Theta ganglion cell type of cat retina.

We define a new bistratified ganglion cell type of cat retina using intracellular staining in vitro. The theta cell has a small soma, slender axon, and delicate, highly branched dendritic arbor. Dendritic fields are intermediate in size among cat ganglion cells, with diameters typically two to three times those of beta cells. Fields increase in size with distance from the area centralis, ranging in diameter from 70 to 150 microns centrally to a maximum of 700 microns in the periphery. Theta cells have markedly smaller dendritic fields within the nasal visual streak than above or below it and smaller fields nasally than temporally. Dendritic arbors are narrowly bistratified. The outer arbor lies in the lower part of sublamina a (OFF sublayer) of the inner plexiform layer where it costratifies with the dendrites of OFF alpha cells. The inner arbor occupies the upper part of sublamina b (ON sublayer), where it costratifies with ON alpha dendrites. The outer and inner arbors are composed of many relatively short segments and are densely interconnected by branches that traverse the a/b sublaminar border. Experiments combining retrograde labeling with intracellular staining indicate that theta cells project to the superior colliculus and to two components of the dorsal lateral geniculate nucleus (the C laminae and medial interlaminar nucleus). Theta cells project contralaterally from the nasal retina and ipsilaterally from the temporal retina. They apparently correspond to a sluggish transient or phasic W-cell with an ON-OFF receptive field center.

The Eta ganglion cell type of cat retina.

We define a morphologic type of ganglion cell in cat retina by using intracellular staining in vitro. The eta cell has a small soma, slender axon, and delicate, highly branched dendritic arbor. Dendritic fields are intermediate in size among cat ganglion cells, with diameters typically two to three times those of beta cells. Fields increase in size as a function of distance from the area centralis, ranging in diameter from 90 microm to 200 microm centrally to a maximum of 600 microm in the periphery. This increase is unusually radially symmetric. By contrast with other cat ganglion cell types, eta cells do not have markedly smaller dendritic fields within the visual streak than above or below it nor much smaller fields nasally than temporally. Dendrites ramify broadly throughout sublamina a (OFF sublayer) of the inner plexiform layer. They arborize most densely in S2, where they costratify with dendrites of OFF alpha cells. There is apparently no matching ON variety of eta cell. Experiments combining retrograde labeling with intracellular staining indicate that eta cells project to the superior colliculus and to two components of the dorsal lateral geniculate nucleus (the C laminae and medial interlaminar nucleus). Eta cells apparently project contralaterally from the nasal retina and ipsilaterally from the temporal retina. The morphology and projection patterns of the eta cell suggest that its physiologic counterpart is a type of sluggish or W-cell with an OFF center, an ON surround, and possibly a transient light response.

The zeta cell: a new ganglion cell type in cat retina.

We define a new morphological type of ganglion cell in cat retina by using intracellular staining in vitro. The zeta cell has a small soma, slender axon, and compact, tufted, unistratified dendritic arbor. Dendritic fields were intermediate in size among cat ganglion cells, typically twice the diameter of beta cell fields. They were smallest in the nasal visual streak (<280 microm diameter), especially near the area centralis (60-150 microm diameter), and largest in the nonstreak periphery (maximum diameter 570 microm). Fields sizes were symmetric about the nasotemporal raphe except near the visual streak, where nasal fields were smaller than temporal ones. Zeta-cell dendrites ramified near the boundary between sublaminae a and b (OFF and ON sublayers) of the inner plexiform layer, occupying the narrow gap separating the dendrites of ON and OFF alpha cells. There was no evidence for separate ON and OFF types of zeta cell. Retrograde labeling studies revealed that both nasally and temporally located zeta cells project to the contralateral superior colliculus, whereas few project to the ipsilateral colliculus or to any subdivision of the dorsal lateral geniculate nucleus. The zeta cell's morphology and projection patterns suggest that it corresponds to the ON-OFF phasic W-cell (also known as the local edge detector) of physiological studies. Zeta cells have particularly small dendritic fields in the visual streak, presumably because they are disproportionately represented in the streak in comparison with other ganglion cell types. These conditions are consistent with optimal spatial resolution along the retinal projection of the visual horizon rather than principally at the center of gaze. Strong commonalities with similar ganglion cell types in ferret, rabbit, and monkey suggest that "zeta-like" cells may be a universal feature of the mammalian retina.

