Flying primates? Megabats have the advanced pathway from eye to midbrain.

The pattern of connections between the retina and midbrain has been determined with electrophysiological and neuroanatomical methods in bats representing the two major subdivisions of the Chiroptera. Megachiropteran fruit bats (megabats), Pteropus spp., were found to have an advanced retinotectal pathway with a vertical hemidecussation of the kind previously found only in primates. In contrast, the microchiropteran bat Macroderma gigas has the "ancestral" or symplesiomorphous pattern of retinotectal connections so far found in all vertebrates except primates. In addition to linking primates and megachiropteran bats, these findings suggest that flight may have evolved twice among the mammals.

Neurons selective for orientation and binocular disparity in the visual Wulst of the barn owl (Tyto alba).

The visual response properties of single neurons in the owl's visual Wulst suggest that this forebrain structure is an analog of the mammalian visual cortex. Features in common with the cat and the monkey visual cortex include a precise topographic organization, a high degree of binocular interaction, and selectivity for orientation, direction of movement, and binocular disparity of straight-line contours.

Depletion of brain catecholamines: failure of ocular dominance shift after monocular occlusion in kittens.

Monocularly deprived kittens were compared with littermates that had had their eyelids sutured for the same time but that had, in addition, been treated with 6-hydroxydopamine to deplete their forebrains of catecholamines. The visual cortices of all the catecholamine-depleted kittens showed high proportions of binocular neurons, in contrast to the control group, most of whose visual cortical neurons were driven exclusively by the nondeprived eye. Catecholamines may play an important role in the maintenance of cortical plasticity during the critical period.

Gamma-aminobutyric acid antagonism in visual cortex: different effects on simple, complex, and hypercomplex neurons.

Intravenous bicuculline was used to examine how removing gamma-aminobutyric acid-mediated inhibition affects the visual response properties of single cortical neurons. Simple neurons were depressed and complex neurons showed increase in the vigor and range of responses. Hypercomplex cells were no longer inhibited by elongated stimuli. The results are consistent with present evidence concerning the origin and distribution of inhibitory connections within the cortex.

Visual experience without lines: effect on developing cortical neurons.

Kittens were reared in a planetarium-like visual environment that lacked straight line contours. Cortical neurons were subsequently highly sensitive to spots of light but not to straight lines, in marked contrast to those from a normal cat. If linear contour processing is an innate function it appears to be subject to substantial modification by early visual experience.

Receptive fields of auditory neurons in the owl.

The influence of sound location on the responses of auditory neurons in the forebrain of the owl (Tyto alba) was studied directly by using a remotely controlled, movable sound source under free-field, anechoic conditions. Some auditory neurons demonstrated well-defined receptive fields that were (i) restricted both in elevation and in azimuth and (ii) relatively independent of the intensity and the nature of the sound stimulus. The majority of the fields were located frontally and contralateral to the recording site.

Early development of X-cells in kitten lateral geniculate nucleus.

Lateral geniculate nucleus cells of the kitten were classified as X-cells or Y-cells with a contrast reversal test and their latencies to optic chiasm shock were measured. X-cells with mature latencies were found as early as 21 days. Y-cells did not have adult latencies at 40 days. The early development of some X-cells may be due to differential rates of fiber myelination and synaptic maturation within the lateral geniculate nucleus.

Primate-like retinotectal decussation in an echolocating megabat, Rousettus aegyptiacus.

