A mathematical model is presented that obeys a strong form of Weber's law – over a range of adapting and stimulus intensities, equal contrast stimuli evoke identical responses. To account for the strong Weber's law, the adaptive stage in the proposed model employs a “delayed” reverse reaction along with a power-law input. It is suggested that this Weber's law mechanism is responsible for a slow, voltage-uncorrelated component of adaptation in the vertebrate photoreceptor. A plausible biochemical mechanism is the G-protein cycle with phosphorylation of photoactivated photopigment (and binding of arrestin to the phosphorylated photopigment) as the adaptive process. In an Appendix, features of the general model and implications of a specific biochemical model are examined by computer simulation.

The pattern of dendritic stratification of retinal ganglion cells in the fetal monkey (Macaca mulatta) was examined using horseradish peroxidase and retinal explants. Ganglion cells in the rhesus monkey are born between embryonic day (E) 30–70 (La Vail et al., 1983). At E60, E67, and E68, approximately 50% of all ganglion cells within the central 3.0 mm of the retina had dendritic arbors that were unistratified within the inner plexiform layer (IPL), while the remaining 50% had bistratified arbors. Unistratified cells had relatively flat arbors that ramified within a restricted portion of the IPL. In contrast, bistratified cells had one portion of the arbor that branched in the inner half of the IPL and a second portion that branched in the outer half of the IPL. Relatively few bistratified cells were encountered in the central 1.0 mm of the retina but were more numerous with increasing eccentricity. At E81, E90, and E110, the dendritic arbors of ganglion cells increased in both area and complexity, but occupied a relatively small percentage of the total depth of the IPL. The bistratified cells encountered at these fetal ages were typically located in the far retinal periphery. Between E125-E140, the dendritic arbors of individual ganglion cells increased in area and depth to occupy a greater proportion of the total IPL than at earlier fetal ages.

These observations suggest that ganglion cells in the macaque undergo at least three stages of dendritic stratification: (1) an initial period of dendritic growth during which the cells have either unistratified or bistratified dendritic arbors; (2) a loss of the majority of bistratified cells through cell death or remodeling of the arbor; and (3) growth or expansion of the arbor to occupy a greater percentage of the total depth of the IPL. The first two stages are similar to recent observations in the fetal cat (Maslim & Stone, 1988) with the exception that dendritic development in the primate lacks an initial diffuse ingrowth to the IPL. Additionally, primate ganglion cells undergo a third stage of dendritic growth in late fetal development during which the arbor occupies a greater proportion of the depth of the IPL.

Light-microscopic immunocytochemistry was used to study serotonin (5HT)-containing retinal cells in the lamprey (Lampetra fluviatilis). Observations of sections and flatmounted retinas enabled us to distinguish four principal types of 5HT-immunoreactive neurons, on the basis of the localization of their somata and the arrangement of their processes in the inner plexiform layer, (IPL). Type 1 cell bodies (9 μm mean diameter) were numerous and were found in the innermost row of the inner nuclear layer (INL). They sent their processes into a dense plexus in sublamina a of the IPL. Type 2 cell bodies (12 μm mean diameter) were observed near the inner limiting membrane, their processes forming a plexus in sublamina b of the IPL. Most of the type 3 cells were bistratified, their cell bodies (similar in dimension to type 1) were located in the INL and their dendrites projected to both plexuses. Type 4 cell bodies (15 μm mean diameter) were observed in the middle of the IPL and could be compared with the interstitial described elsewhere. Their processes probably ended in the 5HT plexus of sublamina b but because of their sinuous course in the IPL, we could not affirm this fact. Most of 5HT immunoreactive cells were thought to be amacrine cells, but the presence of some thin processes emerging either from the soma or the primary dendrite, principally in type 1 and 2 cells, raises the possibility that some ganglion cells could be 5HT immunoreactive. The organization of the 5HT processes into two plexuses located in sublaminae a and b of the IPL resemble the functional ON and OFF pathway seen in the other vertebrates.

