Carlos Eduardo Rocha-Miranda

Postnatal development of retinogeniculate, retino-pretectal and retinotectal projections in the opossum

The postnatal development of retinogeniculate, retinopretectal and retinotectal projections has been studied by the anterograde transport of proline-labeled proteins in 20 pouch young opossums aged from 10 to 60 days. Radioautographical findings suggest delayed development of uncrossed as compared to crossed projections. There is a phase of overlapping projections from both eyes in thalamic and tectal target sites. Partial segregation of projections to the dorsal lateral geniculate nucleus (GLD) is preceded by differential distribution of crossed and uncrossed terminal fields along its dorsoventral axis (at age 23 days). The quasilaminar pattern of projections in the dorsocaudal region of GLD pars alpha is incipient by 42 days and is fully established at 60 days of age, as eye opening starts. The mature pattern of projections to the ventral lateral geniculate nucleus (GLV) is established much earlier, at 23 days of age. The development of retinopretectal projections is assessed mostly from the analysis of the olivary pretectal nucleus (PO). Distribution of silver grains into discrete areas coextensive with PO is relatively delayed (by 23 days of age) as compared to the nuclei of the lateral geniculate body. Soon after, however, the mature pattern of projections to PO is established (at 33 days of age). The early development of retinotectal projections (from 10 to 23 days) is compatible with an initial tangential course of crossed optic fibers in the superior colliculus (CS) but other alternatives remain open, such as a sequential outside-in arrangement of terminal fields of deeply coursing fibers. Arborization of uncrossed fibers is delayed at extreme rostromedial and caudolateral portion of the territory of the main uncrossed retinotectal projection. Segregation of uncrossed projections at different depths of CS is nearly complete by 42 days. Differences in the development of terminal fields in different target nuclei or in regions of a given target site are discussed in relation to retinal and local factors.

VISUAL RESPONSE PROPERTIES OF PRETECTAL UNITS IN THE NUCLEUS OF THE OPTIC TRACT OF THE OPOSSUM

SummarySingle-units were recorded from the nucleus of the optic tract. Most of the units showed excitation in response to random check patterns presented on a tangent screen to the contralateral eye, moving in a temporal to nasal direction and/or inhibition in the opposite direction. The excitatory response to the temporal to nasal movement, observed in most units, was unchanged throughout the range of speeds tested, except for a decrease at the slowest (0.6 deg/s) and fastest (150 deg/s) speeds. On the other hand, the inhibitory responses evoked by a nasal to temporal movement, had a peak between 3 and 16 deg/s which decreased towards both extremes. An average of 45% of the units were influenced by the stimulation of the ipsilateral eye. In one third of them the response was very weak. In the remainder, the mean frequency of spikes in one direction of the horizontal movement was more than twice that in the opposite stimulus direction. In the great majority of these units, stimulation of each eye yielded the same overall pattern of directionality, that is, movement of the stimulus towards the recording side led to excitation and/or movement in the reverse direction led to inhibition. Inhibition was stronger than excitation in most ipsilaterally responding units. Excitatory responses elicited by the ipsilateral eye were always weaker than those by the contralateral but in a few cases the ipsilateral inhibitory component was more prominent than the contralateral one.

Retinofugal projections in the opossum, An anterograde degeneration and radioautographic study.

A study of anterograde degeneration and anterograde transport was undertaken in the opossum primary optic system in order to clarify several points regarding fiber organization and patterns of terminal fields. Through the radioautographic technique of axon tracing, it was demonstrated that the accessory optic system follows the generalized scheme of Hayhow, consisting of two fascicles the three terminal nuclei.

Growth and restriction of the ipsilateral retinocollicular projection in the opossum

The distribution of optic nerve fibers and terminals in the superior colliculus (SC) was followed throughout its development in pouch young opossums in order to establish the normal sequence of events leading to the formation of mature patterns. Up to 7 days of life in the pouch, labeled fibers can be followed only as far as the rostral aspect of the optic tract. The earliest evidence for crossed retinal projections in the SC is found at 10 days of age. In parasagittal sections, the label extends along the rostrocaudal tectal axis from the rostral border to the presumptive caudal pole of the SC. Unequivocal evidence for ipsilateral retinocollicular projection is found at 15 days extending to all but the caudal 5th of the rostrocaudal extent of the SC. The projections from both eyes overlap extensively in the SC at 22 days and after this age significant changes occur, mostly at the ipsilateral side: a sub-pial tier of fine label develops excluding both rostral and caudal collicular poles; a deeper tier of coarse label extends from the rostral to the caudal pole and a third, patchy tier of label is found at the prospective strata griseum superficiale and griseum intermediate. By 47 and 60 days the tangential distribution of the projections is virtually indistinguishable from the adult pattern although laminar segregation does not seem as sharp as in the adult. Comparisons of the changeable patterns of ipsilateral retinocollicular projections from 22 to 34 days with the invariant, aberrant pattern in adult animals submitted to uniocular enucleation at either age suggests that the preservation of a juvenile pattern does not provide a comprehensive explanation for the formation of aberrant projections.

