Visual-evoked potentials (VEPs) were recorded from the surface of the optic tectum of the freshwater turtle, Pseudemys scripta elegans, in response to phase reversal of square-wave gratings of different spatial frequency and contrast. The refractive state of a group of 12 turtles in air was assessed from VEPs by placing trial lenses in front of the eye. The group mean refraction did not differ significantly from emmetropia, as compared to 4.8 diopters of hyperopia when refracted retinoscopically. The difference was explained by the retinoscopic reflex originating from the interface between vitreous humor and retina. Peak VEP amplitude was approximately linear with log grating contrast; extrapolation to zero VEP amplitude yielded contrast thresholds as low as 1%. High spatial-frequency cutoffs ranged from 4.4–9.9 cycle/deg in different animals, the highest values corresponding to the intercone spacing in the area centralis and to behavioral measures of acuity in a related species.

It has been proposed that flying foxes (genus Pteropus) have a primate-like pattern of representation in the superficial layers of the superior colliculus (SC), whereby the visual representation in this structure is limited by the same decussation line that limits the retino-geniculo-cortical projection (Pettigrew, 1986). To test this hypothesis, visual receptive fields were plotted based on single- and multi-unit recordings in the SC of ten flying foxes. A complete representation of the contralateral hemifield was observed in the SC. Although the binocular hemifield of vision in Pteropus is 54 deg wide, receptive-field centers invaded the ipsilateral hemifield by only 8 deg, and the receptive-field borders by 13 deg. This invasion is similar to that observed at the border between visual areas VI and V2 in the occipital cortex. The extent of the ipsilateral invasion was not affected by a lesion that completely ablated the occipital visual areas, thus suggesting that this invasion may be consequence of a zone of nasotemporal overlap in the retinal projections to the two colliculi. Neurones located in the superficial layers typically responded briskly to stimulation of both eyes, with a bias towards the contralateral eye. After cortical lesions the neuronal responses to the ipsilateral eye were depressed, and the ocular-dominance histograms shifted towards an even stronger dominance by the contralateral eye. However, cells located in the rostral pole of the SC remained responsive to the ipsilateral eye after cortical lesions. Responses in the stratum opticum and stratum griseum intermediate were more severely affected by cortical lesions than those in the stratum griseum superficiale. Our results demonstrate that the SC in flying foxes retain some generalized mammalian characteristics, such as the stronger direct projections of the contralateral eye and the location of the upper, lower, central, and peripheral representations in the SC. Nonetheless, the extent of visual representation in the SC demonstrates a specialized, primate-like pattern. These observations are consistent with the hypothesis that megachiropterans are members of a group that branched off early during the differentiation of primates from basal mammals.

The ground level visual field of each eye of the leopard frog includes the entire ipsilateral 180-deg field and approximately 60 deg into the frontal contralateral field. When one eye is covered with an opaque patch, a frog responds to prey stimuli over the entire field of the other eye. Nevertheless, when one optic nerve is cut, the animal responds to prey in the ipsilateral hemifield of the connected eye, but only responds as far as about 30 deg past the frontal midline. If one optic tract is cut, the animal does not respond to prey past the frontal midline. We hypothesized that the responses past the frontal midline might be mediated by input from contralaterally projecting isthmotectal fibers. These fibers originate in the nucleus isthmi, a posterior midbrain structure. We found that when we placed an opaque patch over one eye and either ablated the ipsilateral nucleus isthmi, or cut crossing isthmotectal fibers in the optic chiasm, or blocked input to nucleus isthmi by ablating the ipsilateral tectal lobe, animals did not respond to prey stimuli past the frontal midline. We found that when we placed an opaque patch over one eye and cut crossing optic fibers in the anterior part of the optic chiasm (sparing crossing isthmotectal fibers), animals responded to prey stimuli in the nasal half of the seeing eye's contralateral frontal field. Our results suggest that contralaterally projecting isthmotectal fibers enable the frog to respond to stimuli past the frontal midline. We suggest a one-dimensional model of how nucleus isthmi influences tectal function.

