Colour and pattern selectivity of receptive fields in superior colliculus of marmoset monkeys

Abstract

The main subcortical visual targets of retinal output neurones (ganglion cells) are the parvocellular and magnocellular layers of the dorsal lateral geniculate nucleus (LGN) in the thalamus. In addition, a small and heterogeneous collection of ganglion cell axons projects to the koniocellular layers of the LGN, to the superior colliculus (SC), and to other subcortical targets. The functional (receptive field) properties and target specificity of these non-parvocellular, non-magnocellular populations remain poorly understood. It is known that one population of koniocellular layer cells in the LGN (blue-On cells) receives dominant functional input from short-wavelength sensitive (S or ‘blue') cones. Here we asked whether SC neurones also receive S cone inputs. We made extracellular recordings from single neurones (n = 38) in the SC of anaesthetised marmoset monkeys. Responses to drifting and flashed gratings providing defined levels of cone contrast were measured. The SC receptive fields we recorded were often binocular, showed ‘complex cell' like responses (On–Off responses), strong bandpass spatial frequency tuning, direction selectivity, and many showed strong and rapid habituation to repeatedly presented stimuli. We found no evidence for dominant S cone input to any SC neurone recorded. These data suggest that S cone signals may reach cortical pathways for colour vision exclusively through the koniocellular division of the lateral geniculate nucleus.

Figure 1. Example recordings from a neurone recorded in, and electrolytic lesion created by recording electrode in, marmoset superior colliculus

A–C, spatial frequency (A), direction (B), and temporal frequency (C) tuning curves measured in response to stimulations through either the contralateral (left column) or the ipsilateral (right column) eye of a visually responsive neurone in marmoset superior colliculus. Open green symbols show F0 response; filled blue symbols show F1 response; vertical lines at the rightmost x-axis limits show spontaneous activity; error bars report standard deviation. Smooth black lines in A show the difference of Gaussians model that best fits the F1 responses. Stimulus parameters for panel A: grating drift direction 145 deg, drift rate 5Hz, aperture diameter 4 deg. D–E, drawing (D) of coronal section (E) through the midbrain of the marmoset at the level of the superior colliculus, processed with Nissl stain (cresyl violet). Dashed box in D shows the region displayed in E. Black arrow points to electrolytic lesion. The overlay histograms show the encounter position of recorded neurones relative to the (dorsoventral) position where visually driven multiunit activity was observed. PAG: periaqueductal grey; SC: superior colliculus.

Figure 2. Nature of visual response in marmoset superior colliculus: example cells

A, B, D and E, peri-stimulus time histograms (PSTHs) obtained from four different marmoset superior colliculus (SC) neurones during the 500 ms preceding and 1000 ms following the onset of a drifting achromatic grating (red dots immediately above x-axis indicate the temporal period of the grating). During the interval preceding grating onset (at time = 0) the animal viewed a uniform grey screen of the same mean luminance as the grating. Responses are dominated either by the F1 (A and B) or F0 (D and F) component, and are either relatively transient (A and D) or sustained (B and E). C, population average PSTH for a sample of SC neurones. Stimulus temporal frequency and spatial phase varied across cells, so no period markers are provided. Red continuous line shows best fit of stretched exponential decay function. F and I, PSTHs obtained from example parvocellular (F) and magnocellular (I) neurones recorded in marmoset lateral geniculate nucleus (LGN).

Figure 3. Population average response to slow, square wave modulation of a large uniform field

A, superior colliculus population average response to two cycles of 0.5 Hz square wave temporal modulation of an achromatic (thin grey trace) or S cone selective (thick blue trace) uniform field. Note response to offset of S cone modulation (arrow). The temporal profile of the stimulus is illustrated below the graph. B, population average temporal frequency tuning for drifting achromatic gratings. Error bars show standard errors of the mean.

Figure 4. Selectivity of cone inputs to superior colliculus revealed via spatial and contrast tuning: example cells

A–C, spatial frequency tuning (A) and contrast response (B) of a superior colliculus neurone for drifting achromatic (open circles), ML cone selective (magenta triangles) and SWS cone selective (blue squares) gratings. C, PSTH recorded over the first 150 ms following onset of a drifting achromatic grating or varying contrast (constructed from data shown in B). The discharge of the cell is modulated at the frequency of stimulation (F1). Colour code in C indicates grating contrast as identified by x-axis location of the corresponding collared vertical line in B. Error bars (sometimes concealed by data points) show standard errors of the mean. D–F, same as A–C but for a cell in which stimulation primarily induced an elevation in the mean rate of discharge (F0). G–I, same as A–C but for another cell in which stimulation primarily induced an elevation in the mean rate of discharge (F0). This cell shows the strongest indication of SWS cone input (at low spatial frequencies) of all the cells in our sample. Baseline responses (maintained discharge) have been subtracted from amplitude graphs.

