Space and time maps of cone photoreceptor signals in macaque lateral geniculate nucleus

Abstract

We studied neurons in the central visual field representation of the lateral geniculate nucleus (LGN) in macaque monkeys by mapping their receptive fields in space and time. The mapping was performed by reverse correlation of a spike train of a neuron with pseudorandom, binary level stimuli (m-sequence grids). Black and white m-sequence grids were used to map the receptive field for luminance. The locations of receptive field center and surround were determined from this luminance map. To map the contribution of each cone class to the receptive field, we designed red-green or blue-yellow m-sequence grids to isolate the influence of that cone (long, middle, or short wavelength-sensitive: L, M, or S). Magnocellular neurons generally received synergistic input from L and M cones in both the center and the surround. A minority had cone-antagonistic (M-L) input to the surround. Red-green opponent parvocellular neurons received opponent cone input (L+M- or M+L-) that overlapped in space, as sampled by our stimulus grid, but that had somewhat different extents. For example, an L+ center parvocellular neuron would be L+/M- in both center and surround, but the L+ signal would be stronger in the center and the M- signal stronger in the surround. Accordingly, the luminance receptive field would be spatially antagonistic: on-center/off-surround. The space-time maps also characterized LGN dynamics. For example, magnocellular responses were transient, red-green parvocellular responses were more sustained, and blue-on responses were the most sustained for both luminance and cone-isolating stimuli. For all cell types the surround response peaked 8-10 msec later than the center response.

Fig. 1.

The cone-specific and mixed surround models for red–green opponent parvocellular neurons, specifically L-on/M-off type I neurons [after Reid and Shapley (1992), their Fig. 1].Stimuli, Representations of the binary m-sequence grid stimuli, which are either luminance modulated (between black and white) or chromatically modulated between hues that modulate either L cones or M cones in isolation. For the L-cone stimulus the red is brighter than the mean (on); the green is darker than the mean (off). For the M-cone stimulus the green is brighter (on); the red is darker (off).Model, Diagrammatic representations of receptive fields, color-coded in terms of the cone-isolating stimuli that drive them. In the cone-specific surround model (first row) the L-on center (L+) is opposed by an M-off surround (M−). In the mixed surround model the L-on center is opposed both by M-off and L-off surround (L− and M−). Predicted Results, Spatial weighting functions as mapped with the luminance, L-cone, and M-cone stimuli. Responses are coded in false color: on (+) inred and off (−) in blue. Responses of the center cone type, the L cone, represent the critical test between models. In the cone-specific surround the L-cone responses are exclusively on. In the mixed surround (arrow), the L-cone responses are on-center/off-surround.

Fig. 2.

Top, Spatial weighting functions of an off-center magnocellular neuron (23° eccentric) measured with L-cone-isolating, M-cone-isolating, and luminance-modulated stimuli. Each panel corresponds to the same region of visual space, 5.2° on a side. On responses are coded in redand off in blue; the brighter the red orblue, the stronger the response. All maps, L- and M-cone isolating and luminance, have an off-center/on-surround organization. Individual pixels (0.43°) are outlined in black. Pixels in the center (defined as in Materials and Methods) are outlined in white. Surround is a ring of four pixels around the center. Data are smoothed by a function that falls to <10% at one-half pixel. Delay between stimulus and response, 15–30 msec. Bottom, Radial weighing functions calculated from the spatial weighting function above (see Materials and Methods). For comparison with the spatial weighting function, the radial weighing function is reflected about the origin so that each value is shown twice. To facilitate comparison, we have given all responses in units of spikes/(sec · C), whereC is the cone contrast of the stimulus (see Materials and Methods).

Fig. 3.