The current study was designed to reveal the retinotectal pathway in the brain of the echolocating megabat Rousettus aegyptiacus. The retinotectal pathway of other species of megabats shows the primate-like pattern of decussation in the retina; however, it has been reported that the echolocating Rousettus did not share this feature. To test this prior result we injected fluorescent dextran tract tracers into the right (fluororuby) and left (fluoroemerald) superior colliculi of three adult Rousettus. After a 2-week survival period the animals were killed, fixed via transcardial perfusion, and the retinas whole mounted and examined under fluorescent excitation to reveal the pattern of retrograde transport. Red and green labeled retinotectal ganglion cells were found in side-by-side patches on either side of a vertical decussation line in the temporal retina of all six retinas. The Rousettus examined thus exhibited the same pattern of retinal decussation as reported previously for other megabats and primates, but unlike that seen in other mammals. The current result indicates that the prior study appears to have suffered technical problems leading to an incorrect conclusion. The results of our study indicate that, as may be expected, all megabats share the derived retinotectal pathway once thought to be the exclusive domain of primates. The current study provides additional support for the diphyletic origin of the Chiroptera and aligns the megabats phylogenetically as a sister group to primates.

Genomic evolution. Flying DNA.

The extremely high AT content of bat DNA complicates the reconstruction of bat phylogeny from DNA sequence data, but may help throw light on genomic evolution.

Convergence of specialised behaviour, eye movements and visual optics in the sandlance (Teleostei) and the chameleon (Reptilia)

Chameleons have a number of unusual, highly specialised visual features, including telescopic visual optics with a reduced lens power, wide separation of the eye's nodal point from the axis of rotation, a deep-pit fovea, rapid pre-calculated strikes for prey based on monocular depth judgements (including focus), and a complex pattern of partially independent alternating eye movements. The same set of features has been acquired independently by a teleost, the sandlance Limnichthyes fasciatus. Despite its underwater lifestyle, this fish displays visual behaviour and rapid strikes for prey that are remarkably similar to those of the chameleon [1]. In a direct comparison of the two species, we have revealed other, previously unsuspected, similarities, such as corneal accommodation, which was unknown in teleosts, as well as bringing together, for the first time, data collected from both species. The sandlance is the only teleost, among thousands studied, that has corneal refraction, corneal accommodation and reduced lens power, as well as sharing the other specialised optical features seen in chameleons. The independent eye movement pattern in the sandlance is also unusual and similar to that of the chameleon. The selection pressures that have produced this remarkable example of convergence may relate to common visual constraints in the life styles of these two phylogenetically disparate species.

Interhemispheric switching mediates perceptual rivalry.

BACKGROUND: Binocular rivalry refers to the alternating perceptual states that occur when the images seen by the two eyes are too different to be fused into a single percept. Logothetis and colleagues have challenged suggestions that this phenomenon occurs early in the visual pathway. They have shown that, in alert monkeys, neurons in the primary visual cortex continue to respond to their preferred stimulus despite the monkey reporting its absence. Moreover, they found that neural activity higher in the visual pathway is highly correlated with the monkey's reported percept. These and other findings suggest that the neural substrate of binocular rivalry must involve high levels, perhaps the same levels involved in reversible figure alternations. RESULTS: We present evidence that activation or disruption of a single hemisphere in human subjects affects the perceptual alternations of binocular rivalry. Unilateral caloric vestibular stimulation changed the ratio of time spent in each competing perceptual state. Transcranial magnetic stimulation applied to one hemisphere disrupted normal perceptual alternations when the stimulation was timed to occur at one phase of the perceptual switch, but not at the other. Furthermore, activation of a single hemisphere by caloric stimulation affected the perceptual alternations of a reversible figure, the Necker cube. CONCLUSIONS: Our findings suggest that interhemispheric switching mediates perceptual rivalry. Thus, competition for awareness in both binocular rivalry and reversible figures occurs between, rather than within, each hemisphere. This interhemispheric switch hypothesis has implications for understanding the neural mechanisms of conscious experience and also has clinical relevance as the rate of both types of perceptual rivalry is slow in bipolar disorder (manic depression).

A neurophysiological determination of the vertical horopter in the cat and owl.

