Introduction

Classical views of the optic chiasm maintain four propositions about the retinofugal pathways: (1) each optic nerve contains a retinotopic representation of its respective retinal surface; (2) this retinotopic map in the nerve is the basis for the subsequent segregation of the decussating from the non-decussating fibers; (3) this retinotopy in the nerve is also the basis for the presence of retinotopy found within the half-retinal maps in the optic tracts; and (4) the half-retinal maps from each optic nerve are brought together within the chiasm to yield a unified, binocularly congruent, map in the optic tract (Brodal, 1969; DukeElder, 1961; Polyak, 1957; Wolff, 1940). The appeal of this classical view is in its simplicity, based on the assumption that the retinofugal pathway should replicate the sensory surface along its course. We now know that each of these four propositions is incorrect, and that the error is not one simply of degree or extent (Guillery, 1982, 1991). Rather, the above description of the visual pathway is fundamentally flawed because it has failed to take into account the constraints under which the pathway develops. We shall first consider the evidence for rejecting the classical view, from recent studies on the organization of the retinofugal pathway in adult animals and on the development of that organization. We shall then describe three transformations in the fiber order which all occur in the chiasmatic region, two of which were only recently recognized, and for which we must account.

Observations from adult organization

The difference in the fiber order in the optic nerve and tract

The discharges of ON- and OFF-center X and Y retinal ganglion cells in the presence of stationary patterns or of a uniform field of photopic luminance were recorded from urethane-anesthetized adult cats. The interval statistics and power spectra of these discharges were determined from these discharge records. The patterned stimuli were selected and positioned with respect to a cell's receptive field so as to generate steady discharges that were different in mean discharge rate from that cell's discharge for the diffuse field. The interval statistics of discharges recorded for diffuse or patterned illumination for all cell types can be modeled, approximately, as coming from renewal processes with gamma-distributed intervals. The gamma order of the interval distributions was found to be nearly proportional to the mean discharge rate for X cells, but not for Y cells. Typical values for the gamma orders and their dependence on mean rate for different cell types are given. The same model of a renewal process with gamma-distributed intervals is used to model the measured power spectra and performs well. When the gamma order is proportional to mean rate, the power spectral density at low temporal frequencies is independent of discharge rate. Gamma order was proportional to mean rate for X cells but not for Y cells. Nonetheless, the power spectral densities of both cell types at low frequencies were approximately independent of discharge rate. Hence, noise in this band of frequencies can be considered additive. The consequences of departures from the renewal process and of the gamma order not being proportional to mean rate are considered. The significance of different rates of discharge for signaling is discussed.

The relative timing of a number of events during the development of the visual system has recently been suggested to be consistent across a number of mammalian species (Dreher & Robinson, 1988). Some conflicting reports, however, had suggested that the precocial guinea pig might represent an exception to the generalized scheme. A quantitative study was thus carried out on the development of the optic nerve and retina of the guinea pig. Consistent with the prediction of a stable relative time course of mammalian visual development, axons and growth cones were found in the optic stalk from the 24th postconceptional day (40% of the period from conception to eye opening —the cecal period), the peak number of axons was observed on the 32nd postconceptional day (56% of the cecal period), and the phase of rapid axonal loss extended to the 39th and 42nd postconceptional days (68–74% of the cecal period). The number of axons in the adult optic nerve (117,000) represented about 37% of the peak number of axons. Additional observations indicated that during development of the optic nerve the mean axonal diameter increased approximately threefold from 0.31 μm to 1.06 μm. As in other mammals studied so far, myelination was first noted after the period of rapid axonal loss and continued until in the adult 97% of axons were found to be myelinated. In the retina, the presence of pyknotic profiles in the ganglion cell layers extends throughout the periods of loss of the optic nerve axons. Finally, the presence of pyknotic profiles in the amacrine sublayer suggest that in the guinea pig, as in other mammalian species, there is a loss of displaced amacrine cells as well as ganglion cells from the ganglion cell layer.

We showed high-contrast, second-order motion stimuli to subjects whilst recording their horizontal eye movements. These stimuli were very poor at evoking optokinetic nystagmus. Smooth-pursuit eye movements and fixation were reduced by a masking band ±2.5 deg above and below an imaginary fixation point. First-order stimuli evoked vigorous optokinetic nystagmus (OKN) under identical conditions and also when matched for apparent contrast. These findings are discussed in terms of the site of detection of second-order motion.

The compound lateral eye of the adult horseshoe crab, Limulus polyphemus, views the world with approximately 1000 ommatidia. Their optical properties and orientation determine the eye's resolution, field of view, and light collecting ability. Optic axes of adjacent ommatidia diverge from 1–15 deg with an average value of 5.5 deg yielding an average resolution of 0.1 cycles/deg. Resolution is not uniform across the eye: along horizontal planes, it is maximal in the anterior region of the eye (0.22 cycle/deg) and minimal in the posterior region (0.07 cycle/deg); along vertical planes, it is maximal near or just below the horizon (0.23 cycle/deg) and minimal above the horizon (0.04 cycle/deg). Together the ommatidia of one eye view approximately 60% of the hemispheric world on one side of the body. There is little binocular overlap (<1% of total field). Ommatidial facets of up to 320 μm in diameter (among the largest known in the animal kingdom) make the eye a superb light collector. Limulus are known to use vision to find mates both day and night. Apparently, the optics of the lateral eye sample a large enough part of the world with sufficient resolution and light-collecting ability for the animal to succeed at this essential task.