Spatiotemporal weighting functions of the same magnocellular neuron (Fig. 2) for multiple delays, from the 0 msec bin (0–15 msec) to the 74 msec bin (74–89 msec). Responses to different stimuli, shown fromleft to right: L cone, M cone, and luminance. Conventions are as in Figure 2. Off-center response starts in the 0 msec bin, peaks in the 15 msec bin, and reverses sign (rebounds) at either 30 or 44 msec. On-surround starts at 15, peaks at 30, and reverses at 44 msec. The M-cone response is delayed slightly relative to the L-cone response. Scale at bottomindicates response magnitudes in spikes/(sec · C), where C is the cone contrast of the stimulus.

Fig. 4.

Temporal weighting functions of the same magnocellular neuron (Figs. 2, 3) for receptive field center (thick lines) and surround (thin lines). Each data point is for a range of times between stimulus and response (sampled at the stimulus update rate, or 14.8 msec; short tick marks). The data points marked with caretscorrespond to responses during the first bin (in the range 0–14.8 msec). Time labels (long tick marks) are interpolated with respect to the data points (short tick marks), as specified in Materials and Methods. Note that the M-cone response is both weaker and somewhat slower than the L-cone response. All responses are in spikes/(sec · C), where C is the cone contrast of the stimulus.

Fig. 5.

Spatial weighting functions and radial weighing functions of two parvocellular neurons as measured with L-cone-isolating, M-cone-isolating, and luminance-modulated stimuli (conventions are as in Fig. 2). A, L-on/M-off neuron, 9° eccentric. The on-center/off-surround luminance response was used to define the receptive field center, outlined in white(see Materials and Methods). Note that neither the center cone type (L) nor the surround cone type (M) exhibits center/surround opponency (Fig. 1, arrow). B, M-off/L-on neuron, 11° eccentric. Although the signatures of the L-cone and M-cone responses are the same as in A, the M-off response dominates. Total region shown, 1.0° on a side; pixel size, 7.5 min. Delay between stimulus and response, 15–44 msec, the sum of the 15–30 and the 30–44 msec bins (see Materials and Methods). Because the luminance weighting function was much weaker than L-cone and M-cone weighting functions, it was multiplied by a factor of 2.0 to increase visibility. Conventions are as in Figure 2.

Fig. 6.

Spatiotemporal weighting functions of the same two parvocellular neurons (Fig. 5). A, L-on/M-off neuron.B, M-off/L-on neuron. Conventions are as in Figure3.

Fig. 7.

Temporal weighting functions of the same two parvocellular neurons (Figs. 5, 6). A, L-on/M-off neuron. Note that the L-cone response is on in both the center (thick line) and in the surround (thin line), but the center response is stronger. The M-cone response is off in both regions, but the surround is stronger. The opposite relationships between center and surround hold for the M-off/L-on neuron (B). Conventions are as in Figure 4.

Fig. 8.

Spatial weighting functions and radial weighing functions of an S-on/L-off neuron (12° eccentric, recorded at the bottom of the parvocellular layers), as measured with L-, M-, and S-cone-isolating and luminance-modulated stimuli. Total region shown, 1.25° on a side; pixel size, 7.5 min. Delay between stimulus and response, 15–44 msec, the sum of the 15–30 and the 30–44 msec bins (see Materials and Methods). The luminance weighting function was multiplied by 2.0 to increase visibility. Conventions are as in Figure2.

Fig. 9.

Spatiotemporal weighting functions of the same S-on/L-off neuron (Fig. 8). Conventions are as in Figure3.

Fig. 10.

Temporal weighting functions for all red–green opponent parvocellular neurons (A–D) and S-cone-dominated neurons (E, F). For each cell type three or four sets of temporal weighting functions are plotted separately for both center (top) and surround (bottom); L-cone, M-cone, luminance, and, for some cells, S-cone responses are shown. For each cell all weighting functions are normalized by the same value. Red–green responses are normalized by the peak of the center response for the center cone type (L cone in A, B; M cone in C, D). S-on/L-off responses (E) are normalized by the S-cone surround peak (which was stronger than the S center). S-off responses (F) are normalized by the S-cone center. Data from four neurons that gave the weakest responses [normalization value <3.0 (spikes/sec)/(unit contrast)] are plotted in gray. Note that for red–green neurons the center cone types (L cone, A, B; M cone,C, D) have the same sign responses in the center and surround (with only two clear exceptions, shown byarrows). The luminance responses, however, have opposite signs in the center and surround.