The phenomenon of apparent motion can arise when two spatially separated visual tokens are presented in temporal sequence. If tokens at opposite corners of a hypothetical square are presented simultaneously followed by simultaneous presentation of tokens at the remaining two corners, an apparent motion percept may occur along either the vertical or horizontal axis. The display is perceptually metastable since most observers will perceive motion along only one axis at a time. The metastable display, however, produces anisotropic results, in that with central fixation, vertical motion is seen more frequently than horizontal motion. The ratio of the vertical to horizontal length of the sides of a rectangle needed to achieve equal frequencies of motion judgments along the respective axes falls in the range of 1.18–1.92 for different observers in our experiments. It appears that signal transmission across the vertical midline is a major determinant of the vertical bias, since the anisotropic effects disappear when the fixation point is sufficiently offset along the horizontal meridian so as to cause a fully homonymous representation of all of the metastable tokens. One of the factors may be signal degradation or delay in callosal transmission which could reduce the strength of the motion signal along the horizontal axis. In addition, there appears to be a strip along the vertical midline with a width of 30–50 min are within which reduced levels of anisotropy are found. The possibility that this strip is a consequence of a zone of naso-temporal overlap in the projection of the retina to the brain along the vertical meridian will be discussed.

A circadian clock modulates the structure and function of the lateral eyes of Limulus polyphemus, greatly increasing their sensitivity at night. During the mating season, male Limulus are visually attracted both day and night to females and objects that resemble females. This paper asks how well Limulus can see day and night, and whether the circadian changes in retinal sensitivity might influence the ability of these animals to find mates. We recorded the visual behavior of male and female horseshoe crabs in the vicinity of an object – a cement hemisphere (29.5 cm diameter) similar in size and shape to a female horseshoe crab – placed in a mating area near Mashnee Dike, Bourne, Massachusetts. Males oriented toward this target from an average distance of 0.94 m during the day and 0.88 m at night; and females appeared to avoid the target. We conclude that males can see potential mates at night almost as well as they can during the day. Apparently the circadian changes in the retina help compensate for the daily changes in illumination in the animal's normal environment. This study provides the first evidence for a role of visual circadian rhythms in an animal's natural behavior.

This study was designed to monitor the development of inhibitory interactions elicited in the cat visual system by oriented visual stimuli. Steady-state visual-evoked potentials (VEPs) were recorded from the scalp of 11 behaving and alert kittens while they viewed contrast-reversed sinusoidal gratings. In adult cats, the form of VEP contrast-response curves (the amplitude of second harmonic modulation as a function of stimulus contrast) was modified by superimposing a mask grating on the test. Parallel masks displaced the curves to a higher contrast region (probably via contrast gain-control mechanisms), increasing contrast threshold without affecting the slope of the curve. Orthogonal gratings, on the other hand, decrease the slope of the curve without affecting threshold (so called cross-orientation inhibition: Morrone et al., 1981). These effects are similar to those previously reported in human VEPs (Morrone & Burr, 1986; Burr & Morrone, 1987) and single cortical cat cells (Morrone et al., 1982). For young kittens of 20 days, the orthogonal mask had no effect whatsoever on the response curves, and the effect of the parallel mask was much less than for adult cats. At about 40 days, the orthogonal mask began to attenuate responses multiplicatively, and by 50 days the amount of multiplicative attenuation had reached adult levels. The effect of the parallel mask (as indicated by the increase in threshold elevation) increased gradually from 20–50 days. The results are consistent with the existence of at least two types of inhibition in cat visual neurones that develop at different rates.

