Development of commissural neurons in the wallaby (Macropus eugenii)

We have examined the development of the laminar and areal distribution of cortical commissural neurons in a marsupial mammal, the wallaby Macropus eugenii. In this species, commissural axons approach the major cerebral commissure, the anterior commissure, via either the internal capsule or the external capsule and first cross the midline at postnatal day 14 (P14). By retrogradely labelling these axons with 1,1′-dioctadecyl-3,3,3′,3′-tetramethylindocarbocyanine (DiI) at P15, we show here that the cell bodies of these neurons are restricted to a region of cortex adjacent to the rhinal fissure. Most of these labelled neurons are located in the compact cell zone of the cortical plate, with only a few labelled cells found in the zone of loosely packed cells deep to this layer. Over the subsequent 66 days, commissural neurons are found progressively more dorsally, rostrally, and caudally, so that, by P80, they are present throughout the extent of the neocortex. At this age, they are mainly pyramidal in morphology and form a single band within the deeper part of layer 5 of the developing cortex. From P80 to adulthood, the distribution of commissural neurons has been assessed in the visual cortex by using retrograde transport of horseradish peroxidase. At P80, labelled neurons with immature pyramidal morphology are present throughout the occipital cortex; as in DiI material, somata are located in deep layer 5. At P165, previously shown to be the age when commissural axon numbers peak, widespread labelling is present in the occipital region, with labelled cells now found in two bands corresponding to layers 3 and 5. After this age, neurons become more restricted in distribution, so that, by adulthood, commissural neurons are no longer apparent throughout area 17 but are restricted to a localised region around the area 17/18 boundary. Within this region, labelling is still present in layers 3 and 5 but is more dense in layer 3. The gradual restriction of commissural fields seen here in the wallaby is similar to that reported in the neocortex in many eutherians. These findings also support studies in eutheria, suggesting that subplate neurons do not appear to play a major role in commissural development. J. Comp. Neurol. 387:507–523, 1997. © 1997 Wiley-Liss, Inc.     

Retinotopic organization in the dorsal lateral geniculate nucleus of the tammar wallaby (Macropus eugenii)

Electrophysiological recordings were made from 187 single cells in the tammar wallaby (Macropus eugenii) dorsal lateral geniculate nucleus (LGNd). The results show that it is topographically organized such that the superior visual field is represented dorsally, the inferior field is represented ventrally, the nasal visual field is represented caudally, and the temporal visual field is represented rostrally. The visual field of one eye ranges from -30 degrees nasal to +179 degrees temporal in azimuth and +73 degrees superior to -49 degrees inferior in elevation. Ganglion cells that had receptive field positions between -9 degrees and +179 degrees projected to the contralateral LGNd while the ganglion cells that projected to the ipsilateral LGNd had visual fields from 0 to +30 degrees. The binocular visual field extends 60 degrees in azimuth. This representation in the LGNd is expanded relative to the monocular representation. There is also an increased representation of the horizon in the temporal field corresponding to the visual streak of retinal ganglion cells. The binocular visual field is located where contralateral and ipsilateral laminae are shown to interdigitate by proline autoradiography. There are nine eye-specific laminae in the LGNd. Four receive afferents from the contralateral eye and five receive afferents from the ipsilateral eye. The lines of isoelevation are perpendicular to the coronal plane of section while the lines of isoazimuth are nearly parallel to the coronal plane. The lines of projection representing one visual direction are inferred to be perpendicular to the tangent of curvature of the laminae as in the LGNd of other mammals. The majority of cells (85%) recorded had on- or off-centre responses. On- and off-centre responses were not apparently segregated in the LGNd but segregation may not have been revealed by the single-unit recording technique.     

Early development of the hypothalamus of a wallaby (Macropus eugenii)