Distribution and coverage of beta cells in the cat retina.

We have reexamined the retinal distribution and dendritic field dimensions of beta cells in the cat retina. Beta cells were labeled by retrograde transport from the A-layers of the lateral geniculate nucleus and distinguished from alpha cells on the basis of soma size. Dendritic fields of beta cells were visualized by intracellular staining in vitro. The fraction of cat ganglion cells that were beta cells varied with retinal location. Except near the area centralis, beta cells represented about half of all ganglion cells in the nasal hemiretina. They contributed as heavily as the other major ganglion cell classes to the nasal visual streak. In and near the area centralis and in the temporal retina, beta cells represented about two-thirds of all ganglion cells. The areas of beta cell dendritic fields were reciprocally related to beta cell density. For example, they were 3-fold smaller within the visual streak than at matched eccentricities outside it. For many cells, we could estimate both local beta cell density and dendritic field area. Coverage factor (dendritic field area x local density) remained constant at about 4 despite 100-fold variations in beta cell density, and was independent of eccentricity, nasotemporal location, or position relative to the visual streak. Analysis in terms of sampling theory suggests that the beta cell array is matched to X-cell spatial resolution so as to optimize acuity. The beta cell distribution and its systematic reflection in dendritic architecture predict acuity levels that apparently correlate well with actual visual performance across the cat's visual field.

Organization of the striate-recipient zone of the cats lateralis posterior-pulvinar complex and its relations with the geniculostriate system.

The extrageniculate visual thalamus of the cat is divisible into several major subdivisions but only one receives dense fiber projections from the striate cortex. In the present study, modern axon transport techniques and acetylcholinesterase histochemistry were used to examine the internal organization of this striate-recipient zone and some of its afferent and efferent connections. A detailed study of the corticothalamic fiber projections of the striate cortex clarified the topographic organization and boundaries of the striate-recipient zone. The nature and course of "projection lines" within the zone were defined and the subdivision was shown to correspond closely to a region of relatively weak acetylcholinesterase staining. Corticothalamic projections from two regions of the extrastriate visual cortex, area 19 and the medial division of the Clare-Bishop complex, converge with those from area 17 in the striate-recipient zone, but these extrastriate areas have more widespread projections to the extrageniculate thalamus than does the striate cortex. A weak subcortical projection to the striate-recipient zone was demonstrated, apparently originating in the superior colliculus. Retrograde tracing experiments indicated that the corticothalamic inputs of the striate-recipient zone are precisely reciprocal by thalamocortical projections. Extrageniculate thalamic projections to area 17 arise exclusively from this thalamic subdivision and are highly topographically ordered. The striate-recipient zone projects massively and apparently retinotopically to area 19 and to the medial division of the Clarc-Bishop area, as well as area 21(a), but these extrastriate areas receive additional afferents from other subdivisions of the extrageniculate thalamus. These findings appear to rule out a "non-specific" functional role for the striate-recipient zone. In its topographic organization, its reciprocal connections with areas of the visual cortex, and its sheer volume, the zone seems comparable to the dorsal lateral geniculate nucleus and may be fairly considered a satellite of the geniculocortical system. Certain of the zone's organizational and connectional features may be clues to its functional role and its possible homologues in other mammalian forms.

Evidence for intrinsic expression of enkephalin-like immunoreactivity and opioid binding sites in cat superior colliculus.

