Research ArticleNEUROSCIENCE

A distinct population of heterogeneously color-tuned neurons in macaque visual cortex

See allHide authors and affiliations

Science Advances  19 Feb 2021:
Vol. 7, no. 8, eabc5837
DOI: 10.1126/sciadv.abc5837
  • Fig. 1 Subfield stimulation of V4 neurons with equiluminant color stimuli.

    (A) Natural image with chromatically uniform and nonuniform regions at two different spatial locations. Image taken from McGill Calibrated Colour Image Database (76) (photographer: unknown, McGill University). (B) Schematic of chronically implanted Utah array in area V4. (C) Equiluminant color stimulus set plotted in u,v space. (D) Angular plot of same color stimulus with respect to the u,v coordinates of an equiluminant neutral gray background. (E) Schematic description of full–receptive field (RF) stimulation using a “reverse correlation” movie consisting of 16 equiluminant colors. (F) Schematic description of sub-RF stimulation using the same reverse correlation approach targeting small (~1°) subfields.

  • Fig. 2 Heterogeneous color tuning properties in V4.

    (A) Example V4 RFs generated using RF mapping stimuli (see Materials and Methods), cells 1 and 3 (monkey T), and cell 2 (monkey M). Coordinates (0,0) represent the fixation point. (B) Tuning curves for the same neurons when the entire RF is stimulated with equiluminant color stimuli. Color selectivity index (CSI) are 0.5 (cell 1), 0.24 (cell 2), and 0.30 (cell 3), respectively. (C) Zoomed in version of the heatmap in (A) (cell 1) showing the finer 5 × 5 grid for allocating subfields. (D) Tuning curves at each of the 25 locations in (C) reconstructed using reverse correlation analysis. CSImean = 0.60 ± 0.01. (E) Overlay of all subfield tuning curves (red) on the full-field tuning curve (black) for the homogeneous RF shown in (C). (F) Same as in (C) except in the case of a neuron (cell 4; monkey M) with heterogeneously tuned RF. (G) Tuning of each subfield at different spatial locations within the RF shown in (F). CSImean = 0.31 ± 0.02. (H) Same as in (E) except for the heterogeneous RF shown in (F). Note no significant tuning in responses (P > 0.05; Rayleigh’s test, CSI = 0.11) obtained with full-field stimulation of the heterogeneous RF. Error bars represent SEM.

  • Fig. 3 Tuning for multiple colors within the RF of heterogeneous neurons.

    (A) Distribution of heterogeneity index (HI) of 270 V4 neurons pooled from both monkeys (N = 159, monkey T; N = 111 monkey M). Red solid line represents a bimodal Gaussian fit (R2adj = 0.72) generated using the curve fitting toolbox in MATLAB. Distribution of HI for each animal is shown in fig. S3. Black arrow points to the median HI value. (B) Representative examples of subfield color tuning for four neurons (cells 1 and 3, monkey T; cells 2 and 4, monkey M) with a diverse range of HI values. Gray-colored subfields did not show significant tuning to any of the colors in the stimulus set. (C) Number of unique preferred colors that subfields of a neuron are tuned to as a function of the HI of the neuron. Each gray circle represents a single neuron. Black filled circles represent mean values within bins of size HI = 20. Solid black line represents interpolated fit for visualization purposes. (D) CSI of neurons (N = 63) recorded in a subset of sessions with significant tuning for full-RF color stimulation as a function of their HI. Note that full-RF stimulation and sub-RF stimulation were performed on the same day but in different sessions, and only neurons with both full-RF and subfield tuning were included in the analysis. Black solid line represents linear fit to the data showing significant negative correlation (Pearson’s correlation, r = −0.31, P < 0.001).

  • Fig. 4 Differential temporal dynamics of color tuning in homogeneous and heterogeneous neurons.

