Ipsilateral Retinal Projection Research Articles

Expansion of the ipsilateral retinal projection in the frog brain during optic nerve regeneration: sequence of reinnervation and retinotopic organization.

AbstractThe sequential reinnervation and distribution of optics axons in diencephalic and mesencephalic targets was studied after crushing the optic nerve in 37 adult Rana pipiens. Following intravitreal injection of 3H‐proline at various times after nerve crush the distribution of regenerating optic axons was traced using autoradiographic methods. The maximal distribution of regenerating axons was reached between 6 and 8 weeks after optic nerve crush. On the contralateral side of the brain, the distribution of fibers was similar to the normal projection. Ipsilaterally, silver grain density was greater than normal in the optic tract and projections were expanded to all optic targets on this side of the brain. These abnormal projections were sustained for a least 6 months after nerve crush.The sequence of reinnervation of targets on both sides of the brain differed from normal development. Unlike development, regenerating optic axons were found in the ipsilateral optic tract prior to the time they were found on the contralateral side of the brain. Also unlike development, regenerating axons did not begin to reinnervate targets in the anterior thalamus until several weeks after reinnervation of the posterior thalamus and tectum had begun. The expanded distribution of regenerating axons within optic targets on the ipsilateral side of the brain became evident at the time optic axons first invaded each area.Most optic axons appeared to regenerate from the point of nerve crush. The retinal stump of the crushed nerve was filled with labeled axons in all six frogs given intravitreal 3H‐proline injections between 1 and 7 days after nerve crush. In addition, using a modified Fink‐Heimer method, few degenerating axons were found in the retinal stump of four frogs sacrificed between 2 and 8 days after optic nerve crush.In ten frogs studied between 3 and 6 months after nerve crush, horseradish peroxidase (HRP) was placed on different portions of the tectum ipsilateral to the crush. In each case HRP was retrogradely transported to ganglion cells in both retinae. The cells labeled in the ipsilateral retina corresponded in position to the same region of the contralateral retina although many fewer cells were labeled ipsilaterally. Cutting the optic tract on the side opposite the HRP placement did not affect the results. No ganglion cells were labeled in the ipsilateral retina of two frogs not receiving optic nerve crush.These results show that axons from all parts of the retina regenerate to the ipsilateral side of the brain during optic nerve regeneration and the distribution of these misrouted axons, at least to the tectum, overlaps the intact distribution from the other eye. Differences between development and regeneration in the patterns of growth of optic axons may be related to this anomaly.

Evidence for ganglion cell death during development of the Ipsilateral retinal projection in the rat

When one eye of a rat is removed at birth an increased projection to the brain is found from the remaining eye. This projection arises from the whole retina and mainly from ganglion cells which project to only one hemisphere of the brain. In the normal course of development many of these cells die and the uncrossed projection diminishes to form the normal adult pattern.

Effects of neonatal enucleation on receptive-field properties of visual neurons in superior colliculus of the golden hamster.

1. Monocular enucleation in infant hamsters results in a marked expansion of the normally very limited ipsilateral retinotectal projection (13). In 34 hamsters subjected to removal of one eye within 12 h of birth, the receptive-field characteristics of superior collicular neurons ipsilateral and contralateral to the remaining eye were investigated quantitatively and compared to those of normal animals. In six additional neonatal enucleates, the density of the expanded retinotectal projection was studied with the autoradiographic method and an attempt was made to relate the anatomical reorganization with the electrophysiological findings, 2. The response characteristics of visual cells in the colliculus contralateral to the remaining eye were not significantly different from those observed in normal animals. In the ipsilateral tectum, however, numerous changes were observed. Visual receptive fields were abnormally large. The incidence of directional selectivity was markedly reduced, as were the magnitudes of the discharges elicited by either flashed or moving stimuli. Fewer cells were activated by small flashed spots and most of the units that were responsive to such stimulation failed to exhibit the surround suppression typical for the majority of tectal neurons in normal hamsters. Most cells in the ipsilateral colliculus responded only to relatively low (less than 50 degrees/s) stimulus velocities and response decrements resulting from repeated stimulation also occurred much more readily for the neurons tested on this side. 3. The results of additional experiments in neonatal enucleates (n = 8), which were also subjected to acute bilateral removal of the visual cortex, demonstrated that such damage resulted in a marked reduction in the incidence of directional selectivity in the colliculus contralateral to the remaining eye but had no effect on the responses of cells innervated by the aberrant ipsilateral pathway. 4. A correlation between the relative density of the ipsilateral retinal projection at different points in the colliculus, as demonstrated by the autroradiography and the nature of the visual responses obtained in different portions of the structure, indicated that receptive-field size was negatively correlated with the density of the aberrant retinotectal projection and that absolute responsivity (number of impulses elicited by an optimal stimulus) was positively correlated with autoradiographic grain density. 5. These findings demonstrate that while the aberrant retinocollicular projection can, along with the other visual inputs to the tectum, result in the organization of normal response properties for a small number of tectal neurons, the majority of the visual cells innervated by this pathway have responses that are appreciably different from normal.

Studies of visual function and its decay in mice with hereditary retinal degeneration.