We have studied the development of the hypothalamus of an Australian marsupial, the tammar wallaby (Macropus eugenii), to provide an initial anatomic framework for future research on the developing hypothalamus of diprotodontid metatheria. Cytoarchitectural (hematoxylin and eosin), immunohistochemical (CD 15 and growth associated protein, GAP-43), tritiated thymidine autoradiography, and carbocyanine dye tracing techniques were applied. Until 12 days after birth (P12), the developing hypothalamus consisted of mainly a ventricular germinal zone with a thin marginal layer, but by P25, most hypothalamic nuclei were well differentiated, indicating that the bulk of hypothalamic cytoarchitectural development occurs between P12 and P25. Strong CD 15 immunoreactivity was found in radial glial fibers in the rostral hypothalamus during early developmental ages, separating individual hypothalamic compartments. Immunoreactivity for GAP-43 was used to reveal developing fiber bundles. The medial forebrain bundle was apparent by P0, and the fornix appeared at P12. Tritiated thymidine autoradiography revealed lateral-to-medial and dorsal-to-ventral neurogenetic gradients similar to those seen in rodents. Dye tracing showed that projections to the posterior pituitary arose from the supraoptic nucleus at P5 and from the paraventricular nucleus at P10. Projections to the medulla were first found from the lateral hypothalamic area at P0 and paraventricular nucleus at P10. In conclusion, the pattern of development of the wallaby hypothalamus is broadly similar to that found in eutheria, with comparable neurogenetic compartments to those identified in rodents. Because most hypothalamic maturation takes place after birth, wallabies provide a useful model for experimentally manipulating the developing mammalian hypothalamus.     

The first thalamocortical synapses are made in the cortical plate in the developing visual cortex of the wallaby (Macropus eugenii)

The time course of development and laminar distribution of thalamocortical synapses in the visual cortex of the marsupial mammal the wallaby (Macropus eugenii) has been studied by electron microscopy from the time of afferent ingrowth to the appearance of layer 4, the main target for thalamic axons. Axons were labeled from the thalamus by a fluorescent carbocyanine dye in fixed tissue or by transneuronal transport of horseradish peroxidase conjugated to wheat germ agglutinin from the eye. Thalamic axons first reached the cortex 2 weeks after birth and grew into the developing cortical plate without a waiting period in the subplate. The first thalamocortical synapses were detected 2 weeks later solely throughout the loosely packed zone of the cortical plate, where layer 6 cells previously have been shown to reside. As the thickness of the cortex increased with age, thalamocortical synapses were increasingly prevalent in the loosely packed zone of the cortical plate. With the appearance of layer 4, thalamocortical synapses were found there as well as in the marginal zone and layer 6. There was no evidence for an early population of thalamocortical synapses in the subplate. The first synapses made by thalamic axons were in a region containing layer 6 cells, one of their normal targets in the mature cortex.     

Conduction and synaptic transmission in the optic nerve and the superior colliculus during development of the retinocollicular projection in the wallaby (Macropus eugenii)

When do the developing connections between mammalian retinal ganglion cells and the superior colliculus become functional? Evoked potentials elicited by optic nerve stimulation in the pouch young of the wallaby were used to answer the question. Up to 42 days after birth, the evoked potentials in the colliculus appeared to be generated by axon conduction. Synaptic activity was first recorded from the rostral colliculus at 45 days, and was found to be progressively more caudal, spreading to cover the colliculus, by 65 days. From the earliest indication of synaptic activity until eye opening at 140 days, current source density (CSD) analysis consistently showed the same basic pattern: an initial deep sink from synaptic activity of fast (Y type) fibres, and a more superficial longer-latency sink from slower (W type) fibres. All features became more clearly delineated with age. The indirect retinocorticocollicular connection appeared between 134 days and 146 days. The ability of optic nerve fibres to sustain action potentials precedes their formation of functional synapses with collicular neurons, which happens abruptly at three months before eye opening. CSD analysis showed that the relationship between the conduction velocity of optic nerve fibres and their depth of termination is evident from the first signs of synapse formation. J. Comp. Neurol. 380:472–484, 1997. © 1997 Wiley-Liss, Inc.     

Cytoarchitecture and visual field representation in area 17 of the tammar wallaby (Macropus eugenii).

Tritiated proline was injected into one eye in the tammar wallaby and transported label was studied in the cortex after transneuronal passage through the lateral geniculate nucleus. The autoradiographic label and cytoarchitecture were used to anatomically demarcate the borders of area 17. Electrophysiological recordings from single units were done to obtain a retinotopic map of area 17. Single units in area 17 were found to have orientation sensitivity comparable to those seen in placental mammals such as cat and monkey. They could also be classified as simple, complex, and hypercomplex cells. Changes in the cortical areal magnification factor with eccentricity were found to match the drop off in retinal ganglion cell density only along the vertical meridian representation. Along the horizontal meridian, the cortical magnification falls off significantly with eccentricity, whereas the ganglion cell density shows only a mild reduction. Thus central vision, especially the binocular segment, is heavily represented at the cost of the periphery.     