We have investigated the cellular localization of opioid peptides and binding sites in the cat's superior colliculus by testing the effects of retinal deafferentation and intracollicular excitotoxin lesions on patterns of enkephalin-like immunostaining and opiate receptor ligand binding. In normal cats, enkephalin-like immunoreactivity marks a thin tier in the most dorsal stratum griseum superficiale, small neurons of the stratum griseum superficiale, and patches of fibers in the intermediate and deeper gray layers. Eliminating crossed retinotectal afferents by contralateral eye enucleation had little immediate effect on this pattern, although chronic eye enucleation from birth did reduce immunoreactivity in the superficial layers. By contrast, fiber-sparing destruction of collicular neurons by the excitotoxins N-methyl-D-aspartate and ibotenic acid virtually eliminated enkephalin-like immunoreactivity in the neuropil of the upper stratum griseum superficiale, presumably by killing enkephalinergic cells of the superficial layers. Such lesions did not eliminate the patches of enkephalin-like immunoreactivity in the deeper layers. In normal cats, opiate receptor ligand binding is dense in the stratum griseum superficiale, particularly in its upper tier, and moderately dense in the intermediate gray layer. Contralateral eye removal had no detectable effect on the binding pattern, but excitotoxin lesions of the colliculus dramatically reduced binding in both superficial and deep layers. Some ligand binding, including part of that in the upper stratum griseum superficiale, apparently survived such lesions. Similar effects were observed in the lateral geniculate nucleus: enucleation produced no change in binding, whereas excitotoxin lesions greatly reduced specific opiate binding. We conclude that in the superficial collicular layers, both enkephalin-like opioid peptides and their membrane receptors are largely expressed by neurons of intrinsic collicular origin. The close correspondence between the location of these intrinsic opioid elements and the tier of retinal afferents terminating in the upper stratum griseum superficiale further suggests that opiatergic interneurons may modulate retinotectal transmission postsynaptically.

A method for reliable and permanent intracellular staining of retinal ganglion cells.

We have developed a method for reliable, permanent, high-resolution intracellular staining of ganglion cells in mammalian retinas. Living ganglion cells in the isolated retina are impaled in vitro and injected intracellularly with both Lucifer Yellow (LY) and biocytin. After fixation and aggressive pretreatment of the retina with detergents, the LY is tagged immunohistochemically with biotin using a commercially available anti-LY antibody and a biotinylated secondary antibody. A conventional avidin-biotin procedure is then used to visualize both the biocytin and the biotinylated bridge antibody, yielding complete Golgi-like filling of the soma, dendrites and axon. Advantages of the method include the ease and speed of dye injection, the reliable recovery of stained cells, the large number of cells which can be stained in single retinas, and the high resolution and permanence of the stain, which permit prolonged examination and quantitative analysis.

Autoradiographic evidence for a projection from the pretectal nucleus of the optic tract to the dorsal lateral geniculate complex in the cat.

A pathway from the pretectal region to the dorsal division of the lateral geniculate body has been studied by autoradiography in adult cats following injection of tritium-labeled amino acids into the meso-diencephalic border zone. The findings suggest that the pretecto-geniculate connection arises in the ipsilateral nucleus of the optic tract (NOT) and terminates in the principle dorsal layers of the geniculate body (A and A1), in lamina C and most massively in the medial interlaminar nucleus. In the A layers and lamina C, the pretectal fibers from a relatively even matting with partial interruptions occurring at the interlaminar leaflets. The ventral C layers do not appear to receive a substantial pretectal input as they were only weakly labeled, and partly in a perforant fiber pattern, after injections confined to the pretectum. Topographic ordering of the projection was evident at least along the medial to lateral axis of the NOT, fibers from the medial part terminating caudally, and those from the lateral part rostrally, within the lateral geniculate complex. The laminar pattern of termination correlates closely with the distribution of retinal Y-cell input and acetylcholinesterase activity in the geniculate body but contrasts sharply with the pattern of termination of tecto-geniculate fibers. Of potential importance in considering the functional significance of the pretecto-geniculate pathway is the fact that the NOT has been implicated in the mechanism of optokinetic nystagmus and the fact that the pathway terminates within the layers of the lateral geniculate body known to provide the main geniculo-cortical input to layer IV of the striate cortex.

Convergence of retinal W-cell and corticotectal input to cells of the cat superior colliculus.