Two types of centrifugal pathways to the retina have been found in the vertebrates, according to the location of the cell bodies and presence or absence of connections with the optic tectum. One type is represented by the isthmo-optic nucleus (ION) of birds and, therefore, termed “ION-type” retinopetal system. The other type is termed “non-ION-type” retinopetal system. The ION-type retinopetal systems have been found in the cyclostomes, teleosts, reptiles, and birds. This review describes the anatomy and physiology of the ION-type retinopetal systems, mainly of birds and teleosts. On the basis of anatomical and physiological evidence cited in this review, the ION-type retinopetal systems can be regarded as the tectofugal pathways to the retina. The function of the ION-type retinopetal systems is discussed in detail, with special emphasis on their relation to the role of the tectum in mediating visuomotor behavior.

Recordings of field potentials in nucleus isthmi (NI) were obtained in an in vitro preparation of goldfish brain using a lateral approach. Horseradish peroxidase (HRP) was injected from recording electrodes to verify recordings within the nucleus and to label axonal pathways and cell bodies. Activity in NI was repetitive and could be elicited by stimulation of the optic nerve, tectum, pretectum, or tectobulbar tract. Spontaneous activity was present in some preparations and consisted of bursts with intervening silent periods. Anatomical and electrophysiological evidence indicated that the primary isthmotectal pathway is composed of fine fibers that exit NI rostrally and pass through pretectum to enter tectum rostrally. An afferent pathway consisting of both fine- and large-diameter fibers entered NI ventromedially; the large diameter axons have been previously reported in percomorph fishes, but were not thought to be present in cyprinids such as goldfish. The large diameter axons arise from labeled cell bodies in the region of the lateral thalamic nucleus. No labeled cell bodies were seen in ipsilateral nucleus pretectalis superficialis, pars magnocellularis, where they are seen in percomorphs. The fine axons, which have not been reported in percomorph fishes, were shown to arise from tectal bipolar (type VI) neurons. As in percomorphs, tectal type XIV neurons were also labeled. This and corroborating recordings from nucleus isthmi constitute the first demonstration of a tectoisthmic projection in a cyprinid fish.

Recent immunocytochemical studies indicate the existence of several classes of peptide- (PRGC) and catecholamine-containing retinal ganglion cells in anurans, birds, and mammals. Different classes of PRGC project to discrete and seemingly unique layers in the retino-recipient portion of the anuran and avian optic tectum. Peptide-containing retinofugal projections to the frog tectum originate early in development, and are reestablished by some classes of PRGC during regeneration of the optic nerve. These findings indicate that chemically specific, parallel retinofugal pathways presumably subserve different functional aspects of vision in vertebrates. Exciting prospects for research include the correlation of physiologically with immunocytochemically defined classes of retinal ganglion cells, the analysis of the possible role of neuroactive peptides in retinofugal transmission, and the pharmacological manipulation of putative peptidergic retinofugal pathways to analyze their role in visual function.

Tectal evoked potentials (TEPs) in response to sinusoidal gratings of different contrast, spatial and temporal frequency have been recorded from the tectal surface of the pigeon. Responses have been digitally filtered in order to isolate transient oscillatory (fast) potentials (50–150 Hz), transient slow potentials (1–50 Hz), and the steady-state second-harmonic component (16.6 Hz). Transient slow potentials, as well as the steady-state second-harmonic component, are band-pass spatially tuned with a maximum at 0.5 cycles/deg and attenuation at higher and lower spatial frequencies. The high spatial frequency cutoff is 4–5 cycles/deg. Both transient slow potentials and the steady-state second-harmonic component increase in amplitude as a function of log contrast and saturate at about 20% contrast. The contrast sensitivity, as determined by extrapolating TEP amplitude to 0 V is 0.1–0.2%. These characteristics of spatial-frequency selectivity and contrast sensitivity are similar to those reported for single tectal cells. Unlike slow potentials, oscillatory potentials are not band-pass spatially tuned. In addition, their contrast response function does not saturate at moderate contrast. These differences suggest that tectal evoked slow and fast potentials reflect the activity of different neuronal mechanisms.