Receptive field properties of single units in the opossum striate cortex.

On the basis of their trigger-features, 98 units out of 127 recorded in striate cortex of immobilized opossums, under forced breathing of a nitrous oxide/oxygen mixture, were classified into 5 receptive field groups. Group 1 units (20/127) responding to small stationary spots were shown to be made up of regions of opposite response type and mutual antagonism, separate by linear boundaries. The optimal discharge was elicited by a stimulus configuration consisting of rectilinear regions of opposite contrast positioned and oriented in the visual field so as not to elicit antagonism while maximizing the overlap with regions responsive to that contrast. To edges in motion these units were shown to be made up of light and dark discharge centers, the locations of which could not be predicted from the map to stationary spots. In addition to position and orientation, direction was another important stimulus parameter. Group 2 units (34/127) had uniform requirements of stimulus orientation, direction of motion or both, througout the receptive field. Width was rarely a significant variable. Three subgroups were detected: orientation selective, directional selective and orientation-direction sensitive. Group 3 units (18/127) required stopped stimuli. In most instances (14/18) this property was attributed to a suppressive surround with relatively non-specific stimulus requirements. Oriented and non-oriented responsive receptive fields were observed. Group 3 units with no surround (4/18) responded best to properly positioned and oriented wedges, usually of 90 degrees. Group 4 units (24/127) had uniform fields with little stimulus specificity and were often responsive to diffuse light. Although not sensitive to stimulus orientation and direction, motion was frequently a requisite for optimal responses. Group 5 receptive fields (2/127) had concentrically arranged regions of distinct response type which displayed mutual antagonism. No sensitivity to orientation or direction was detected. Twenty-nine units remained unclassified. Other group distinctions were the relatively higher spontaneous activity of group 4 units and the large field sizes encountered among groups 1 and 4 when compared to group 2. Based on their properties and receptive field type distribution, we propose that striate receptive fields in the opossum have a similar organization to those of other mammals.

Patterns of corticocortical, corticotectal, and commissural connections in the opossum visual cortex.

Patterns of connections of the visual cortex of the South American opossum, Didelphis aurita, were revealed by using neuronal tracers to identify and characterize visual specializations of the peristriate cortex (PS). The visuotopy of corticotectal connections of the anterolateral portion of PS (PSal) is symmetrical to that of the striate cortex (ST or primary visual area [V1]). Three consecutive bands of commissural connections coincide, respectively, with the ST‐PS border, the limit between the caudal and rostral PSal halves (PSc and PSr), and the border of PS with the parietal and temporal cortices. PSc and PSr contain regular commissural rings similar to those present in the peristriate cortex of eutherian mammals. ST projections define in PSc two strings of periodical foci consecutively concentric to V1 and a single focus in PSr. Although they were organized topographically, ascending, descending, and commissural connections between ST and PSal showed a high degree of convergence and divergence. These results conform to the model of a single area homologous to the second visual area (V2) bordering V1. Moreover, they suggest the possibility that PSal includes either one or two additional belt‐like areas successively anterior to V2. Along with the finding of alternating bands of high and low cytochrome oxidase activity in PSal, the data further suggest that this region contains modular specializations similar to those of the peristriate cortex of primates and other eutherian mammals. The posterolateral peristriate cortex (PSpl) constitutes another visual area, since it consists of a distinct focus of reciprocal corticocortical and interhemispheric connections and a separate source of corticotectal projections. Finally, a visuomotor function for the orbital cortex is proposed based on its direct projections to optical tectal layers. The close cladistic relationship of opossums to mammalian ancestral forms suggests that the PSal parcelation into belt‐like areas that contain modules reflects the primitive organization of the visual cortex. Moreover, a highly diffuse pattern of corticocortical connections may represent a requirement for a brain with few visual areas to perform global processing. J. Comp. Neurol. 416:224–244, 2000.