1. Conduction velocities of retinotectal W-cell afferents were estimated from differences among latencies of collicular unit responses to supramaximal stimulation of the contralateral optic disk (OD), optic chiasm (OX), and ipsilateral optic tract (OT). W-cell afferents driving collicular neurons had very slowly conducting axons, nearly all below 8 m/s (mean = 5.3 m/s). These match the conduction velocities of W-cell axons terminating in the uppermost superficial gray layer and triggering juxtazonal potentials (JZPs). Such slow conduction velocities are typical of W-cells belonging to the W2 subclass ("phasic W-cells"), but are slower than nearly all W1 cells ("tonic W-cells"). 2. Most W-driven cells were activated at latencies longer than expected for monosynaptic input from these W-cell afferents. However, comparable delays were observed among JZPs, which signal monosynaptic excitation of collicular neurons by W-cell terminals. This suggests that the delayed activation of W-driven cells reflects slowed conduction in the preterminal segments of W-cell afferents rather than polysynaptic transmission of W-cell signals through intermediary neurons in the brain stem or cortex. Thus monosynaptic inputs from retinal W2 cells appear to drive most neurons of the superficial collicular layers. 3. Convergence of retinotectal W-cell and corticotectal pathways was assessed by recording responses of W-driven collicular cells to intracortical stimulation of area 17. The great majority of W-driven collicular cells were activated by cortical stimulation (41/52; 79%), indicating that such convergence is widespread. 4. The population of corticotectal cells influencing W-driven collicular cells may differ from that mediating Hoffmann's Y-indirect pathway. W-driven collicular cells were activated from the striate cortex at longer latencies (mean = 6.3 ms) than cells driven by the Y-indirect pathway (mean = 2.5 ms). In addition, cortically activated W-driven cells were common throughout the superficial gray layer, whereas cells driven by the Y-indirect input were encountered only in the deepest part of the superficial gray and below. 5. W2 cells, apparently the dominant retinotectal cell type, nearly all project contralaterally and are tuned for slow stimulus velocities. Thus the binocularity of W-driven collicular cells and their sensitivity to moderately fast stimulus motion probably reflect the convergent cortical input described here.

Retinal W-cell input to the upper superficial gray layer of the cat's superior colliculus: a conduction-velocity analysis.

1. I have used several methods to estimate the conduction velocities of retinal afferents innervating the upper 50-100 micron of the stratum griseum superficiale (the upper SGS). The measurements were based on a unitary extracellular potential unique to this sublamina, which was first described by McIlwain (28). He termed it the juxtazonal potential (JZP), and showed that it results when a single spike invades the terminal arbor of a single retinal afferent to the upper SGS, triggering synchronous excitatory postsynaptic potentials in postsynaptic collicular cells. 2. Individual unitary JZPs were evoked at fixed latencies by weak shocks to the optic disk, chiasm, or tract. When the same JZP could be evoked in isolation from two stimulus sites, the conduction velocity of the axon triggering the JZP was estimated by dividing the conduction time between the stimulating electrodes (i.e., the "latency difference") into the distance separating these electrodes. This "latency-difference method" lacked general utility, however, since the same JZP could only rarely be evoked in isolation from two stimulus sites. 3. This limitation was circumvented by means of a collision method. When a stimulus that evoked a JZP in isolation was preceded by a sufficiently intense conditioning shock to a second, more central stimulus site, the conditioning stimulus caused the JZP to fail in an all-or-none fashion. It was assumed that when the JZP failed, the conditioning stimulus had exceeded the spike threshold of the axon mediating the JZP and that an antidromic action potential had collided with the orthodromic spike initiated at the peripheral stimulus site. Assessment of the critical interstimulus interval for producing such a collision, together with measurements of the axon's refractory period and the interelectrode conduction distance, permitted an estimate of the conduction velocity of the JZP-triggering axon. Conduction-velocity estimates generated in this way closely matched those based on the latency-difference technique when both methods could be applied. 4. Conduction velocities of 31 JZP-triggering axons analyzed by the collision method ranged from 2.9 to 6.8 m/s [4.6 +/- 1.0 (mean +/- SD)]. Comparable estimates were obtained for such axons by alternative methods based on the absolute latencies of electrically evoked JZPs or of the field potential to which they contribute. The conduction velocities of JZP-triggering axons fell within the range reported for retinal W-cells and entirely outside those of X- and Y-cells, confirming earlier evidence for W-cell input to the upper SGS (7, 15, 18, 28).(ABSTRACT TRUNCATED AT 400 WORDS)

Cat lateral suprasylvian cortex: Y-cell inputs and corticotectal projection.

