Orientation selectivity in macaque V1: diversity and laminar dependence

Abstract

We studied the steady-state orientation selectivity of single neurons in macaque primary visual cortex (V1). To analyze the data, two measures of orientation tuning selectivity, circular variance and orientation bandwidth, were computed from the tuning curves. Circular variance is a global measure of the shape of the tuning curve, whereas orientation bandwidth is a local measure of the sharpness of the tuning curve around its peak. Circular variance in V1 was distributed broadly, indicating a great diversity of orientation selectivity. This diversity was also reflected in the individual cortical layers. However, there was a tendency for neurons with high circular variance, meaning low selectivity for orientation, to be concentrated in layers 4C, 3B, and 5. The relative variation of orientation bandwidth across the cortical layers was less than for circular variance, but it showed a similar laminar dependence. Neurons with large orientation bandwidth were found predominantly in layers 4C and 3B. There was a weak correlation between orientation selectivity and the level of spontaneous activity of the neurons. We also assigned a response modulation ratio for each cell, which is a measure of the linearity of spatial summation. Cells with low modulation ratios tended to have higher circular variance and bandwidth than those with high modulation ratios. These findings suggest a revision to the classical view that nonoriented receptive fields are principally found in layer 4C and the cytochrome oxidase-rich blobs in layer 2/3. Instead, a broad distribution of tuning selectivity is found in all cortical layers, and neurons that are weakly tuned for orientation are ubiquitous in V1 cortex.

Fig. 1.

Distribution of circular variance for the V1 population. Circular variance is defined in Materials and Methods.

Fig. 2.

Distribution of half-bandwidth at 1/ $\sqrt{2}$height for the V1 population.

Fig. 3.

Relationship between orientation bandwidth and circular variance. Scatterplot of orientation bandwidth and circular variance for all cells in the measured V1 population. Cells with bandwidth values larger than 60° are plotted at 60° to make better use of the range of the x-axis. a–f, Examples of individual tuning curves in different locations of the scatterplot. Thex-axis represents stimulus orientation, and its scale is the same for all graphs, from 0 to 180°, as indicated in thebottom plots. The y-axis is the response of the cell in spikes per second. The lower limit on the y-scale is zero for all graphs, and the upper limit is indicated in each case. Thedashed line represents the spontaneous rate of firing. In those examples in which the line is not visible, it means that the spontaneous rate was zero.

Fig. 4.

a, Plot of circular variance against relative cortical depth. b, Statistical summary of the scatterplot data in a. The middle curve drawn with a thicker line represents the median circular variance at different cortical depths. A window size of 100 μm, centered at each location, was used. The thinner curves to theleft and right represent the first and third quartiles of the distribution. Horizontal lines represent the laminar boundaries. Details about the histological reconstruction can be found in Hawken et al. (1988).

Fig. 5.

a, Plot of bandwidth against relative cortical depth. Cells with bandwidth values larger than 60° are plotted at 60° to make better use of the range of thex-axis. b, Statistical summary of the scatterplot data in a. The middle curve drawn with athicker line represents the median bandwidth at different cortical depths. A window size of 100 μm, centered at each location, was used. The thinner curves to the left andright represent the first and third quartiles of the distribution. The layer assignment and relative depth are as described in Figure 4.

Fig. 6.

a, Relationship between circular variance and orthogonal/preferred orientation ratio. b, Relationship between orientation bandwidth (half-width at 1/ $\sqrt{2}$height) and the orthogonal/preferred orientation ratio.

Fig. 7.

a, Plot of spontaneous firing rate against relative cortical depth. Cells with zero spontaneous rate are plotted at 0.1. The layer assignment and relative depth are as described in Figure 4. b, Statistical summary of the scatterplot data in a. The middle curve drawn with a thicker line represents the median spontaneous rate at different cortical depths. A window size of 100 μm, centered at each location, was used. The thinner curves to theleft and right represent the first and third quartiles of the distribution.

Fig. 8.

Relationship between orientation selectivity and spontaneous firing rate. a, Circular variance. b, Bandwidth (1/ $\sqrt{2}$ height). Cells with zero spontaneous rate are plotted at 0.1.

Fig. 9.

Dependence of circular variance as a function of spontaneous rate and the response at the orthogonal. The graph shows a scatterplot of the response at the orthogonal orientation versus the spontaneous rate of the neuron. The size of each data point corresponds to the circular variance of the tuning curve of the cell as illustrated by the scale on theright. Cells with a zero spontaneous rate are plotted with ay-coordinate of 0.1. Cells with a zero orthogonal response are plotted with an x-coordinate of 0.1.

Fig. 10.

The distribution of modulation ratio. The modulation ratio is the amplitude of first harmonic R(F1) divided by the mean spike rate R(F0) for an optimal achromatic drifting sinusoidal grating stimulus. High values of R(F1)/R(F0) indicate that the cells are modulated by spatial pattern in the visual image. Low values of R(F1)/R(F0) signify that such cells are excited, but their spike rate is not modulated up and down by the passage of the bars of a drifting grating.

Fig. 11.

Plot of modulation ratio against relative cortical depth. The continuous thin line gives the running median of the data using a window size of 100 μm, centered at each location. The layer assignment and relative depth are as described in Figure 4.

Fig. 12.

a, Plot of circular variance against modulation ratio. b, A color-coded density of smoothed joint distribution of circular variance versus modulation ratio. Thecolor scale represents the relative density of neurons in the distribution and ranges from 0 (blue) to 1 (red).

Fig. 13.

a, Plot of orientation bandwidth (1/ $\sqrt{2}$ height) against modulation ratio. b, A color-coded density of smoothed joint distribution of orientation bandwidth versus modulation ratio. The color scalerepresents the relative density of neurons in the distribution and ranges from 0 (blue) to 1 (red).

Fig. 14.

Plot of spontaneous firing rate against modulation ratio. Cells with zero spontaneous rate are plotted at 0.1.

Fig. 15.

Diagram model of orientation tuning curves. The tuning curve of a model neuron that has a triangular-shaped tuning curve and also (possibly) a constant baseline response added to it at all orientations. This tuning curve is characterized by the parameters B, the intersection of the sloping portion of the tuning curve with the flat level portion, r₀, the level of constant response, and r_p, the height of the peak response above the constant level.

Fig. 16.

Relationship between orientation bandwidth and circular variance for model neurons. This is the illustration of the calculations in that show how circular variance and bandwidth are related for a range of different model tuning curves, with the parameter c = r₀/r_p taking on the values 0, 0.01, 0.05, 0.1, and 0.2.