Fig. 11.

Temporal weighting functions for all magnocellular neurons. For each cell type three or four sets of temporal weighting functions are plotted separately for both center (top) and surround (bottom); L-cone, M-cone, luminance, and, for some cells, S-cone responses are shown. For each cell all weighting functions are normalized by the same value, the peak of the luminance response.

Fig. 12.

Histogram of the sustained component (see Results) of all magnocellular neurons, red–green opponent parvocellular neurons, and blue-on cells. A, Responses to luminance stimuli. B, Responses to cone-isolating stimuli for the dominant cone type (L cone for magnocellular, center cone for red–green parvocellular, S cone for blue-on). The three populations were nonoverlapping, whatever the stimulus type.

Fig. 13.

Scatter plots of normalized cone weights, following Derrington et al. (1984), plotted for all neurons recorded in parvocellular layers. Shown are M-cone weights plotted versus L-cone weights, in which magnitudes of S-cone weights are determined by the distance from diagonal lines. Points near the diagonal lines are from cells that received negligible S-cone input. Points for which no S-cone measurements were performed are plotted outside the diagonal lines. Symbols signify the eight classes of cells. Antagonistic L-cone versus M-cone responses are in the second (II) and fourth (IV) quadrants. Nonantagonistic (mixed) responses are in the first (I) and third (III) quadrants. Each class clusters distinctly in the plot ofCenter weights (A), but less so in plots of Surround (B) andTotal (C) weights. The two cells that had clear mixed surrounds (Fig. 10A,B) are indicated with arrows (B).

Fig. 14.

Scatter plots of normalized cone weights for magnocellular neurons, as in Figure 13. On-center cells are indicated by symbols with light centers; off-center cells are indicated by symbols with dark centers.

Fig. 15.

Scatter plots of response strengths (not normalized) in the surrounds versus the centers for L-cone (A), M-cone (B), S-cone (C), and luminance responses (D) in units of spikes/(sec ·C), where C is the cone contrast of the stimulus. Data are shown for all neurons recorded in parvocellular layers; the symbols are as in Figure 13. Antagonistic center/surround responses fall in the second and fourth quadrants; nonantagonistic responses fall in the first and third quadrants (seeinsets). With few exceptions, all luminance responses (D) had antagonistic centers and surrounds. Most L-cone responses (A) and all M-cone responses (B) had nonantagonistic centers and surrounds (exceptions are indicated with arrows in A, as in Figs. 10, 13).

Fig. 16.

Scatter plots of magnocellular response strengths in the surrounds versus the centers for L-cone (A), M-cone (B), and luminance responses (C) in units of spikes/(sec · C), where C is the cone contrast of the stimulus. All luminance responses had antagonistic centers and surrounds, as did the L-cone responses. Three of the on-center cells did not receive antagonistic input from the M-cones in the surrounds (B, first quadrant), whereas three did (B, fourth quadrant).

Fig. 17.

Peak times of L- and M-cone responses in centers (A–C) and of luminance responses in centers and surrounds (D–F). A, Scatter plot of M-cone peak times versus L-cone peak times for red–green opponent parvocellular neurons. L-cone responses were faster for L-cone center cells (circles), and M-cone responses were faster for M-cone center cells (squares); thesymbols are as in Figures 13-16.B, For magnocellular neurons the L-cone responses were faster. C, Histogram of differences between M-cone and L-cone peaks. D, E, Scatter plots of surround versus center peaks for red–green opponent parvocellular (D) and magnocellular (E) neurons. Three M-cone center cells with noisy surround responses had nominal peaks >60 msec. These cells were excluded. F, Histogram of differences between surround and center peaks. With two exceptions, all surrounds were slower.