Retinal Y-cells activate most cells in the deep layers of the cat's superior colliculus via an indirect pathway involving the occipital cortex. The lateral suprasylvian area seems to be an important source of visual input to the deep collicular strata but it is unclear whether Y-cell influences reach this extrastriate area and, hence, whether this area participates in the indirect Y-cell pathway. In this study, retinal influences on the posteromedial lateral suprasylvian area (PMLS) were studied in anesthetized cats. Responses to electrical stimulation of the optic disk (OD) and optic chiasm (OX) were recorded in single units in PMLS and in neurons of the dorsal lateral geniculate nucleus (LGNd) that were antidromically driven from PMLS. Virtually all PMLS cells (99%; 99/100) exhibited small differences (less than or equal to 0.8 ms) between OD- and OX-activation latency, indicating that they were driven by a pathway originating in rapidly conducting Y-cell axons. A small number of PMLS cells (17%; 20/118) had very short activation latencies (less than or equal to 3.2 ms from OX), comparable to those of cells in areas 17 and 18 receiving monosynaptic inputs from geniculate Y-cells. Further, LGNd cells with latency behaviors typical of Y-cells could be antidromically driven from PMLS, confirming that geniculate Y-cells project directly to PMLS. Most PMLS cells (83%; 98/118), though exhibiting small OD-OX latency differences, had absolute latencies too long to be attributed to direct inputs from geniculate Y-cells (3.3-8.5 ms from OX). Thus Y-cells in the LGNd influence most PMLS cells by way of a multisynaptic pathway. PMLS cells antidromically activated from the superior colliculus were driven only by this multisynaptic Y-cell input. Total conduction time from the retina through PMLS to the colliculus corresponds closely to the latency of the indirect Y-cell activation observed in the deep collicular layers. These results support the view that the lateral suprasylvian cortex constitutes an important source of visual input to the cat's deep collicular layers and, more generally, that the extrastriate visual cortex may figure prominently in the cortical control of gaze.

Retinotopic organization of the superior colliculus in relation to the retinal distribution of afferent ganglion cells.

Sensory representations in the brain exhibit topographic variations in magnification. These variations have been thought to reflect regional differences in the density of innervation at the sensory receptor surface. In the primate visual cortex, for example, local magnification factors have been reported to be proportional to the corresponding densities of retinal ganglion cells. We sought to learn whether this principle also operates in a second major retinofugal pathway--the projection to the superior colliculus. In cats, we first used retrograde transport to determine the retinal distributions of the ganglion cells that project to the colliculus. Then, we compared the numbers of colliculopetal ganglion cells in selected retinal sectors to the areas of the corresponding collicular representations. Collicular areal magnification was not simply proportional to the density of afferent ganglion cells, being instead at least 5-fold greater than expected in the representation of the central visual field. These data imply that incoming retinal afferents are more widely spaced in the central regions of the tectal map than in the map's periphery. Such variations in afferent density appear to play as large a role as the distribution of ganglion cells in determining the metric of the collicular map.

On the distribution of gamma cells in the cat retina.

Ganglion cells of the cat retina that are neither alpha nor beta cells are often lumped for convenience into a single anatomical group--the gamma cells (Boycott & Wässle, 1974; Stone, 1983; Wässle & Boycott, 1991). Defined in this way, gamma cells are the morphological counterpart to the physiological W-cell class, which includes all ganglion cells that are neither Y (alpha) nor X (beta) cells. We have estimated the retinal distribution of gamma cells by using retrograde transport to label ganglion cells innervating the superior colliculus and by assuming that these included virtually all gamma cells and no beta cells. We excluded labeled alpha cells on the basis of soma size. Our data suggest that gamma cells represent just under half of the ganglion cells in most of the nasal retina, but only about a third of those in the area centralis and temporal retina. Gamma cells do not appear to be more highly concentrated in the nasal visual streak than are other ganglion cells. In the temporal retina, gamma cells with crossed projections to the brain are apparently at least twice as common as those with uncrossed projections.