We have undertaken a determination of the vertical horopter in two species by simultaneously mapping the receptive field positions of binocular cortical neurons at various elevations along the zero azimuthal meridians. In the paralyzed cat our recordings show that the zero meridians of the two eyes are parallel and vertical under paralysis. Slit-pupil photographs demonstrate that paralysis induces an average net intorsin of 9 degrees between the two eyes. Correction back to the unparalyzed state results in the zero meridians themselves being out-torted with respect to each other. Since the two eyes' zero meridians define physiologically the positions of corresponding retinal points, this out-torsion results in a vertical horopter in the mid-sagittal plane which is tilted away from the alert, unparalyzed cat. The limited eye movements of the owl permit the use of an unparalyzed preparation; it is therefore possible to avoid the problem of the cyclotorsion under paralysis which occurs in the cat. The results of our physiological analysis in the burrowing owl (Speotyto cunicularia) also reveal a tilted horopter in this terrestrial avian species.

Retinal ganglion cell topography in teleosts: a comparison between Nissl-stained material and retrograde labelling from the optic nerve.

The retinal topography of cells within the ganglion cell layer of three teleost species is examined in Nissl-stained material in which all neuronal elements containing Nissl substance in the cytoplasm are counted. A topographic comparison is made with retrogradely labelled ganglion cells to differentiate the proportion of nonganglion cells not possessing an axon joining the optic nerve. In the three species studied 92%, 80%, and 66% were found to be the maximum proportion of true ganglion cells in the area centralis, horizontal streak, and periphery, respectively. The proportion of nonganglion cells in the total population of cells counted was 24%. The major contribution to this discrepancy is from peripheral nonspecialized regions of the retina. There is little difference in both topography and peak densities of retinal ganglion cells between the two techniques. The soma areas of both populations are analysed, with the homogeneous nonganglion cell population possessing cells between 5 and 15 micron2 and the heterogeneous ganglion cell soma between 5 and 68 micron2, increasing in size with eccentricity.

The distribution of neurons projecting from the retina and visual cortex to the thalamus and tectum opticum of the barn owl, Tyto alba, and the burrowing owl, Speotyto cunicularia.

Using the HRP retrograde transport technique in two different genera of owls (Speotyto and Tyto), we have studied the distribution of neurons projecting to the optic tectum and the visual thalamus. Small injections of HRP were made into these structures from the pial surface after they had been visualized directly by dissection of the overlying bone. In contrast to the findings in mammals, retinal ganglion cells were labeled only in the eye contralateral to the injection site, whether this was in the thalamus or tectum, and the labeled ganglion cells were found on both nasal and temporal sides of the vertical retinal meridian through the fovea. After thalamic injections, labeling was prominent in temporal retina representing the binocular field, temporal to the optic nerve head. Retinothalamic ganglion cells formed roughly concentric lines of isodensity centered on the fovea (Speotyto) or area centralis (Tyto); labeling from thalamic injections involved both large and medium-sized neurons, but did not involve the smallest nor a conspicuous class of very large neurons. Tectal injections led to prominent labeling along the horizontal streak region, with horizontally elongated isodensity contours in both Tyto and Speotyto; retinotectal ganglion cells were heterogeneous and included a group of very large neurons and anther group of small neurons, neither of which was labeled from the thalamus. In the visual Wulst, labeled neurons were confined to the supragranular layers after both tectal and thalamic injections. Corticotectal neurons were found in both ipsilateral and contralateral visual Wulst. They were characterized by large cell bodies and prominent dendrites. Corticotectal neurons were distributed throughout the mediolateral extent of the ipsilateral Wulst and therefore involved both the monocular and binocular representations of the visual field. Corticothalamic neurons, found only in the ipsilateral Wulst, were characterized by smaller cell bodies and fine dendrites. They were confined to the monocular crescent on the extreme medial edge of the World.

The retinothalamic pathways in Siamese cats.

