Orientation anisotropies in macaque visual areas

Abstract

In mammals, a larger number of neurons in V1 are devoted to cardinal (horizontal and vertical) orientations than to oblique orientations. However, electrophysiological results from the macaque monkey visual cortex are controversial. Both isotropic and anisotropic orientation distributions have been reported. It is also unclear whether different visual areas along the visual hierarchy have different orientation anisotropies. We analyzed orientation maps in a large set of intrinsic signal optical imaging data and found that both V1 and V4 exhibited significant orientation anisotropies. However, their overrepresented orientations were very different: in V1, both cardinal and radial orientations were overrepresented, while in V4, only cardinal bias was presented. These findings suggest that different cortical areas have evolved to emphasize different features that are suitable for their functional purposes, a factor that needs to be considered when efforts are made to explain the relationships between the visual environment and the cortical representation and between the cortical representation and visual perception.

Keywords: ISOI; macaque; orientation anisotropy; visual cortex.

Fig. 1.

Illustration of three types of orientation anisotropies. (A) Illustration of the four grating stimuli used in the present study and one that is presented at the lower left visual field. Black star represents the fovea. The dashed line represents the radial angle (45°) of the location that the stimulus presents. (B) The left and right lower visual field regions and their mean radial angles (dashed lines) corresponding to the right hemisphere (RH, cyan, same below) and left hemisphere (LH, pink, same below) visual cortices imaged in this study. (C–E) Three types of orientation bias models. (C) The cardinal bias model, in which more neurons prefer horizontal (0°) and vertical (90°) orientations than oblique orientations. Left is a polar plot of the distribution. Dashed line represents 0° orientation. Right is a Cartesian plot of similar distributions on the left, in which left- and right-hemispherical distributions are plotted in different colors as in B. In this model, orientation anisotropy is independent of retinotopic location and thus is identical for distributions from the left and right hemispheres. The amplitude of the cardinal anisotropy is denoted as A_c. A₀ represents the baseline. (D) The radial bias model, in which more neurons prefer the orientation pointing toward the foveal fixation (radial angle; e.g., 45° for the stimulus location in A). Right plots the preferred orientation distributions of the left and right hemispheres shown in B, which are symmetrical about the 90° orientation. Note that since the radial angle varies with the cortical locations, each peak of the distribution represents a sum of a range of radial angles. A_r represents the amplitude of the radial bias. (E) The combined model is a linear summation of cardinal and radial biases. The shape of the distribution depends on both the location of the visual field under examination and the relative strengths of the two components.

Fig. 2.

Single-case orientation anisotropy in V1 and V4. (A) Illustration of a typical V1 imaging chamber location (dashed circle) and regions of V1 being analyzed (shading). Scale bar, 10 mm. A, anterior; L, lateral; sts, superior temporal sulcus. (B) An example V1 orientation polar map, based on vector summing of four single-orientation maps (SI Appendix, Fig. S1 E–H), in which different colors represent different preferred orientations. The color index is shown under F. Blood vessel pixels (gray) were excluded from the calculation. Scale bar, 2 mm. (C) The visual field represented by V1 shown in B. Black star represents the fovea. Darkness represents the logarithmic number of pixels. The oblique dashed line represents the mean radial angles of these pixels (${\overline{\theta }}_{\text{r}}=51°$) (SI Appendix, Fig. S3 I and J). HM, horizontal meridian. (D) The orientation distribution calculated from the polar map shown in B (dotted curves, same in three panels) and three types of fitting curves (colored curves). Each data point represents a percentage of the pixels preferring orientations within the 10° bin (±5°). Goodness of fit (adjusted R²) is labeled for each model. The horizontal dashed lines represent the uniform distribution (5.56%). Vertical dashed line represents 90° orientation. (E–H) A single case example of a right-hemispherical V4 using the same plot conventions as in A–D.

Fig. 3.

V1 and V4 population results and fittings of the combined model. (A) The mean distributions of preferred orientations for left-hemisphere (LH, pink, n = 26) and right-hemisphere (RH, cyan, n = 22) V1 cases (data points) and the means of their fittings by the combined model (curves). The horizontal dashed line represents the uniform distribution (5.56%). The vertical dashed line represents 90° orientation. Asterisks at the Bottom of the plot represent significant differences between LH and RH distributions at each orientation bin (*P < 0.05; **P < 0.01; ***P < 0.001; symbol representation is the same in the article; Wilcoxon rank sum test with Bonferroni correction). Error bar: 95% CI, curve shading: 95% CI (same below). (B) The mean orientation distribution of all V1 cases (purple, n = 48), in which every left-hemisphere V1 distribution was flipped horizontally (about the 90° axis, vertical gray dashed line) and treated as right-hemisphere V1 data. Plot conventions same as in A. Gray data points and solid gray line represent the distribution of a shuffled control (see Materials and Methods). (C) The mean cardinal and radial components of V1 combined model fittings. (D–F) Similar to A–C, for V4 cases. (G) Distribution of amplitudes of cardinal and radial components (A_c and A_r) for V1 cases and their shuffled control shown in B. The mean and 95% CI are indicated by “+”. Asterisks represent the significant differences between V1 and its shuffled control (*P < 0.05; ***P < 0.001, two-way ANOVA followed by Bonferroni post hoc tests, same in G–I). (H) Similar to G, for V4 cases. (I) Cardinal and radial modulation ratios in V1 and V4, calculated with the formulas ${\text{A}}_{\text{c}}/\left(100/18\right)$ and ${\text{A}}_{\text{r}}/\left(100/18\right)$.

Fig. 4.

Illustration of orientation anisotropies in macaque V1 and V4. The figure illustrates V1 and V4 anisotropic types and amplitudes. The lower visual field is divided into left (dark) and right (light) quadrants, which correspond to the right and left hemispheres, respectively. Black star represents the fovea. Dashed lines represent mean radial angles, which are 45° and 135° for the lower left and lower right, same below. The red, blue, and gray fillings represent cardinal, radial, and isotropic components. For the lower visual field, V1 contains an overrepresentation of orientations in both cardinal (horizontal and vertical) and radial axes. V4 contains an overrepresentation of orientations along the cardinal axes only.