A tecto-rotundo-telencephalic pathway in the rattlesnake: evidence for a forebrain representation of the infrared sense.

Rattlesnakes possess a sensory system specialized for the detection of infrared (IR) radiation. IR signals ascend as far as the optic tectum, where they generate a spatiotopic map. It is unknown if such signals reach the forebrain, but the existence of prominent tectothalamic pathways in other vertebrates makes this a distinct possibility. In nonmammalian forms, the major target of ascending tectal visual signals is nucleus rotundus, a thalamic nucleus that projects in turn to the subpallial telencephalon. We sought to determine whether a tecto-rotundo-telencephalic system exists in rattlesnakes and, if so, whether it carries IR as well as visual information. We have identified a thalamic nucleus in the rattlesnake Crotalus viridis that matches the n. rotundus of other reptiles in its topographic location, cytoarchitecture, and connections. Using anterograde and retrograde transport of HRP, we have demonstrated a strong ipsilateral and weaker contralateral tectorotundal projection. Tectorotundal cells lay primarily in the deeper tectal layers, which receive input from the IR system, but also in the superficial, visual layers. In n. rotundus, single units recorded extracellularly invariably responded to visual stimuli, but many were also sensitive to unimodal IR stimuli. IR and visual receptive fields were very large and often bilateral. Some rotundal units appeared sensitive to substrate vibration. Most habituated rapidly. Nucleus rotundus was found to project to a sector of the ipsilateral anterior dorsal ventricular ridge (ADVR) of the telencephalon. Single units in this region of the ADVR resembled those in rotundus, responding to visual, IR, and/or vibrational stimuli and possessing large, often bilateral receptive fields. These findings demonstrate the existence of a tecto-rotundo-telencephalic pathway in rattlesnakes and suggest that this system conveys IR as well as visual information to the forebrain. Ascending tectofugal pathways have been implicated in the discrimination of form. Thus, pattern recognition may have to be added to orientation as a proper function of the IR system of pit vipers.

Visual cortical inputs to deep layers of cat's superior colliculus.

In the superior colliculi of cats anesthetized with ketamine, 84% of identified output cells of the deep layers could be driven by shocks to the contralateral optic disk, optic chiasm, or ipsilateral optic tract; 75% of these deep-layer cells had response latencies reflecting a polysynaptic influence of retinal Y-cells. Following large, acute lesions of the ipsilateral occipital cortex (including visual areas 17, 18, 19, and the posteromedial lateral suprasylvian area (PMLS), only 18% of deep-layer output cells were driven by electrical stimulation of the optic pathway and only 4% exhibited an indirect Y-cell influence. Thus, one or more of these visual areas may be important for the relay of retinal information, and particularly of Y-cell information, to the deep layers of the superior colliculus. This hypothesis is supported by the observation that intracortical stimulation in areas 17, 18, 19, and PMLS activated many cells of the ipsilateral, deep tectal layers at latencies consistent with those exhibited by the indirect Y-cell pathway. The distributions of activation latencies were similar to those observed in the superficial layers, raising the possibility that at least some of the cortical influence on the deep layers may be mediated by direct connections. Cells of the deep layers were more likely to be excited by a cortical stimulus that activated cells immediately above them in the superficial layers than by a stimulus that did not. This indicates that the functional connections between visual cortex and the deep collicular layers exhibit a topographic orderliness similar to that previously described for corticotectal projections to the superficial layers. These results provide further evidence that the visual cortex exerts a significant influence on cells of the deep collicular strata and that the pathways involved are capable of mediating the indirect, retinal Y-cell input to these neurons.