The pretectal complex in the opossum: projections from the striate cortex and correlation with retinal terminal fields

Two terminal fields were revealed in the pretectal complex of the opossum by the Fink-Heimer method after striate cortical lesions. A rostral field is located within a rostrolateral strip of the compact part of the anterior pretectal nucleus, where a partial topographic arrangement of this projection is present. A caudal field is located within the sub-brachial nucleus of the optic tract, located between the brachium of the superior colliculus and the posterior pretectal nucleus. The corticotopic projection to this field is mirror-symmetric to that found in the superior colliculus and overlaps a bilateral projection from the retina. Based on neural pathway evidence, it is concluded that the nucleus of the optic tract in the opossum can be subdivided in (a) an intrabrachial nucleus receiving a direct projection from the contralateral retina and (b) a sub-brachial nucleus receiving projections from both retinae and from the striate cortex. The pretectal complex, as the superior colliculus, can be anatomically subdivided in a superficial region receiving visual input (the optic pretectum) and a deep region only remotely connected to the visual system. The optic pretectum, however, differs from the superior colliculus in displaying a multiple-map arrangement within its constituent nuclei, instead of a single continuous representation of the visual field.

Disparity selective units in the superior colliculus of the opossum

SummaryBinocular visual responses can be recorded in two regions of the superficial layers of the superior colliculus of the opossum. The direct binocular region (DBR) represents the binocular portion of the contralateral hemifield whereas the rostral pole (RP) represents the binocular portion of the ipsilateral hemifield. In the present study single units from both of these regions were tested with binocular and monocular stimulation. Most cells in both regions showed response facilitation when both eyes were simultaneously stimulated and, when tested with different binocular disparities, most cells showed broadly-tuned disparity selectivity. DBR units usually preferred disparities near zero whereas RP units had a wider range of preferred disparities, with a tendency toward positive (crossed) values. This data indicates that the superior colliculus of the opossum could provide a neural substrate for a coarse analysis of depth and also might help control vergence eye movements. The different ranges of disparity selectivity of DBR and RP are consistent with the previously reported monocular receptive-field data and suggest that DBR and RP analyze different depths of the 3-dimensional visual scene.

The ipsilateral field representation in the striate cortex of the opossum.

SummaryReference axes for the visuotopic study of the opossums striate cortex were estimated from corresponding binocular response fields using multi-unit recording. These central binocular axes (CBA) were derived from experimental data based on the concept that corresponding receptive fields for each eye should be mostly in register under natural conditions. Vertical reference meridians, orthogonal to these axes, define a contralateral and an ipsilateral field for each eye with respect to the recording site. An ipsilateral field representation was observed for both eyes in the striate cortex at the transition zone with peristriate. Maximal values for the center and border of ipsilateral receptive fields were, respectively, 8 and 20 degrees for the contralateral eye and 6 and 14 degrees for the ipsilateral eye. An equivalent ipsilateral field representation was found in animals that had the anterior commissure cut prior to the recording session. This suggests that the ipsilateral field of both eyes may be represented in the striate cortex via the ipsilateral optic tract. Additionally, it was observed that the region of higher ganglion cell density in the retina shows a flattened distribution and that the CBA intersects the retina at the temporal aspect of this region.

Effects of Monocular Enucleation at Different Stages of Development on the Uncrossed Retinocollicular Projection in the Opossum

Pouch young opossums aged from 5 to 34 days underwent unilateral eye enucleation and the projection from the remaining eye to the superior colliculus (SC) was explored at maturity by anatomical and physiological methods. The results were compared to data from normal or adult enucleated animals. Analysis of the experimental group showed that early enucleation resulted in an increased ipsilateral pathway which varied in terminal distribution with the timing of the lesion. When performed in the very young (first and second postnatal week) the uncrossed retinocollicular projection covered the entire area of the superficial layers of the superior colliculus but formed mediolateral bands of high and low label density at the rostral aspects of the SC. In the remainder of the early enucleated group the labeling also covered the entire area of the optic layers but the density of labeling was relatively homogeneous throughout the rostrocaudal extension of the SC. The distribution pattern of the uncrossed projection in adult enucleated opossums was similar to that described previously in normal animals. The electrophysiological results showed that, at all ages examined, early enucleation resulted in an orderly but expanded map in the SC restricted to the sector of the visual field seen by the temporal retina. The different anatomical patterns found in animals enucleated at these two early stages of development could not be distinguished by multiunit recordings.