Ehud Kaplan

X and Y cells in the lateral geniculate nucleus of macaque monkeys.

1. Cells of the lateral geniculate nucleus (l.g.n.) in macaque monkeys were sorted into two functional groups on the basis of spatial summation of visually evoked neural signals. 2. Cells were called X cells if their responses to contrast reversal of fine sine gratings were at the fundamental temporal modulation frequency with null positions one quarter of a cycle away from positions for peak response. Cells were called Y cells if their responses to such stimuli were at twice the modulation frequency and were approximately independent of spatial phase. 3. Ninety‐nine percent of the cells in the four dorsal parvocellular layers of the l.g.n. were X cells; about seventy‐five percent of the cells in the two ventral magnocellular layers were also X cells. The remainder were Y cells. 4. We confirmed previous findings that magnocellular cells had a shorter latency of response to electrical stimulation of the optic chiasm. 5. Magnocellular cells had much higher contrast sensitivities than did parvocellular cells. 6. Therefore, two distinct classes of X cells exist in the macaque l.g.n.: parvocellular X cells and magnocellular X cells. The great difference in their properties suggests that they have different functions in vision. The Y cells in the magnocellular layers form a third functional group with spatial properties distinctly different from the X cells. 7. We propose that the magnocellular layers of the macaque monkeys l.g.n. may be homologous to the A and A1 layers of the cats l.g.n.

Chapter 7 New views of primate retinal function

This review will focus on some of the recent advances in our knowledge of the monkey retina, particularly those dealing with the physiological properties of retinal ganglion cells and thalamic neurons in macaque monkey

Fractal character of the neural spike train in the visual system of the cat.

We used a variety of statistical measures to identify the point process that describes the maintained discharge of retinal ganglion cells (RGCs) and neurons in the lateral geniculate nucleus (LGN) of the cat. These measures are based on both interevent intervals and event counts and include the interevent-interval histogram, rescaled range analysis, the event-number histogram, the Fano factor, Allan factor, and the periodogram. In addition, we applied these measures to surrogate versions of the data, generated by random shuffling of the order of interevent intervals. The continuing statistics reveal 1/f-type fluctuations in the data (long-duration power-law correlation), which are not present in the shuffled data. Estimates of the fractal exponents measured for RGC- and their target LGN-spike trains are similar in value, indicating that the fractal behavior either is transmitted form one cell to the other or has a common origin. The gamma-r renewal process model, often used in the analysis of visual-neuron interevent intervals, describes certain short-term features of the RGC and LGN data reasonably well but fails to account for the long-duration correlation. We present a new model for visual-system nerve-spike firings: a gamma-r renewal process whose mean is modulated by fractal binomial noise. This fractal, doubly stochastic point process characterizes the statistical behavior of both RGC and LGN data sets remarkably well.

Contrast affects the transmission of visual information through the mammalian lateral geniculate nucleus.

1. We recorded with one electrode action potentials of single principal cells in the lateral geniculate nucleus (l.g.n.) of cats and monkeys, together with their retinal inputs, recorded as synaptic potentials (S potentials; Bishop, Burke & Davis, 1958; Cleland, Dubin & Levick, 1971; Kaplan & Shapley, 1984). 2. We studied the effect of stimulus contrast on the transmission of visual information from the retina to the l.g.n., compared the spontaneous discharge of l.g.n. cells with that of their retinal inputs, and studied the driven (modulated) and maintained (unmodulated) discharge of l.g.n. neurones and their retinal drives. 3. The spontaneous discharge of l.g.n. cells was considerably lower than that of their retinal drives. 4. The maintained (unmodulated) discharge of l.g.n. cells during stimulation was lower than that of their retinal drives, and was largely unaffected by the stimulus contrast. 5. The responses of both the retinal input and l.g.n. cells increased with contrast, but at different rates: a given increment of contrast caused a larger increment of response in the retinal input than in the l.g.n. target cells. 6. The transmission ratio (l.g.n. response/retinal response) for most cells depended upon the stimulus contrast. This dependence indicates the presence of a non‐linear contrast gain control. 7. The amount by which the l.g.n. attenuated the retinal input depended upon the temporal frequency, and, to a lesser extent, upon the spatial frequency of the stimulus. 8. The effect of contrast on signal transmission between the retina and l.g.n. was essentially the same in the macaque monkey as in the cat. 9. The attenuation of the retinal input by the l.g.n. contrast gain control could serve to prevent saturation and extend the dynamic range of cortical units, which probably receive input from several l.g.n. units.

Contrast sensitivity and spatial frequency response of primate cortical neurons in and around the cytochrome oxidase blobs

The striate cortex of macaque monkeys contains an array of patches which stain heavily for the enzyme cytochrome oxidase (CO blobs). Cells inside and outside these blobs are often described as belonging to two distinct populations or streams. In order to better understand the function of the CO blobs, we measured the contrast sensitivity and spatial frequency response of single neurons in and around the CO blobs. Density profiles of each blob were assessed using a new quantitative method, and correlations of local CO density with the physiology were noted. We found that the CO density dropped off gradually with distance from blob centers: in a typical blob the CO density dropped from 75% to 25% over 100 microns. Recordings were confined to cortical layers 2/3. Most neurons in these layers have poor contrast sensitivity, similar to that of the parvocellular neurons in the lateral geniculate nucleus. However, in a small proportion of layers 2/3 neurons we found higher contrast sensitivity, similar to that of the magnocellular neurons. These neurons were found to cluster near blob centers. This finding is consistent with (indirect) parvocellular input spread uniformly throughout layers 2/3, and (indirect) magnocellular input focused on CO blobs. We also measured spatial tuning curves for both single units and multiple unit activity. In agreement with other workers we found that the optimal spatial frequencies of cells near blob centers were low (median 2.8 c/deg), while the optimal frequencies of cells in the interblob regions were spread over a wide range of spatial frequencies. The high cut-off spatial frequency of multi-unit activity increased with distance from blob centers. We found no correlation between spatial bandwidth and distance from blob centers. All measured physiological properties varied gradually with distance from CO blob centers. This suggests that the view of blob cells subserving visual functions which are entirely distinct from non-blob cells may have to be reevaluated.

