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. 2009 Oct 20;106(42):18034-9.
doi: 10.1073/pnas.0810943106. Epub 2009 Oct 1.

Color-tuned neurons are spatially clustered according to color preference within alert macaque posterior inferior temporal cortex

Affiliations

Color-tuned neurons are spatially clustered according to color preference within alert macaque posterior inferior temporal cortex

Bevil R Conway et al. Proc Natl Acad Sci U S A. .

Abstract

Large islands of extrastriate cortex that are enriched for color-tuned neurons have recently been described in alert macaque using a combination of functional magnetic resonance imaging (fMRI) and single-unit recording. These millimeter-sized islands, dubbed "globs," are scattered throughout the posterior inferior temporal cortex (PIT), a swath of brain anterior to area V3, including areas V4, PITd, and posterior TEO. We investigated the micro-organization of neurons within the globs. We used fMRI to identify the globs and then used MRI-guided microelectrodes to test the color properties of single glob cells. We used color stimuli that sample the CIELUV perceptual color space at regular intervals to test the color tuning of single units, and make two observations. First, color-tuned neurons of various color preferences were found within single globs. Second, adjacent glob cells tended to have the same color tuning, demonstrating that glob cells are clustered by color preference and suggesting that they are arranged in color columns. Neurons separated by 50 microm, measured parallel to the cortical sheet, had more similar color tuning than neurons separated by 100 microm, suggesting that the scale of the color columns is <100 microm. These results show that color-tuned neurons in PIT are organized by color preference on a finer scale than the scale of single globs. Moreover, the color preferences of neurons recorded sequentially along a given electrode penetration shifted gradually in many penetrations, suggesting that the color columns are arranged according to a chromotopic map reflecting perceptual color space.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
Color-tuning of 6 glob cells. (A) A pair of green-tuned cells recorded simultaneously from a single electrode penetration. The panels on the left show poststimulus time histograms to an optimally shaped bar of various colors. Responses were determined to white and black (top 2 rows in each histogram) and to 3 sets of 45 colored versions of the bar presented against a neutral gray background. One set of colors was of lower luminance than the background (top section of each histogram), another set was equiluminant with the background (middle section), and a third set was of higher luminance than the background (bottom section). The CIELUV hue angles are given in degrees (see Table S1 and Fig. S2). For ease of presentation, the responses to each color set are compressed into 15 rows, with each row showing the average response to 3 consecutive colors in the cycle. The stimulus onset is at 0 ms. Stimulus duration is indicated by the step at the bottom (histogram bins, 1 ms). The gray scale bar shows the average number of spikes per stimulus repeat per bin. The lack of activity immediately following stimulus onset up to ≈70 ms is the response latency. The panel on the right shows the color tuning determined using a subset of stimuli that sampled the CIELUV color space at uniform color-angle intervals (see Materials and Methods); the peak is normalized to the maximum response. An asterisk indicates the Rayleigh vector. The P value of the Rayleigh vector is .02 for the top cell and .005 for the bottom cell, and the color-tuning index (CI, see Materials and Methods) is 0.93 for the top cell and 0.97 for the bottom cell. (B) A pair of blue-tuned cells recorded simultaneously from a single electrode penetration. The P value of the Rayleigh vector is .004 for the top cell and .04 for the bottom cell, and the CI is 0.96 for both cells. (C) A pair of cells tuned in the red region, recorded from a single electrode penetration, 175 μm apart. The P value of the Rayleigh vector is .03 for the top cell and .06 for the bottom cell, and the CI is 0.93 for the top cell and 0.97 for the bottom cell.
Fig. 2.
Fig. 2.
Sequence regularity of color tuning along an electrode penetration. (A) High-resolution confirmation MRI of electrode with superimposed functional activation (color > black and white). (Scale bar: 1 cm.) The inset shows an enlargement of the boxed region with the cortex outlined. (B) Color tuning of 6 sequentially encountered neurons (see Fig. 1 for axes). (C) Color tuning of all neurons encountered along the electrode path (n = 22 cells; the numbers indicate the cells shown in B). Data points from some cells are overlapping. The gray symbols are outliers, with color preferences that are complementary to red. (D) Latency of the sequentially encountered neurons. Gray symbols indicate outliers in C.
Fig. 3.
Fig. 3.
Preferred color of all neurons for all electrode penetrations. Each panel shows the responses for a single penetration. The different symbols indicate recordings from different globs. The circle, triangle, asterisk, and diamond correspond to globs 3, 2, 4, and 7, respectively, in ref. ; the square corresponds to the glob shown in Supplementary Figure 4 of ref. . Glob 3 is within the region designated PITd, immediately anterior to the V4 boundary defined retinotopically; globs 2, 4, and 7 are within V4.
Fig. 4.
Fig. 4.
Adjacent neurons have similar color preferences. (A) The color preference of neighboring cells is highly correlated (P = 10−54; r2 = 0.58). Axes correspond to the CIELUV polar-angle designation for each color (Table S1 and Fig. S2). The scale bar indicates the number of pairs of cells. Color preference is defined as the CIELUV color stimulus that elicited the maximal response. (B) Color separation between the preferred colors of adjacent neurons. The mean of the distribution is not significantly different from 0 (Student t test).
Fig. 5.
Fig. 5.
Neurons that are closer together are more likely to have similar color tuning than neurons that are further apart. The difference in preferred color between pairs of recorded neurons is plotted against the distance separating the cells measured parallel to the cortical surface. Comparison intervals generated by the MATLAB multcompare function are shown. Neurons along penetrations perpendicular to the cortical surface, and neurons recorded simultaneously, are at 0 mm. The difference in color tuning of a given pair of neurons depends on the separation distance (P < .001, ANOVA). With increasing separation distances, pairs of neurons are significantly more likely to have different color tuning (P < .02). Moreover, all pairs of neurons separated by .25 mm or less have significantly lower color-tuning differences than predicted by chance (random).

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