Postnatal development of primary visual projections in the tammar wallaby (Macropus eugenii)

The time course and pattern of retinal innervation of primary visual areas was traced in pouch-young wallabies. Tritiated proline was injected into one eye of animals ranging in age from 1 to 72 days after birth. These results are compared to the 11 primary visual areas found in the adult wallaby, seven of which receive binocular input while four are monocular. At birth retinal ganglion cell axons have not reached any visual areas. Two to 4 days after birth, all of the axons are crossing to the contralateral optic tract. Nine to 12 days after birth axons begin to invade the contralateral lateral geniculate nucleus, the superior colliculus, and the medial terminal nucleus. Twenty to 21 days after birth, ipsilateral axons invade the lateral geniculate nucleus and superior colliculus. The contralateral projection precedes the ipsilateral projection in all binocular visual areas. By 25 days, ipsilateral and contralateral afferents share common territory in the lateral geniculate nucleus; however, afferents from each eye are initially concentrated in appropriate areas. Between 52 and 72 days, afferents to the dorsal lateral geniculate nucleus are gradually segregated into nine terminal bands. Four are contralateral while five are ipsilateral. By 72 days, the ipsilateral component to the superior colliculus is clustered beneath the contralateral projection a deeper layer. Projections to four monocular visual areas--lateral posterior nucleus, dorsal terminal nucleus, lateral terminal nucleus, and nucleus of the optic tract--are established later than binocular visual areas, except the suprachiasmatic nucleus. The suprachiasmatic nucleus is the last to be bilaterally innervated even though it is situated closest to the optic chiasm. At the light microscope level a mature pattern of visual development is emerging by 72 days, although the eyes do not open until 140 days.     

Effects of very early monocular and binocular enucleation on primary visual centers in the tammar wallaby (Macropus eugenii)

The role of retinal afferents and their binocular interactions in the development of mammalian primary visual centers has been studied in the marsupial wallaby. Monocular and binocular enucleation was performed prior to any retinal innervation of the visual centers. After monocular enucleation retinal projections were traced by horseradish peroxidase histochemistry and compared with those in normal animals and those during development. The topography of retinal projections to the superior colliculus and the dorsal lateral geniculate nucleus after monocular enucleation was determined by making retinal lesions and tracing the remaining projections with horseradish peroxidase. The position and nature of the filling defects in terminal label were compared with controls with similarly placed lesions. The superior colliculus and dorsal lateral geniculate nucleus ipsilateral to the remaining eye were shrunken. Projections to the ipsilateral superior colliculus, ipsilateral accessory optic nuclei, and ipsilateral suprachiasmatic nucleus, although enlarged, never approached the density contralaterally, as was also the case during normal development. The expanded projection in the ipsilateral superior colliculus came primarily from temporal and ventral retina. In the dorsal lateral geniculate nucleus, terminal bands and cellular laminae, although not identical to normal, did develop. During normal development overlap of afferents from the two eyes occurs in the binocular region. The decrease in volume of the nucleus ipsilateral to the remaining eye after monocular enucleation suggests that the monocular region disappears in the absence of appropriate input and the binocular region survives. Contralaterally there was no decrease in volume, compatible with this idea. The topography of retinal projections supports this interpretation. It was normal contralaterally while ipsilaterally it was appropriate for the normal binocular region. There was an expansion of the projection along the lines of projection in what would normally be binocular regions of the nucleus, where retinal afferents failed to segregate in the absence of binocular competition. After binocular enucleation the alpha and beta segments of the dorsal lateral geniculate nucleus were still recognizable but cell-sparse zones were absent, as was the characteristic orientation of primary dendrites of geniculocortical cells. There are rigid developmental constraints operating on the innervation of territory by retinal afferents from the two eyes, and many features of the mature pattern arise without binocular interactions during development.     

Development of the olfactory system in a wallaby (Macropus eugenii)