This study was performed in order to establish whether selective depletion of serotonin (5-HT) and its metabolite 5-hydroxyindoleacetic acid (5-HIAA) in the pigeon optic tectum (TeO) induced by p-chloroamphetamine (p-CA) modified tectal evoked potentials (TEPs). TEPs in response to sinusoidal gratings of different contrast, spatial and temporal frequency were recorded in control pigeons and in pigeons intraperitoneally injected with p-CA (10 mg/kg; two administrations in consecutive days). TEPs of p-CA treated pigeons, as compared to those of control pigeons, were reduced in amplitude as a function of contrast, spatial and temporal frequency. In addition, TEPs of p-CA treated pigeons differed from those recorded in controls in their transfer characteristics of contrast and spatial frequency. In particular, TEPs of p-CA treated pigeons did not saturate at moderate contrast, unlike those of controls. Furthermore, the TEP spatial tuning in p-CA treated pigeons is broader than that in controls; it thus suggests a reduction of spatial-frequency selectivity. These findings indicate that a selective neurotoxin for serotonergic systems, such as p-CA, can serve as a useful denervation tool for the study of the serotonergic function in the pigeon TeO. In addition, selective changes of TEP properties suggest the possibility that serotonergic afferents play a modulatory role on the receptive-field characteristics of tectal neurons.

Multiunit activity was recorded in the optic tectum of awake pigeons with two electrodes at sites varying in depth and separated by 0.3 to 3.0 mm. Autocorrelation and cross-correlation functions were computed from the recorded spike trains to determine temporal relationships in the neuronal firing patterns. Cross-correlation analysis revealed that spatially separate groups of cells in the tectum show synchronous responses to a visual stimulus. Strong synchronization occurred in both superficial and deep layers of the tectum, in general with zero-phase shift. The response synchronization in the avian optic tectum resembles that observed in the mammalian cortex, suggesting that it may subserve common functions in visual processing.

A small number of enkephalin-like immunoreactive cells were observed in the ganglion cell layer of the pigeon retina. Many of these neurons were identified as ganglion cells, since they were retrogradely labeled after injections of fluorescent latex microspheres in the contralateral optic tectum. These ganglion cells were mainly distributed in the inferior retina, and their soma sizes ranged from 12–26 μm in the largest axis. The enkephalin-containing ganglion cells appear to represent only a very small percentage of the ganglion cells projecting to the optic tectum (less than 0.1%). Two to 7 weeks after removal of the neural retina, there was an almost complete elimination of an enkephalin-like immunoreactive plexus in layer 3 of the contralateral, rostrodorsal optic tectum. These data provide evidence for the existence of a population of enkephalinergic retinal ganglion cells with projections to the optic tectum.

Immunohistochemical and retrograde tracing techniques were combined to study the retinal ganglion cells which project to the pars ventralis of the lateral geniculate nucleus (GLv) in the pigeon. Using two different fluorescent tracers, two histochemically-distinct populations of ganglion cells were found to project to both the GLv and the optic tectum. The first population of ganglion cells exhibited tyrosine hydroxylase-like immunoreactivity and represented about 20% of all ganglion cells which were retrogradely labeled from the GLv. The second population of ganglion cells showed substance P-like immunoreactivity and represented about 13% of all ganglion cells projecting to the GLv. These results confirm earlier suggestions that the retinal axons projecting to the GLv also project elsewhere and demonstrate that heterogeneity of retinal ganglion cells transmitters is evident even within a single retino-recipient nucleus such as the GLv.

The eyes of adult barn owls (Tyto alba) are virtually fixed in the head in positions that are highly consistent from one individual to the next. However, early in development the eyes are exodeviated; the eyes achieve their adult positions during the owl's second month of life. Disruption of binocular vision in baby owls leads to permanent, highly abnormal eye positions and interocular alignment. Of three owls raised with both eyelids sutured closed, two developed exotropic strabismus and one developed esotropic strabismus. Two owls reared with monocular vision developed esotropic strabismus, whereas three owls reared with fused, but optically deviated binocular vision developed normal eye positions. Thus, the alignment of the eyes in adults results from an active process that depends on fused binocular vision during early life.

Extracellular microelectrode recordings from the optic tecta of strabismic owls reveal that many units retain binocular inputs from corresponding points of the two eyes: the left-eye and right-eye receptive fields of individual units are misaligned by an amount predicted by the direction and magnitude of the strabismus. These results indicate that an innately determined pattern of connections in the brain anticipates the eye positions necessary to achieve binocular fusion. The hypothesis is put forth that the powerful activation of such binocular neurons by strong, synchronous inputs from the two eyes is the signal required by the optimotor system that proper eye alignment has been attained.