By injecting one lateral geniculate nucleus with large amounts of horseradish peroxidase (HRP), we have determined the retinal distributions of contra- and ipsilaterally projecting retinothalamic ganglion cells in the Siamese cat. In accord with the data of others, we observe that large numbers of temporal ganglion cells, which normally send axons ipsilaterally, instead misproject to the contralateral thalamus. However, in contrast to the expectations raised by previous work, we do not find the Siamese defect to be a simple 20 degrees shift of the naso-temporal decussation line. Rather, there is intermingling of the crossed and uncrossed retinothalamic populations in the temporal retina, with a gradual increase in the proportion of ipsilaterally projecting ganglion cells as one moves temporally. Thus, the Siamese abnormality represents not only a temporal displacement of the retinothalamic decussation line, but also a smearing of the normally rather sharp division between regions of ipsilateral and contralateral projection. Cell size measurements and anterograde transport of H3-proline confirm the HRP findings and suggest differential effects of the Siamese abnormality according to ganglion cell class. In particular, it appears that the large ganglion cells to misproject to a greater degree than the rest of the retinothalamic population.

The decussation of the retinothalamic pathway in the cat, with a note on the major meridians of the cat's eye.

We have studied the naso-temporal division of the retinothalamic pathway of the cat by making large unilateral injections of horseradish peroxidase into the lateral geniculate nucleus. In confirmation of previous work, our retinal whole-mounts show a distinct vertical decussation line separating the contralaterally projecting nasal retina from the ipsilaterally projecting temporal retina. The ipsilateral decussation line is quite sharp, while the contralateral decussation is somewhat more diffuse, with numbers of large cells extending a few degrees into the temporal retina. However, in contrast to the results of optic tract section, our material (demonstrating the thalamic component only) does not reveal any significant population of contralaterally projecting small cells across most of the temporal retina. The previous observation of approximately 200 micrometer of naso-temporal overlap in the area centralis is confirmed here, and evidence is presented that this overlap may increase at eccentricities above the horizontal meridian. Taken together with previously published data, this demonstration of the vertical decussation line has allowed us to estimate the relative inclinations of the major meridians of the cat's eye.

Preservation of binocularity after monocular deprivation in the striate cortex of kittens treated with 6-hydroxydopamine.

The results of single unit recordings from Area 17 of monocularly deprived kittens were compared with similar ones from littermates who had been monocularly lid-sutured for the same period of time, but who had in addition been given intraventricular injections of 6-hydroxydopamine (6-OHDA) to deplete brain catecholamines. This visual cortices of all catecholamine-depleted kittens showed high proportions of binocular neurons, in contrast to the control group, a majority of whose visual cortical neurons were driven exclusively by the non-deprived eye. Preservation of binocularity in 6-OHDA-treated kittens was dose-related. Even after a 1 to 2-week period of lidsuture which reduced binocularity to 20% in controls, normal proportions of binocular neurons (greater than 75%) were preserved if the cumulative dose had been 10 mg 6-OHDA or more. The density of single neurons sampled from electrode tracks through the cortex of drug-treated kittens was high and did not differ significantly from controls. Neurons were isolated every 100 micron on the average. There was some indication that the drug's effect in preventing an ocular dominance shift disappears by six weeks following cessation of 6-OHDA treatment. This reversal of the physiological effects in cortex is preceded by recovery from the behavioral manifestations of 6-OHDA treatments. Binocularity was only slightly increased in a kitten who received large doses of 6-OHDA after a period of monocular deprivation. This observation, together with control recordings from normal kittens and adults treated with 6-OHDA, indicates that the direct effects of 6-OHDA on cortical neurons' response properties play a minor role in comparison to its effects in reducing the sensitivity of the cortex to monocular deprivation. The overwhelming majority of cortical neurons in 6-OHDA-treated kittens remained normal in receptive field properties after a period of monocular deprivation. These data support the hypothesis that catecholamines are required for the maintenance of visual cortical plasticity during the critical period.

Restoration of visual cortical plasticity by local microperfusion of norepinephrine.