Chapter 2 The dynamics of primate retinal ganglion cells

A knowledge of the dynamics (temporal properties) of neuronal populations is essential for an understanding of their function, and is also crucial when one attempts to develop computational or mathematical models of the neurons. Here we review the temporal properties of the receptive fields (RFs) of the two best-studied types of ganglion cells in the primate retina, those that project to the parvocellular (P) and magnocellular (M) layers of the dorsal lateral geniculate nucleus. The center and surround mechanisms of the P RFs are approximately linear, and their impulse responses are very similar, although the surround lags the center by a few milliseconds. The center and surround are chromatically opponent. With the appropriate stimulus, one can find significant nonlinearities in their responses, and also in the interaction between the center and surround. The phase lag between the responses of the center and surround depends on the temporal frequency, so that at high temporal frequency the antagonism between them is reduced or abolished. The temporal responses of M cells are nonlinear, and with increasing contrast they show the effects of a contrast gain control. The different dynamical properties of the two populations suggest that M cells participate in motion analysis, while P cells are used for the analysis of form, texture, and perhaps color.

The receptive field of the primate P retinal ganglion cell, II: Nonlinear dynamics

The receptive-field properties of retinal ganglion cells (RGCs) provide information about early visual processing. In the primate retina, P cells form the largest class of RGCs (Rodieck, 1988). A detailed exploration of the dynamics of the two subdivisions of the P-cell receptive field--the center and the surround--was undertaken. In the preceding paper (Benardete & Kaplan, 1996), the first-order responses of the center and the surround of P cells were described, which were obtained with a new technique, the multiple m-sequence stimulus (Benardete & Victor, 1994). In this paper, the investigation of P-cell responses measured as S-potentials in the lateral geniculate nucleus (LGN) is continued, and significant nonlinear, second-order responses from the center and the surround are described. These responses are quantified by fitting a mathematical model, the linear-nonlinear-linear (LNL) model (Korenberg, 1973; Korenberg & Hunter, 1986; Victor, 1988) to the data. In a second series of experiments, demonstration that steady illumination of the surround modifies the gain of the center to contrast signals (see also Kaplan & Shapley, 1989) is made. In P ON cells, increasing the steady illumination of the surround decreases the gain and speeds up the centers first-order response. In P OFF cells, increasing the steady illumination of the surround increases the gain of the center while speeding up the response. The results of both sets of experiments are related to the known anatomy and physiology of the P cell.

A population study of integrate-and-fire-or-burst neurons

Any realistic model of the neuronal pathway from the retina to the visual cortex (V1) must account for the burstingbehavior of neurons in the lateral geniculate nucleus (LGN). A robust but minimal model, the integrate- and-fire-or-burst (IFB) model, has recently been proposed for individual LGN neurons. Based on this, we derive a dynamic population model and study a population of such LGN cells. This population model, the first simulation of its kind evolving in a two-dimensional phase space, is used to study the behavior of bursting populations in response to diverse stimulus conditions.

Hue maps in primate striate cortex.

The macaque striate cortex (V1) contains neurons that respond preferentially to various hues. The properties of these hue-selective neurons have been studied extensively at the single-unit level, but it is unclear how stimulus hue is represented by the distribution of activity across neuronal populations in V1. Here we use the intrinsic optical signal to image V1 responses to spatially uniform stimuli of various hues. We found that (1) each of these stimuli activates an array of patches in the supragranular layers of the parafoveal V1; (2) the patches activated by different hues overlapped partially; 3) the peak locations of these patches were determined by stimulus hue. The peaks associated with various hues form well-separated clusters, in which nearby peaks represent perceptually similar hues. Each cluster represents a full gamut of hue in a small cortical area ( approximately 160 microm long). The hue order is preserved within each peak cluster, but the clusters have various geometrical shapes. These clusters were co-localized with regions that responded preferentially to chromatic gratings compared with achromatic ones. Our results suggest that V1 contains an array of hue maps, in which the hue of a stimulus is represented by the location of the peak response to the stimulus. The orderly, organized hue maps in V1, together with the recently discovered hue maps in the extrastriate cortical area V2, are likely to play an important role in hue perception in primates.

Dynamics of primate P retinal ganglion cells: responses to chromatic and achromatic stimuli

1 The majority of primate retinal ganglion cells (RGCs) project to the parvocellular layers of the lateral geniculate nucleus (LGN). These P cells play a central role in early visual processing. 2 An improved method of systems analysis has allowed us to explore the dynamics of the colour‐opponent subregions of P‐cell receptive fields with a single chromatic stimulus. The data show that the centre and surround subregions of the P‐cell receptive field have similar temporal responses, but the surround is slightly delayed. The centre and surround demonstrate a large degree of chromatic selectivity. 3 The responses of the centre and surround subregions were fitted with a linear model and the model was used to predict the responses of P cells to new chromatic and achromatic stimuli. Although linear models predict the chromatic responses well, simple linear combinations of centre and surround responses fail to predict P‐cell responses to achromatic stimuli. 4 The temporal responses of the different subpopulations of P cells, such as ON/OFF or L‐centre/M‐centre were not significantly different.