We have developed two brain slice preparations for studying tectofugal visual pathways in the chick: conventional, 400-μm slices (“thin slices”), and “thick slices” which encompass the rostral pole of the optic tectum and the contralateral optic nerve. Stimulation was delivered with a bipolar electrode positioned in stratum opticum in thin slices and in the contralateral optic nerve in thick slices. While the latter preparation provided a means of exclusively and unambiguously activating retinal afferents, several lines of evidence also indicated that the evoked field potentials in thin slices were chiefly consequent to retinal afferent excitation: (1) the similarity of evoked field potentials in thin slices to those in thick slice preparations; (2) their precise localization in retinorecipient layers as shown by prelabeling from retina with FITC-coupled cholera toxin; (3) transmission delays appropriate for retinal afferents as established with the thick slice preparation; (4) patterns of labeled afferents resulting from applications of Dil crystals to slices fixed after recording; and (5) the similarity in transmitter pharmacology between thin and thick slice preparations. Pharmacological manipulations carried out with bath-applied antagonists indicated that glutamate is the principal retinotectal transmitter. The broadly active glutamate receptor blocker, kynurenic acid, reversibly eliminated the postsynaptic component of the field potential as confirmed with 0 Ca2+ saline. A complete block was also effected by the non-NMDA antagonists CNQX and DNQX. The specific NMDA antagonist, APS, caused a smaller and variable reduction in response amplitude. The GABA antagonist, bicuculline, caused a prolongation of the monosynaptic field epsp in retinorecipient layers and an enhancement of the long-latency, negative wave in cellular layers below, supporting a late, excitation-limiting role for this inhibitory transmitter.

This commentary extends the review by Hiroyuki Uchiyama (1989) entitled “Centrifugal pathways to the retina: influence of the optic tectum” Visual Neuroscience 3, 183–206. A further scrutiny is made of the topography of the isthmo-retinal projection of the pigeon, which provides the most fully investigated example of a retinopetal projection. It is suggested that the topographical organization in this system is compatible with it's input being derived from the lower visual field (and upper retina) and it's output being directed to the horizon and lower retina. This is another form of attentional hypothesis for the centrifugal pathway, compatible with a role in ground feeding, and is testable by current tracing techniques in neurobiology.

The nucleus isthmi (NI) of the frog receives input from the ipsilateral optic tectum and projects back to both optic tecta. After ablation of NI, frogs display no visually elicited prey-catching or threat avoidance behavior. Neural mechanisms that underlie the loss of such important behavior have not been solved. Electrophysiological examination of the contralateral isthmotectal projection has proved that it contributes to binocular vision. On the other hand, there are very few physiological investigations of the ipsilateral isthmotectal projection. In this study, current source density (CSD) analysis was applied to contra- and ipsilateral isthmotectal projections. The contralateral projection produced monosynaptic sinks in superficial layers and in layer 8. The results confirmed former findings obtained by single unit recordings. The ipsilateral projection elicited a prominent monosynaptic sink in layer 8. Recipient neurons were located in layers 6–7. These results, combined with those from the former intracellular study, led to the following neuronal circuit. Afferents from the ipsilateral NI inhibit non-efferent pear shaped neurons in the superficial layers, and strongly excite large ganglionic neurons projecting to the descending motor regions. Thus feedback to the output neurons strengthens the visually elicited responses.

Visually evoked extracellular neural activity was recorded from the nucleus isthmi (NI) of goldfish and bluegill sunfish. When moving anywhere within the right eye's visual field, three-dimensional checkered balls or patterns on a computer screen evoked bursts of spikes in the left NI. Object motion parallel to the longitudinal body axis gave responses that habituated markedly upon repetition, but movement into recently unstimulated regions of the visual field gave vigorous responses. Thus, while NI's response is not visuotopic, its habituation is. An object approaching the animal's body generated a rising spike density, whereas object recession generated only a transient burst. During the approach of a checkered stimulus ball, average NI spike density rose linearly as the ball-to-eye distance decreased and at a rate proportional to the ball's speed (2.5–30 cm/s). Increasing ball size (2.2–9.2 cm) did not affect the rate of activity rise at a given speed, but did increase overall activity levels. NI also responded reliably to expanding textures of fixed overall size. The results suggest that NI signals changes in motion of objects relative to the fish, and estimates the proximity of approaching objects.

