolution of this process to clarify potential underlying mechanisms. With a 10 x 10 microelectrode array, we recorded the simultaneous activity of multiple cells in the cat primary visual cortex while stimulating with drifting sine-wave gratings. We preserved temporal integrity and systematically degraded spatial integrity of the sine-wave gratings by adding spatial noise. Neural synchronization was analyzed in the time and frequency domains by conducting cross-correlation and coherence analyses. The general association between neural spike trains depends strongly on spatial integrity, with coherence in the gamma band (35-70 Hz) showing greater sensitivity to the change of spatial structure than other frequency bands. Analysis of the temporal dynamics of synchronization in both time and frequency domains suggests that spike timing synchronization is triggered nearly instantaneously by coherent structure in the stimuli, whereas frequency-specific oscillatory components develop more slowly, presumably through network interactions. Our results suggest that, whereas temporal integrity is required for the generation of synchrony, spatial integrity is critical in triggering subsequent gamma band synchronization.

Synchronous activity in cat visual cortex encodes collinear and cocircular contours.

We explored how contour information in primary visual cortex might be embedded in the simultaneous activity of multiple cells recorded with a 100-electrode array. Synchronous activity in cat visual cortex was more selective and predictable in discriminating between drifting grating and concentric ring stimuli than changes in firing rate. Synchrony was found even between cells with wholly different orientation preferences when their receptive fields were circularly aligned, and membership in synchronous groups was orientation and curvature dependent. The existence of synchrony between cocircular cells reinforces its role as a general mechanism for contour integration and shape detection as predicted by association field concepts. Our data suggest that cortical synchrony results from common and synchronous input from earlier visual areas and that it could serve to shape extrastriate response selectivity.