The responses of simple cells were recorded from the visual cortex of cats, as a function of the position and contrast of counterphase and drifting grating patterns, to assess whether direction selectivity can be accounted for on the basis of linear summation. The expected responses to a counterphase grating, given a strictly linear model, would be the sum of the responses to the two drifting components. The measured responses were not consistent with the linear prediction. For example, nearly all cells showed two positions where the responses approached zero (i.e. two “null phase positions”); this was true, even for the most direction selective cells. However, the measured responses were consistent with the hypothesis that direction selectivity is a consequence of the linear spatiotemporal receptive-field structure, coupled with the nonlinearities revealed by the contrast-response function: contrast gain control, halfwave rectification, and expansive exponent. When arranged in a particular sequence, each of these linear and nonlinear mechanisms performs a useful function in a general model of simple cells. The linear spatiotemporal receptive field initiates stimulus selectivity (for direction, orientation, spatial frequency, etc.). The expansive response exponent enhances selectivity. The contrast-set gain control maintains selectivity (over a wide range of contrasts, in spite of the limited dynamic response range and steep slope of the contrast-response function). Rectification conserves metabolic energy.

Two physiologically distinct, HRP-marked turtle retinal ganglion cells were examined for their morphology, GABAergic, glycinergic, and bipolar cell synaptic inputs, using electron-microscopic autoradiography and postembedding immunocytochemistry. One cell was a color-opponent, transient ON/OFF ganglion cell. Its center response to red was a sustained hyperpolarization, and its center response to green was a depolarization with increased spiking at onset. The HRP-injected cell most resembled G6, from previous Golgi-impregnation studies (Kolb, 1982; Kolb et al., 1988). It was a narrow-field bistratified cell, whose two broad dendritic strata peaked at approximately levels L20–25 (sublamina a) and L60 (sublamina b) of the inner plexiform layer. Bipolar cell synapses onto G6 were found evenly distributed between its distal and proximal dendritic strata, spanning L20–75. These inputs probably originated from several different bipolar cells, reflecting the complexity of the center response. GABAergic inputs were found onto both the distal and proximal strata, from near L20–L85. Only a few glycinergic inputs, confined to dendrites at L50–70, were observed.

A second ganglion cell type that we physiologically characterized and HRP-injected had sustained ON-center, sustained OFF-surround responses. Two examples were studied; both were bistratified in sublamina b, near L60–70 and L85–100, with branches up to near L40. They resembled G10, from previous Golgi-impregnation studies (Kolb, 1982; Kolb et al., 1988). One cell was partially reconstructed to look at the distributions of GABAergic and glycinergic amacrine cell, and bipolar cell inputs. Although synapses from bipolar cells were equally divided between the two major dendritic strata of G10, the inputs to the distal stratum were close to the soma, and the inputs to the more proximal stratum were on the peripheral dendrites. This arrangement may reflect input from two distinct types of ON-bipolar cell. GABAergic and glycinergic inputs to G10 costratified to both strata and to the distal branches; but where glycinergic inputs were found distributed throughout the arbor, GABAergic inputs appeared to be confined to peripheral dendrites. We hypothesize on the neural elements involved and the circuitry that may underlie the physiologically recorded receptive fields of these two very different ganglion cell types in the turtle retina.

The center of the receptive field of some retinal ganglion cells exhibits an interesting fine structure: the relative amplitudes of responses to onset and responses to offset of a small spot of light varies systematically as the spot is positioned at various places within the center. Although this pattern may appear complicated, a simple model can account for it in detail. The model postulates that the ganglion cell receives input from separate ON and OFF processes within the center of its receptive field. These processes have the form of Gaussian functions and are laterally displaced from each other. These central ON and OFF input processes are not associated with the additional antagonistic surround of the receptive field.

The model is examined for various parameters of the input processes. The observed systematic variation in the ratio of offset to onset responses is predicted when the two processes are of nearly equal width (standard deviation of the Gaussians). Receptive fields made of more than two Gaussians produce various patterns, depending on the relative standard deviations of the Gaussians. Oblong fields, reminiscent of those found in visual cortex, may be generated from a relatively small number of circularly symmetric Gaussian processes.

Behavioral and electrophysiological measures were used to elucidate the retinal modulation of oculomotor control in the turtle. Eye movements were recorded following intravitreal applications of 2-amino-4-phosphonobutyrate (APB) and the GABA antagonists picrotoxin and bicuculline. Visual responses of single basal optic nucleus (BON) neurons of the accessory optic system were studied in parallel experiments. The effectiveness of APB, a glutamate analog thought to act selectively on the retinal ON pathway, was assessed independently by recording electroretinograms or ganglion cell activity.