The superficial layers of the frog optic tectum receive a projection from the contralateral eye that forms a point-to-point map of the visual field. The monocular part of the visual field of the contralateral eye is represented in the caudolateral region of the tectum while the binocular part of the visual field is represented in the rostromedial tectum. Within the representation of the binocular field (rostromedial tectum), the maps of visual space from each eye are aligned. The tectal representation of the binocular visual field of the ipsilateral eye is mediated through a crossed projection from the midbrain nucleus isthmi. This isthmotectal projection also terminates in the caudolateral region of the optic tectum, yet there has been no indication that it forms a functional connection. By extracellular recording in intermediate layer 7 of the caudolateral tectum, we have discovered electrical activity driven by visual stimulation in the monocular visual field of the ipsilateral eye. The units driven from the ipsilateral eye burst upon initial presentation of the stimulus. At individual layer 7 recording sites in the caudolateral tectum, the multiunit receptive field evoked from the ipsilateral eye is located at the mirror image spatial location to the multiunit receptive field driven by the contralateral eye. Thus, as revealed electrophysiologically, there are superimposed topographic maps of the monocular visual fields in the caudolateral tectum. The ipsilateral eye monocular visual field representation can be abolished by electrolytic ablation of contralateral nucleus isthmi.

Although the zebrafish has become an important model in visual neuroscience, little has been done to examine the processing of its higher visual centers. The purpose of this work was twofold. The first purpose was to examine the physiology of the zebrafish retinotectal system and its relationship to retinal physiology. Spectral sensitivity functions were derived from visually evoked tectal responses and these functions were compared to the functions of electroretinogram (ERG) responses obtained using the same stimulus conditions. The second purpose was to examine the recovery of visual functioning of the tectum following optic nerve damage. The optic nerves of adult zebrafish were damaged (crushed), and tectal visual processing was assessed following damage. The results showed that the spectral sensitivity functions based on the On-responses of the tectum and ERG were qualitatively similar. The functions based on each response type received similar cone contributions including both nonopponent and opponent contributions. However, the spectral sensitivity functions based on the Off-responses of the tectum and ERG differed. The results also showed that the zebrafish visual system is capable of neural regeneration. By 90 days following an optic nerve crush, the spectral sensitivity function based on the tectal On-response was similar to functions obtained from normal zebrafish. Although the tectal Off-response did recover, the spectral sensitivity based on the Off-response was not the same as the function of normal zebrafish. These results support the notion that different levels of the visual system process information differently and that the zebrafish visual system, like those of other lower vertebrates, is capable of functional regeneration.

This work studies the afferent connectivity to different functionally identified tectal zones in goldfish. The sources of afferents contributed to different degrees to the functionally defined zones. The dorsocentral area of the telencephalon was connected mainly with the ipsilateral anteromedial tectal zone. At diencephalic levels, neurons were found in three different regions: preoptic, thalamic, and pretectal. Preoptic structures (suprachiasmatic and preoptic nuclei) projected mainly to the anteromedial tectal zone, whereas thalamic (ventral and dorsal) and pretectal (central, superficial, and posterior commissure) nuclei projected to all divisions of the tectum. In the mesencephalon, the mesencephalic reticular formation, torus longitudinalis, torus semicircularis, and nucleus isthmi were, in the anteroposterior axis, topographically connected with the tectum. In addition, neurons in the contralateral tectum projected to the injected zones in a symmetrical point-to-point correspondence. At rhombencephalic levels, the superior reticular formation was connected to all studied tectal zones, whereas medial and inferior reticular formations were connected with medial and posterior tectal zones. The present results support a different quantitative afferent connectivity to each tectal zone, possibly based on the sensorimotor transformations that the optic tectum carries out to generate orienting responses.

Neural activity in the optic tectum was compared with activity in the nucleus isthmi (NI) of both goldfish and sunfish with the aim of understanding how the two brain structures interact to process visual information. The two species yielded very similar results. Superficial tectum responds reliably to visual stimulation with topographically organized receptive fields; deep tectum and NI respond to stimulation throughout the field of the contralateral eye and habituate rapidly. Bursts of large-amplitude spiking in NI occur spontaneously and in response to contralateral visual stimulation. These NI bursts correlate with activity bursts across the tectal lobe on the same side, especially in the deeper layers. NI bursts may also synchronize with spiking activity in deep tectum. Trains of small-amplitude spikes in NI can be elicited by both ipsilateral and contralateral stimulation, but are not reflected in tectal activity. Simultaneous recordings from two sites in one NI were almost identical, suggesting that NI operates as a functional unit, broadcasting the same message across the ipsilateral tectal lobe.