We have investigated the effects of inactivation of localized sites in area 17 on the visual responses of cells in visuotopically corresponding regions of area 18. Experiments were performed on adult normal cats. The striate cortex was inactivated by the injection of nanoliters of lidocaine hydrochloride or of γ-aminobutyric acid (GABA) dissolved in a staining solution. Responses of the simple and complex cells of area 18 to optimally oriented light and dark bars moving in the two directions of motion were recorded before, during, and after the drug injection. Two main effects are described.

First, for a substantial number of cells, the drug injection provoked an overall reduction of the cell's visual responses. This nonspecific effect largely predominated in the complex cell family (76% of the units affected). This effect is consistent with the presence of long-range excitatory connections in the visual cortex.

Second, the inactivation of area 17 could affect specific receptive-field properties of cells in area 18. The main specific effect was a loss of direction selectivity of a number of cells in area 18, mainly in the simple family (more than 53% of the units affected). The change in direction selectivity comes either from a disinhibitory effect in the nonpreferred direction or from a reduction of response in the preferred direction. It is proposed that the disinhibitory effects were mediated by inhibitory interneurones within area 18. In a very few cases, the change of directional preference was associated with a modification of the cell's response profile.

These results showed that the signals from area 17 are necessary to drive a number of units in area 18, and that area 17 can contribute to, or at least modulate, the receptive-field properties of a large number of cells in the parastriate area.

Deactivation of light-activated squid rhodopsin was studied in vitro using GTPγS binding by G-protein as a direct measure of rhodopsin activity. Deactivation was inhibited by dilution of the retinal suspension or by removal of soluble components. Deactivation could be restored by addition of soluble material to washed membranes. These results indicate that the deactivation is not due entirely to a conformational transition within rhodopsin itself, but depends on the interaction with other molecules. The possibility that phosphorylation is involved in the deactivation was studied. Deactivation occurred in the presence and absence of added ATP. Deactivation also occurred in the presence of kinase inhibitors and after addition of apyrase, which reduced residual ATP levels to below 1μM. These results indicate that light-induced phosphorylation is not required for deactivation of squid rhodopsin. In this regard deactivation of squid rhodopsin is different from that of vertebrate rhodopsin, which requires phosphorylation.

The morphology of retinal ganglion cells within the central retina during formation of the fovea was examined in retinal explants with horseradish-peroxidase histochemistry. A foveal depression was first apparent in retinal wholemounts at embryonic day 112 (El 12; gestational term is approximately 165 days). At earlier fetal ages, the site of the future fovea was identified by several criteria that included peak density of ganglion cells, lack of blood vessels in the inner retinal layers, arcuate fiber bundles, and the absence of rod outer segments in the photoreceptor layer. Prior to E112, the terminal dendritic arbor of retinal ganglion cells within the central retina extended into the inner plexiform layer and were located directly beneath their somas of origin or at most were slightly displaced from it. For example, at E90 the mean horizontal displacement of the geometric center of the dendritic arbor from the somas of cells within 600 μm of the estimated center of the future fovea was 4.1 μm (S.D. 2.7, range 1.0-10.0, n = 97). Following formation of the foveal depression the dendritic arbors of cells were significantly displaced from their somas. For example, at E138 the mean displacement was 41.2 μm (S.D. 12.2, range 12.0-56.0, n = 97). The displacement of the dendritic arbor which occurred during this period was not accounted for by areal growth of the dendritic arbor, the somas, or the retina, but was produced by the lengthening of the primary dendritic trunk. Moreover, no significant displacement was observed within the remaining 1.5–6.5 mm of the central retina. These observations provide evidence supporting early speculations that the formation of the foveal pit occurs, in part, by the radial migration of ganglion cells from the center of the fovea during its formation. Our analyses suggest that this migration occurs by the lengthening of the primary dendrite presumably by the addition of membrane. This migration is in a direction opposite to the inward movement of photoreceptors that occurs during late fetal and early postnatal periods (Packer et al., 1990, Journal of Comparative Neurology 298, 472–493).

The reports of rod-dominated psychophysical spectral sensitivity from the deprived eye of monocularly lid-sutured (MD) monkeys are intriguing but difficult to reconcile with the absence of any reported deprivation effects in retina. As most studies of MD retina have been from cat, we have examined psychophysically the increment threshold spectral sensitivity of MD cats using both reaction time and simultaneous two-choice behavioral procedures. Although the deprived eyes exhibited an absolute increment threshold sensitivity deficit, both rod and cone spectral sensitivity functions were obtained on large white backgrounds. This normal transition from rod to cone vision, as background luminance increased, was also found in threshold vs. intensity functions. Using their deprived eye, some cats exhibited a rod spectral sensitivity function when a smaller, normally photopic, background was used providing some support for a hypothesis that the rod-dominated spectral sensitivity observed in monkey may represent detection of scattered stimulus light. Alternatively monocular deprivation may reveal a rod-dominated mechanism which exists in monkey but not in cat.