Functional implications of mouse hereditary retinal degeneration have been studied at the level of the superior colliculus and visual cortex in the C57BL/6J-le rd strain. On autoradiography at a light-microscopic level, following eye injection with radioactive compounds, central visual structures appeared normal. A slight reduction in ipsilateral retinal projection was probably related to reduced retinal pigmentation associated with the light ear (le) mutation. In recordings from visual cortex and tectum in rd mice older than five months the cells discharged with highly rhythmic maintained activity. This ongoing activity depended on retinal input, since temporary asphyxia of the eye stopped it immediately. The frequency of the rhythm was influenced by the anesthesia. In these older mice no visual receptive fields could be mapped, but in a few tectal recordings it was possible to suppress the maintained activity by diffuse, very intense illumination. As in normal mice, no auditory or somatosensory responses were observed in the visual cortex or upper tectal layers. In recordings from tectum before the age of three weeks retinotopic topography and receptive fields were normal. By day 24 no receptive fields could be recorded from parts of the tectum representing the central 90--100 degrees of the visual field, whereas within a peripheral ring responses were still roughly normal under photopic conditions. Over the following four months these peripheral responses faded away slowly. Incremental thresholds, especially in the scotopic range, were elevated, rising slowly to unmeasurable values. Similarly during dark adaptation the thresholds fell to values several log units above those reached in normal mice; these values of dark adapted thresholds in rd mice rose with age. This is consistent with morphological changes known to occur in the retina as a consequence, of the rd mutation the rods degenerating before the cones.

The paths and destinations of the induced ipsilateral retinal projection in goldfish

Adult goldfish had one tectal lobe removed surgically, and several months later, the eye contralateral to the missing tectum was injected with radioactive proline. Radioautographs of the brains were studied to trace the paths and termination sites of the optic fibers. The optic tract decussated at the chiasm, as normally, but then ran caudally in a large neuroma on the tectum-less side of the brain. Substantial numbers of fibers left this neuroma to enter two or more of five commissures, through which they recrossed the midline. These commissures: transverse, minor, horizontal, posterior and ansate, ordinarily contain few or no optic fibers. All are normally linked with the tectum. Negligible numbers of aberrant optic fibers recrossed the midline elsewhere. On the intact side of the brain, ipsilateral to the injected eye, the optic fibers innervated some or all of the nuclei and areas normally served by contralateral retinal fibers. An earlier behavioral study of these same fish had shown that some of them made reversed optokinetic nystagmus in response to stripe movement seen by the eye projecting ipsilaterally; others failed to respond to stimuli through this eye. In all the reversed responders, a caudal group of retinal projection sites was labeled ipsilaterally. This included the basal optic nucleus and the caudal portions of nucleus dorsolateralis thalami and area pretectalis. In the non-responders, these targets were not labeled ipsilaterally. Together, these results suggest that one or more of these three sites is or are responsible for optokinetic nystagmus in normal goldfish.

Early lesions of superior colliculus: factors affecting the formation of abnormal retinal projections.

The longest fibers of the main optic tract reach the upper layers of the superior colliculus (SC) of the midbrain. Destruction of this terminal area in newborn hamsters caused striking anomalies in the distribution of the optic tract, studied after the animals were fully grown. Evidence of termination was found in areas normally devoid of such termination: in the remaining tissue of the colliculus and in the thalamic nucleus lateralis posterior (LP). An abnormally high density of termination was found in part of the ventral nucleus of the lateral geniculate body. These thalamic regions normally receive connections from SC. Retinofugal axons could also be induced to terminate in the medial geniculate body of the thalamus if the brachium of the inferior colliculus, which normally carries auditory information to this cell group, was ablated at birth together with the lesion of SC.If the superficial layers of SC were destroyed unilaterally at birth, axons from the eye contralateral to the lesion not only reached the area of early damage, but also formed an abnormal decussation, crossing the tectal midline to terminate in the medial zone of the undamaged colliculus. Axons from the two eyes <i>competed for terminal space </i>in this intact colliculus, for they terminated in a nonoverlapping manner, and if the axons from the eye contralateral to the remaining SC were eliminated at birth, the anomalously recrossing axons increased in quantity and spread across the entire SC on the 'wrong' side of the midbrain. Hamsters with such an anomaly showed wrong-direction turning in response to visual stimuli in a large part of the visual field.The less the amount of termination found in SC, the greater was the amount in LP. Thus, optic tract axons showed a <i>'pruning effect' </i>which may be attributed to a tendency for axons to conserve the quantity of their terminal arborizations. The pruning effect alone may account for the hypertrophy we found, after early SC lesions, of the dorsal terminal nucleus of the accessory optic tract. The tendency to invade vacated terminal space may be sufficient to account for an effect of early unilateral eye removal, namely, a pronounced increase in an ipsilateral retinal projection to the medial terminal nucleus of the accessory optic tract.The greatest alterations in axonal projections were seen when the two effects, competition and pruning, seemed to act jointly. Additional factors may have to be considered in fully explaining such neuroplasticity; some of these have been suggested.

OPTIC NERVE REGENERATION WITH RETURN OF VISION IN ANURANS

OPTIC NERVE REGENERATION WITH RETURN OF VISION IN ANURANS