Modality maps within primate somatosensory cortex

Abstract

The sensations of pressure, flutter, and vibration are psychophysically distinct tactile modalities produced by frequency-specific vibrotactile stimulation of different mechanoreceptors in the skin. The information coded by the different low-threshold mechanoreceptors are carried by anatomically and electrophysiologically distinct pathways that remain separate at least up to and including the input stage of primary somatosensory cortex (SI) in primates, area 3b. Little is known about the functional organization of tactile representation beyond that stage. By using intrinsic optical imaging methods to record from area 1, the second processing stage of SI, we present evidence that pressure, flutter, and vibratory stimuli activate spatially distinct cortical domains in area 1, further strengthening the foundation for modality-specific processing streams in SI. These modality domains exhibit an organization that is unlike the discontinuous modality maps in visual area V2 but more like the continuous visual orientation maps in V1. The results demonstrate that psychophysically distinct sensory modalities can have fundamentally different modes of cortical representation.

Fig. 2.

Area 1 vector maps. Shown above A is the color-coded vector space. (A-C) Digits D2 (A), D4 (B), and D4 (C) were stimulated. (Left) Composite vector maps. Red, green, and blue indicate strong preference for pressure, flutter, and vibration, respectively. (Center) Vector maps with color threshold outlines overlain. (Right) Colored outlines of thresholded color maps. Outlines were obtained by selecting pixels that exceeded an 80% magnitude threshold and fell within ±15° of cardinal SA, RA, or PC vectors. (Scale bar, 1 mm.) Anterior to top, medial to right. (D) Histograms indicate the distributions of the outlined domain diameters. (Left) All domains (n = 108). (Right) Domains separated by case. (E) Domain size distribution in area 3b (cf. 19). (F) Vector map (area indicated by rectangular box in C Right) thresholded to six colors. (Inset) Possible pinwheel centers. Note clockwise and counterclockwise SA (red), RA (green), and PC (blue) rotations.

Fig. 1.

Vibrotactile stimulation of D4 evokes modality-specific activation in area 1. (A) Temporal development and consistency of the intrinsic cortical response to pressure, flutter, and vibratory stimuli. Dark pixels indicate activation. For each stimulus, six images spanning 3 sec are shown (stimulus onset at frame 0.2 sec). (Scale bar, 1 mm.) A, anterior; M, medial. Data are the sum of 40 trials. (B) Single-condition blank-subtracted maps show modality-specific activation patterns. (a-c) Same as last images shown in A (3 sec). (d and i) Subtraction maps of flutter-pressure (RA-SA) illustrate irregular alternating dark (preference for flutter) and light (preference for pressure) domains (gray pixels indicate equal preference for both). (e) Blank condition map. (f-i) Activation outlines of a-d obtained by low-pass filtering and thresholding. The red diamond, green square, and blue triangle indicate sampled locations in k-m.(j) Blood vessel map with pressure, flutter, and vibration activation outlines superimposed. Sample electrode penetrations are indicated by labeled dots. The black box indicates the region shown in Fig. 3C. (k-m) Time courses of signal reflectance change illustrate modality-specific preference: pressure-dominant locus (red diamonds), flutter-dominant locus (green squares), and vibration-dominant locus (blue triangles). (n) Location of fingerpad representation in area 1 in the squirrel monkey (adapted from ref. 45). Small red box indicates area of imaging. Data are the sum of 40 trials. (Scale bar, 1 mm.)

Fig. 3.

D2 activation in areas 3b and 1. Green boxes indicate centers of D2 activations in area 3b (upper) and area 1 (lower). (A) Vessel map with recorded digit locations. (B) Raw image of D2 indentation. (C) Modality vector map (red, green, and blue indicate responses for SA, RA, and PC, respectively) shows strongest activation modules in centers of D2 activation but also weaker activation outside D2 center zones. (Scale bar, 1 mm.)

Fig. 4.

Model of SA, RA, and PC preference domains in area 1. Not unlike thalamocortical arbors from the lateral geniculate nucleus, single thalamocortical or corticocortical inputs in layer 4 of area 1 have multiple arbors, each spanning 200-300 μm in width. Some arbors of each SA, RA, and PC input overlap at a “hot spot.” Other arbors extend to nontopographic locations away from the hot spot and locally establish some degree of modality-specific dominance. A continuous modality map results in layers 2/3 (upward lines) by varying arbor overlap: little overlap (centers of red, green, and blue domains), some overlap (e.g., magenta or yellow-green domains, not depicted), and high overlap (black or white domains, not depicted).