Using a newly developed technique of continuous microperfusion, we obtained further evidence in support of our hypothesis that the neocortical catecholamines (CAs), particularly norepinephrine (NE), are responsible for a high level of cortical plasticity. We used the visual cortical changes in ocular dominance which follow a brief monocular deprivation as a simple and reliable index of cortical plasticity. Local perfusion of kitten visual cortex with 1 mg/ml (4.0 mM) 6-hydroxydopamine (6-OHDA) prevented the effects of monocular deprivation in kittens, thus replicating the results we had obtained using intraventricular injections (Kasamatsu and Pettigrew, '76b, '79). Locally perfused NE at a concentration of of 10(-2) mg/ml (48.6 micron) restored visual cortical plasticity in animals which were no longer susceptible to brief monocular lid-suture. These numbers refer to the concentration of solutions in the cannula/minipump system. The effective concentrations at the site of recording (about 2 mm away) are probably much lower than these. This effect of NE perfusion was seen both in kittens which had received prior 6-OHDA treatment as well as in older animals which had outgrown the susceptible period. In the kittens we obtained as a nearly complete shift in ocular dominance toward the open eye and in the older animals a decrease in binocularity was obtained. The changes were found only in the local region of visual cortex perfused with either NE or 6-OHDA, while nearby cortical regions in the same animals were unaffected. There were no obvious changes in receptive field properties of individual neurons other than ocularity, and externally perfused NE did not itself reduce binocularity in normal animals: the effects of NE described about only occurred when the animal's visual experience was simultaneously altered. These results support the view that NE plays an important role in cortical plasticity.

Somatosensory cortical representation in the Australian ghost bat, Macroderma gigas.

Bats of the two suborders Microchiroptera and Megachiroptera have a modified hand in which the digits of the forelimb are caudally oriented to form the wing. In a previous study of a megachiropteran species, this modification of body plan was found to be reflected in the somatosensory cortical representation such that the orientation of the digit representation was reversed compared with walking mammals. This finding suggests that the precise details of arrangement of topographical maps are functionally significant and do not merely reflect an order imposed by peripheral innervation. Recent evidence for separate origins of Microchiroptera and Megachiroptera raises the question of whether the cortical somatosensory representation in Microchiroptera will also have a reversal of digit orientation compared with walking mammals. We recorded multiunit activity from the somatosensory cortex of a microchiropteran bat, Macroderma gigas. We found two orderly representations of the body surface, SI and SII, in both of which the digit orientation was opposite to the head orientation in accordance with adaptation for flight, and reversed with respect to equivalent maps in other mammals. We also found minor variations in body surface representation compared with Megachiroptera, in line with their proposed independent evolution.

The dorsal lateral geniculate nucleus of macropodid marsupials: cytoarchitecture and retinal projections.

The anatomy of the dorsal lateral geniculate nucleus (LGd) is described in five macropodid species, including two rat kangaroos (bettong and potoroo), two wallabies (pademelon and tammar), and the large grey kangaroo. The distribution of retinal terminals in the LGd was examined following intraocular injections of tritiated amino acids. There are considerable differences in both LGd cytoarchitecture and the patterns of retinal terminations among the five species. Cytoarchitecture in the bettong LGd is relatively simple, displaying a minimal regional differentiation. In contrast, the potoroo LGd is quite complex and displays several well-defined cell laminae, each of which is associated with input from a single eye. Both rat kangaroos display the same basic pattern of retinal termination with three bands of terminals from the contralateral eye and four from the ipsilateral eye. The bands are less sharply defined in the bettong, in which terminals from each eye overlap to a greater extent than is seen in the potoroo. The wallabies and kangaroos display a more complex LGd architecture and patterning of retinal terminal bands. Bilateral retinal projections within the same LGd lamina are unusual in these large macropodids. The number of terminal bands reaches ten in the grey kangaroo--four from the contralateral eye and six from the ipsilateral eye. The pademelon LGd is unusual in that it shows intraspecies variation with some animals displaying five ipsilateral terminal bands and others only four. The results are discussed in comparison with the patterns of LGd organisation observed in other mammalian lines, placental and marsupial. We conclude that LGd lamination and the segregation of retinal inputs to the LGd in marsupials are likely to be the result of evolutionary factors which differ from those which have produced ocular segregation and complex lamination in several lines of placental mammals.