Injections of APB into the turtle's eye reduced or blocked the injected eye's ability to drive horizontal optokinetic nystagmus, as also observed in rabbit and cat (Knapp et al., 1988; Yucel et al., 1989). Single-unit recordings from the BON during APB superfusion (50–200 μM APB) of the contralateral retina demonstrated that these cells, which are direction-sensitive and respond to the offset of light flashes, have their responses to moving stimuli blocked by APB.

During the APB effect, GABA antagonists were applied to the same eye. Although moderate doses of APB were sufficient to block optokinetic or BON light responses, the addition of GABA blockers still elicited a spontaneous temporal-to-nasal nystagmus (Ariel, 1989) or visually responsive yet direction-insensitive responses from BON cells (Schuerger et al., 1990). These results are discussed in terms of the retinal output to pathways involved in oculomotor control of optokinetic nystagmus.

We report on the existence of lagged Y (YL) cells in the A laminae of the cat lateral geniculate nucleus (LGN) and on criteria for identifying them using visual and electrical stimulation. Like the lagged X (XL) cells described previously (Mastronarde, 1987a; Humphrey & Weller, 1988a), YL cells responded to a spot stimulus with an initial dip in firing and a delayed latency to discharge after spot onset, and an anomalously prolonged firing after spot offset. However, the cells received excitatory input from retinal Y rather than X afferents, and showed nonlinear spatial summation and other Y-like receptive-field properties. Three YL cells tested for antidromic activation from visual cortex were found to be relay cells, with long conduction latencies similar to those of XL cells.

Simultaneous recordings of a YL cell and its retinal Y afferents show striking parallels between lagged X and Y cells in retinogeniculate functional connectivity, and suggest that the YL-cell response profile reflects inhibitory processes occurring within the LGN. The YL cells comprised -5% of Y cells and -1% of all cells in the A laminae. Although infrequently encountered in the LGN, they may be roughly as numerous as Y cells in the retina, and hence could fulfill an important role in vision.

A visual-evoked-potential (VEP) masking technique was used to assess the effects of short- and long-term monocular deprivation on the development of visual inhibitory interactions in kittens. VEP contrast-response curves were recorded in response to contrast-reversed sinusoidal gratings, both with and without superimposed high-contrast masks. The contrast-response curves measured from the nondeprived eye were similar to those of normal cats: with no mask VEP amplitudes increase with contrast up to saturation at about 10% contrast; parallel masks shift the curves to the right, decreasing thresholds; and orthogonal masks decrease the slope of the contrast-response curves without affecting thresholds. After monocular deprivation (either brief or extensive), the contrast-response curves without mask did not show the typical response saturation, and neither parallel nor orthogonal mask had any effect on the contrast-response curves. The masking effects did not return after 100 days of normal vision, although contrast sensitivity and acuity recovered to about half of the normal levels during that period. The results indicate that the inhibitory intracortical circuitry that mediates the orientation-dependent masking effects are highly vulnerable to visual experience.

The effect of background illumination on horizontal cell receptive-field size and dye coupling was investigated in isolated superfused goldfish retinas. Background illumination reduced both horizontal cell receptive-field size and dye coupling. The effect of light on horizontal cell receptive-field size was mimicked by treating the retina with 20 μM dopamine. To test the hypothesis that the effects of light were due to endogenous dopamine release, the effect of light was studied in goldfish retinas in which dopaminergic interplexiform cells were lesioned using 6-hydroxydopamine treatment. In lesioned retinas, background illumination reduced both horizontal cell receptive-field size and dye coupling. Furthermore, the effect of background illumination on unlesioned animals could not be blocked by prior treatment with the D1 dopamine receptor antagonist SCH-23390. These results suggest that, in goldfish retina, dopamine release is not the only mechanism by which horizontal cell receptive-field size could be reduced by light.