Figure 5. Selectivity of cone inputs to superior colliculus revealed via spatial and contrast tuning: population average

A and B, population average spatial frequency tuning (A) and contrast response (B) calculated across our sample of 29 superior colliculus neurones for drifting achromatic (open symbols), ML cone selective (large magenta symbols) and SWS cone selective (small blue symbols) gratings. C and D, same as A and B but prior to averaging across cells, each individual cell's tuning curve was normalized to its maximum achromatic response. Normalization was done separately for spatial frequency and contrast data. Data show that the achromatic tuning curves are almost completely explained by the ML tuning curves, with no contribution from SWS cones. Error bars show standard errors of the mean; n listed in each panel identifies the number of neurones contributing to the population average. Baseline responses (maintained discharge) have been subtracted from amplitude graphs.

Figure 6. Comparison of cone inputs to bandpass and lowpass superior colliculus neurones

A and C, population average raw (A) and normalized (D) spatial frequency tuning for drifting achromatic (large open symbols), ML cone selective (large magenta symbols) and SWS cone selective (small blue symbols) gratings; calculated for bandpass superior colliculus neurones ([response to lowest SF]/[response to best SF] < 0.5). B and D, same as A and C but calculated only for lowpass neurones ([response to lowest SF]/[response to best SF]≥ 0.5). Error bars show standard errors of the mean; n listed in each panel identifies the number of neurones contributing to the population average. Baseline responses (maintained discharge) have been subtracted from amplitude graphs.

Figure 7. Comparison of the relative strength of S cone inputs to superior colliculus (SC) neurones and to neurones in lateral geniculate nucleus (LGN)

A and B, population average spatial frequency (A) and contrast (B) tuning of SC neurones for drifting achromatic gratings (large open circles) and SWS cone selective gratings (small blue symbols); data are reproduced from Fig. 5A. Filled grey (upper) and dashed blue (lower) polygons show bootstrapped mean and 95% confidence intervals for the equivalent population tuning of parvocellular (P) LGN neurones. C and D, same as A and B but comparison is now with magnocellular (M) LGN neurones. Error bars show standard errors of the mean; n listed in each panel identifies the number of superior colliculus neurones contributing to the population average, and the number of P and M neurones drawn from our LGN database on each bootstrap resample. Baseline responses (maintained discharge) have been subtracted from amplitude graphs.

Figure 8. Summary of S cone signal strength in subcortical targets and primary visual cortex

Panels A–E show scatterplots and marginal histograms of relative S cone weight (S/[S + ML]) obtained in superior colliculus (SC, panel A), primary visual cortex (V1, panel B) and three populations in lateral geniculate nucleus: magnocellular cells (M, panel C); blue-On and blue-Off cells (Bon + Boff, panel D); parvocellular cells (P, panel E). For each panel the y-axis show measured S cone weight, and the x-axis shows the prediction of a simple ‘random connections’ model where the weight is determined simply by the local proportion of S cones at the visual field eccentricity of the recorded neurone . Panel F shows, at enlarged scale, convex hull outlines of the non-blue populations. Note heavy overlap of these distributions. One outlier M cell (cf. panel C) was not included in the convex hull. V1 data re-analysed from Hashemi-Nezhad et al. (2008). LGN data pooled from the current study and two of our previous studies (Hashemi-Nezhad et al. 2008; Tailby et al. 2008b).

Figure 9. Direction tuning of superior colliculus neurones for drifting achromatic gratings

A–C, direction tuning curves for three example superior colliculus neurones: a moderately orientation tuned neurone (A), a moderately direction tuned neurone (B), and the most strongly direction tuned neurone in our sample (C). Error bars show standard errors of the mean; DI: direction index; OI: orientation index, calculated as explained in the text. D, population average (thick blue line) and median (thin red line) direction tuning curve of our sample of superior colliculus neurones; thin grey lines show individual direction tuning curves, demonstrating variability across cells. DI and OI refer to values calculated on the average curve (blue line). Data are aligned to the direction of maximal response and normalized to maximum response amplitude. Error bars show standard errors of the mean; n in panel identifies D the number of neurones contributing to the population average. E, scatterplot of DI against OI for the 27 cells in our sample. F, histogram of DI; mean and median DI calculated from the values obtained in individual cells (shown in E). G, histogram of OI; mean and median OI calculated from the values obtained in individual cells (shown in E). Baseline responses (maintained discharge) have been subtracted from amplitude graphs.