Widespread spatial integration in primary somatosensory cortex - PubMed (original) (raw)

Widespread spatial integration in primary somatosensory cortex

Jamie L Reed et al. Proc Natl Acad Sci U S A. 2008.

Abstract

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.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.

Fig. 1.

An example of correlated spike activity recorded from two adjacent electrodes in monkey 1. (A) A lateral schematic view of an owl monkey brain with area 3b shaded. Subdivisions representing the face and hand are outlined, including those that cannot be seen from a surface view. LS, lateral sulcus; STS, superior temporal sulcus. (B) The location of the array within the area 3b hand representation. The approximate representations of the digits (D1–5) and the digital (P1–3), thenar (PTh), hypothenar (PH) and insular (Pi) pads of the hand are identified and outlined. The red dots mark the electrodes where the two neurons were recorded for the analysis shown in C. Both neurons had RFs on the PTh pad. (C) An example of the spike timing synchrony of units recorded from adjacent electrodes. Two probes simultaneously indented the skin on the PTh and P1 pads. Spike synchrony between the two neurons is shown in the normalized joint peristimulus time histogram, the JPSTH matrix. The two PSTHs of the responses to 100 repetitions of 0.5-s skin indentations are shown to the left and below the matrix, with the cross-correlation histogram derived from the JPSTH analysis directly below. The colored pixels in the JPSTH matrix represent the magnitude of the normalized correlation at different lag times over a poststimulus time of 700 ms. Strong spike synchrony occurred around a 0-ms lag time throughout the period. The cross-correlation histogram (black) revealed a peak correlation of 0.16 that exceeded the mean correlation from the shuffled trials (red).

Fig. 2.

Fig. 2.

An example of widespread spike timing correlations and firing activity. Significant peak correlations across the sampled neuron-units in the 100-electrode array are displayed in a grid. A color map representing the peak firing rates of the units is overlaid on a schematic of the area 3b hand representation to indicate the approximate spatial locations of the electrodes. Shown is one example from monkey 1 when a single site on the thenar (PTh) palm was stimulated repeatedly (100 trials). Dots indicate electrode sites and significant correlations between units are represented by the lines connecting the dots. The size of the dots and the thickness of the connecting lines are visual representations of the peak magnitude of the correlation. Each colored box represents the peak firing rate of a unit at one electrode site. Peak firing rates are shown for those units included in the synchrony analysis. Dark blue squares indicate electrodes not analyzed for spike synchrony because units did not show sustained responses to stimulation.

Fig. 3.

Fig. 3.

Relationship of spike timing peak correlation magnitude to the distance between electrodes. The normalized, significant peak correlation magnitudes are plotted as a function of distance between the correlated unit pairs for monkeys 1 and 2 when nonadjacent sites were simultaneously stimulated (Dual-Site) or when single sites were stimulated as controls (Single-Site).

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