The representation of the visual field in the part of area 17 containing neurons that project axons across the corpus callosum to the contralateral hemisphere was defined in the cat. Of 1424 sites sampled along 77 electrode tracks, 768 proved to be in the callosal sending zone, which was identified by retrograde transport of horseradish peroxidase that had been deposited in the opposite hemisphere. The results show that the callosal sending zone has a fairly constant width of between 3 and 4 mm at most levels in area 17. However, the representation of the contralateral field at the different elevations of the visual field is not equal in this zone. The zone represents positions within 4 deg of the midline at the 0-deg horizontal meridian, and positions out to 15-deg azimuths in the upper hemifield and out to positions of 25-deg azimuth in the lower hemifield. The shape of the representation is approximately mirror-symmetric about the horizontal meridian, although there is a greater extent in the lower hemifield, which can be accounted for by the greater range of elevations (>60 deg) represented there compared with the upper hemifield (-40 deg). The representation in the sending zone of one hemisphere matches that present in the area 17/18 transition zone, which receives the bulk of transcallosal projections, in the opposite hemisphere. The observations on the sending zone show that callosal connections of area 17 are concerned with a vertical hour-glass-shaped region of the visual field centered on the midline. The observations suggest that in addition to interactions between neurons concerned with positions immediately adjacent to the midline, there are positions, especially high and low in the visual field, where interactions can occur between neurons that have receptive fields displaced some distance from the midline.

In the arthropod medulla, which is the second ganglion on the afferent visual pathway, a column of about 40 cells represents each point in space (i.e. compound eye facet). Some stages of visual processing underlying the responses of one class of cells in the locust medulla have been identified. These transient cells give very similar responses to intensity increments and decrements, and also to pulses and steps; there is no spontaneous activity and a stimulus causes one or two spikes to fire at fixed latencies. Movement, however, produces a prolonged spike discharge by successive excitation of subunits within the receptive field.

One of the main features of the transient cells' responses is a self-inhibition which attenuates responses to successive stimuli at one point. This inhibition is restricted to the outputs of single receptor (rhabdom), it decays after about 100 ms, and is polarity sensitive so that stimuli of one polarity (e.g. dimming) do not inhibit responses to stimuli of the opposite polarity (e.g. brightening). The inhibition effectively alters the contrast threshold of the cells, because after adaptation with stimuli of one contrast, a modest (<20%) increase in contrast is sufficient to elicit an unadapted response. Transient cells are not directionally selective and there are no local spatio-temporal interactions of the kind necessary for directional selectivity. But, by analogy with the directional veto in directionally selective cells in the rabbit retina (Barlow & Levick, 1965), self-inhibition is suggested as a mechanism of non-directional motion detection. After the inhibition, there is some spatial pooling of signals which is followed by rectification. The transient cells' spiking outputs could abstract a refined subset of visual information which may encode the presence, but not the direction, amplitude, or polarity of moving object borders.

Several neurophysiological studies have shown that the visual cerebral cortex of macaque monkeys performing delayed match-to-sample tasks contains individual neurons whose levels of activity depend on the sample the animal is required to remember. Haenny et al. (1988) reported that the activity of neurons in area V4 of monkeys performing an orientation matching task depends on the orientation for which the animal is searching. It was proposed that these neurons contribute to a representation of the orientation being sought.

We have further characterized these neurons by recording visual responses from individual neurons during multiple behavioral tasks. Animals were trained to perform an orientation match-to-sample task using either a visual or a tactile orientation sample. In a set of 89 neurons examined using both types of sample, 25% showed statistically significant effects of sample orientation regardless of whether the sample was visual or tactile. Most of these preferred the same sample orientation in both conditions. These results allow us to specify the nature of the information signaled by these neurons more precisely than has previously been possible.

For 193 units tested using one of the matching tasks, responses were also recorded while the animal performed a simple fixation task. In this task the animal was not required to attend to the visual stimuli that were presented. A few neurons that were responsive during the matching task were silent during fixation, but a comparable number was much more responsive during fixation. Across the whole population there was no systematic change in either responsivity or selectivity for orientation under the two conditions.