    (A) Schematic representation of two possible mechanisms that could account for heterogeneously tuned RFs: feedforward inputs with weak recurrent processing (left) and feedforward coupled with strong recurrent processing (right). Dashed and solid lines represent weak and strong recurrent connections. (B) Color stimulus movie flashed at 60 Hz targeting a randomly chosen subfield in a given trial. (C) Responses of two example neurons (cell 1, monkey T; cell 2, monkey M) across multiple trials to the movie consisting of a pseudorandom sequence of all 16 colors constructed from the hue wheel C(θ) as described previously. Tuning curves are constructed at multiple delays τ to examine dynamics of color tuning. Black bar represents the duration of the presentation of the color movie (1.6 s). (D) Heatmap representation of the tuning curve of an example subfield of a homogeneous cell (monkey T, HI = 16) as a function of temporal delay (y axis). (E) Same as in (D) except for a neuron (monkey M, HI = 62.5) with heterogeneously tuned RF. Note the difference in latency at which peak firing rate is attained for the example neurons. The subfield PC for each example neuron is shown to the left. (F) Mean peak tuning latency averaged over subfields as a function of the HI of neurons (N = 270). Filled color circles correspond to example neurons in (D) and (E), with blue and red representing the homogeneous and heterogeneous cells, respectively. Solid line represents linear fit to the data showing a significant positive correlation (Pearson’s correlation coefficient, r = 0.43, P < 0.001).

  • Fig. 5 Stimulus-specific adaptation differentially alters color tuning in heterogeneous and homogeneous neurons.

    (A) Schematic description of adaptation and control trials to examine the changes in tuning for each subfield. (B) Schematic depiction of Δθ (change in PC) and Δϕ (angular difference between the preadaptation PC and that of the adapter) on the color circle defined in Fig. 1D. Red line, angular position of adapter; yellow line, preadaptation PC; and green line, post adaptation PC. (C) Three representative examples of subfields showing repulsive (Δθ = 48°, monkey M), attractive (Δθ = −18°, monkey T), and almost negligible shifts (Δθ = 3°, monkey M) after adaptation for different Δϕ values. Black arrow shows the position of the adapting color in terms of color angle. (D) Mean change in PC (Δθ) of individual subfields post adaptation as a function of the distance between the adapting color and subfield’s PC before adaptation (Δϕ). Filled red circles represent mean of the binned values of (Δθ) for bin widths of Δϕ = 22.5°. Asterisks denote statistically significant difference (two-tailed Wilcoxon signed-rank test, P < 0.01) from a distribution with zero median. (E) Change in HI post adaptation as a function of HI prior to adaptation. Filled red circles represent mean of binned values for bin widths of Δϕ = 22.5°. Asterisks denote statistically significant difference from 0 (two-tailed Wilcoxon signed-rank test, P < 0.01). Error bars in (C) to (E) represent SEM.

  • Fig. 6 Functional role of homogeneous and heterogeneous RFs.

    (A) Schematic description of functional significance of homogeneously and heterogeneously tuned neurons. (B) Example spike raster of a homogenously tuned neuron for spatially uniform (blue) and nonuniform color stimuli (red). (C) Baseline-corrected PSTHs of the example neuron on the left stimulated at its PC (inset) using a full-RF uniform stimulus (blue trace, inset; Rayleigh test, P < 0.01) and for a nonuniform stimulus (red trace). Shaded region represents stimulus duration. (D) Example spike raster of a heterogeneous neuron across trials for uniform/nonuniform stimuli. (E) Red/blue traces represent the PSTH of responses to a nonuniform/uniform stimulus; no significant tuning (Rayleigh test, P > 0.05) when full-RF is stimulated with uniform color patches (inset). Solid lines and shaded regions (blue and red): means and SEM. (F) Baseline-subtracted peak responses for homogeneous (N = 47, blue circles) and heterogeneous cells (N = 45, filled blue circles) stimulated with full-field uniform color patches. Black filled circles with bars represent means/SEM of responses for each group. (G) Same as in (F) except when both cell classes are stimulated with nonuniform color patches customized based on PC of subfields of heterogeneous cells. Filled black circles: mean value for respective cell classes. Asterisks: statistical significance (Wilcoxon rank sum test, P < 0.05) (H) Schematic description of how homogeneously and heterogeneously tuned neurons can represent different patches of a complex image through firing rate differences. Image taken from McGill Calibrated Colour Image Database (76) (photographer: unknown, McGill University).

Supplementary Materials

  • Supplementary Materials

    A distinct population of heterogeneously color-tuned neurons in macaque visual cortex

    Sunny Nigam, Sorin Pojoga, Valentin Dragoi

    Download Supplement

    This PDF file includes:

    • Table S1
    • Figs. S1 to S8

    Files in this Data Supplement:

Stay Connected to Science Advances

Navigate This Article