Spatial frequency and orientation tuning dynamics in area V1

Abstract

Spatial frequency (SF) and orientation tuning are intrinsic properties of neurons in primary visual cortex (area V1). To investigate the neural mechanisms mediating selectivity in the awake animal, we measured the temporal dynamics of SF and orientation tuning. We adapted a high-speed reverse-correlation method previously used to characterize orientation tuning dynamics in anesthetized animals to estimate efficiently the complete spatiotemporal receptive fields in area V1 of behaving macaques. We found that SF and orientation tuning are largely separable over time in single neurons. However, spatiotemporal receptive fields also contain a small nonseparable component that reflects a significant difference in response latency for low and high SF stimuli. The observed relationship between stimulus SF and latency represents a dynamic shift in SF tuning, and suggests that single V1 neurons might receive convergent input from the magno- and parvocellular processing streams. Although previous studies with anesthetized animals suggested that orientation tuning could change dramatically over time, we find no substantial evidence of dynamic changes in orientation tuning.

Figure 1

Complete STRF for a typical V1 neuron. STRFs described in this report are three-dimensional matrices with dimensions of time, SF, and orientation, as indicated by the schematic Inset. The complete STRF can be visualized as three sets of slices cut perpendicular to the cardinal axes. (a) Slices perpendicular to the time axis represent joint SF-orientation tuning at different response latencies. The color in each slice indicates the relative probability that each SF-orientation combination will elicit spikes at the indicated latency. (b) Slices perpendicular to the orientation axis represent the temporal evolution of SF tuning within a single orientation channel. (c) Slices perpendicular to the SF axis represent the temporal evolution of orientation tuning within a single SF channel. STRFs are depicted here by using a color map that spans the range ± max (|STRF|). cyc, cycles.

Figure 2

Latency measurements from STRFs. The time course of tuning can be visualized by plotting the overall variance of each SF-orientation slice as a function of Δt. (a) Solid line indicates the variance profile for a single V1 neuron. Horizontal solid and dashed lines indicate the mean ± 2SD (computed from Δt < 0; see text for details). (b) Latency to first spike is defined as the first time point when the variance exceeds twice the SD of the noncausal region of the STRF. Very short latencies apparent in the histogram (<20 ms) are caused by noise. Artifactually short estimates of the latency to first spike are caused by spurious peaks in the variance profile that can push the profile over the 2SD threshold. (c) Optimal latency, the latency at which the cell is maximally selective, is given by the peak of the variance curve (see text for details). For both histograms, the filled arrowheads and open horizontal bars indicate the mean ± SD.

Figure 3

Separability of SF, orientation, and time. (a) Complete STRF for a single V1 neuron. (b) Separability is evaluated in orthogonal SF-orientation, SF-time, and orientation-time planes (see text for details). (c) Linearly separable reconstruction of joint SF-orientation tuning for a typical V1 neuron based on simple marginal sums (red lines) and the first singular vector (green lines). The underlying color map shows measured SF-orientation tuning, and the overlying contours indicate the separable predictions. (d) Histogram shows the mean (±SEM) of the first 10 singular values from the SF-orientation SVD analysis for 52 V1 neurons. The red curve represents the mean (±SEM) percent STRF power accounted for by successive inclusion of additional singular vectors (see text for details). This analysis reveals a high degree of SF-orientation separability in V1. cyc, cycles.

Figure 4

Dynamic changes in SF tuning. (a) The solid curve indicates the time course of tuning of a typical V1 neuron (see Fig. 2a), the gray highlighted region shows the time window in which the neuron is responding (2 SD units around the mean of the best-fit Gaussian, as defined in the text). Filled circles represent the SF most likely to elicit a spike (i.e., the best SF) at each time slice (dashed line is the best linear fit). This cell shows an extreme change in SF tuning over time; in less than 25 ms, the best SF shifts by more than an octave from low to high SF. (Inset) Joint SF-orientation tuning at indicated latencies. (b) Distribution of SF shifts for all 52 neurons. Positive slopes indicate short latency responses to low SFs and long latency responses to high SFs (arrow indicates mean shift = +0.15 ± 0.25 cycles/degree per ms; mean ± SD). cyc, cycles.