We used carbocyanine dye tracing techniques in conjunction with hematoxylin and eosin staining, immunohistochemistry for GAP-43, and tritiated thymidine autoradiography to examine the development of the olfactory pathways in early pouch young tammar wallabies (Macropus eugenii). The overarching aim was to test the hypothesis that the olfactory system of newborn tammars is sufficiently mature at birth to contribute to the guidance of the pouch young to the nipple. Although GAP-43 immunoreactive fibers emerge from the olfactory epithelium and enter the olfactory bulb at birth, all other components of the olfactory pathway in newborn tammars are very immature at birth, postnatal day (P0). In particular, maturation of the vomeronasal organ and its projections to the accessory olfactory bulb appears to be delayed until P5 and the olfactory bulb is poorly differentiated until P12, with glomerular formation delayed until P25. The lateral olfactory tract is also very immature at birth with pioneer axons having penetrated only the most rostral portion of the piriform lobe. Interestingly, there were some early (P0) projections from the olfactory epithelium to the medial septal region and lamina terminalis (by the terminal nerve) and to olfactory tubercle and basal forebrain. The former of these is presumably serving the transfer of LHRH(+) neurons to the forebrain, as seen in eutherians, but neither of these very early pathways is sufficiently robust or connected to the more caudal neuraxis to play a role in nipple finding. Tritiated thymidine autoradiography confirmed that most piriform cortex pyramidal neurons are generated in the first week of life and are unlikely to be able to contribute to circuitry guiding the climb to the pouch. Our findings lead us to reject the hypothesis that olfactory projections contribute to guidance of the newborn tammar to the pouch and nipple. It appears far more likely that the trigeminal pathways play a significant role in this behavior because the central projections of the trigeminal nerve are more mature at birth in this marsupial.     

Mammalian motoneuron cell death: development of the lateral motor column of a wallaby (Macropus eugenii)

We have investigated the development of the lumbar lateral motor column of the tammar as a model of mammalian motoneuron cell death that is accessible to experimental manipulation. The tammar is an Australian marsupial, belonging to the subfamily of wallabies and kangaroos. After a gestational period of 26-28 days, the pup crawls to its mother's pouch using its forelimbs. The major morphometric events that shape the formation of the hindlimb occurred between 21 days gestation and birth. At birth the premuscle masses had divided and motor nerves had begun to penetrate the muscles of the thigh and shank. The period of motoneuron cell death was biphasic and occurred entirely postnatally. During phase I, between birth and 40 days, 59% of motoneurons were lost. Cell numbers then stabilised before falling a further 24%, to give an overall loss of 70%. Most of phase II cell loss occurred between 90 and 150 days. The possibility that a second period of motoneuron cell death may be a common feature of mammals is discussed.     

Cyto- and chemoarchitecture of the cortex of the tammar wallaby (Macropus eugenii): areal organization

We have examined the cyto- and chemoarchitecture of the isocortex of a diprotodontid marsupial, the tammar wallaby (Macropus eugenii), using Nissl staining in combination with enzyme histochemical (acetylcholinesterase - AChE, NADPH-diaphorase - NADPHd, cytochrome oxidase) and immunohistochemical (non-phosphorylated neurofilament - SMI-32) markers. The primary sensory cortex showed distinctive patterns of reactivity in cytochrome oxidase, acetylcholinesterase and NADPH diaphorase. For example, in AChE material, S1 showed a heterogeneous appearance, with regions exhibiting a double layer of AChE activity (layers II and IV) adjacent to poorly reactive regions. In NADPHd preparations, activity in S1 was strongest in layers I to IV although, as in AChE material, there were consistent patches of reduced NADPHd activity which corresponded to poorly reactive regions in the AChE sections. Each of the primary sensory areas of the isocortex showed a different pattern of distribution of SMI-32+ neurons. In V1, SMI-32+ neurons were distributed in two layers (III and V) throughout the tangential extent of that region. In S1, SMI-32+ neurons were concentrated in layer V, but large and discrete patches within S1 had additional SMI-32+ neurons in layer III. In primary auditory cortex there was a dense band of SMI-32+ neurons in layer V, with only occasional labeled pyramidal neurons in layer III. In the secondary sensory areas (V2 and S2) SMI-32+ neurons were either distributed in layers III and V (V2) or solely within layer V (S2). The tangential and laminar distribution of Type I reactive NADPH diaphorase neurons in the tammar wallaby cortex was more like that seen in eutheria than in polyprotodontid metatheria.     

Geometry of the projection of the visual field onto the superior colliculus of the wallaby (Macropus eugenii). II. Stability of the projection after prolonged rearing with rotational squint

At about the time of eye opening, one eye of seven tammar wallaby pouch young was surgically rotated about the optic axis by approximately 90°. In adulthood the projection of the visual field through the rotated eye onto the contralateral superior colliculus was mapped electrophysiologically. Although apparently distorted, the projection could be coherently rerotated mathematically to a reasonable copy of the normal projection from the opposite eye of the same animal, including details such as regional variations of the magnification factor. The same was true of three adult animals in which the eye rotation was done after anaesthesia immediately before the electrophysiological mapping. In animals in which the visual field seen through one eye, the other being normal, was rotated for the entire period of visual experience, there was no sign of compensation or rearrangement of the topographic map. Retinocollicular synaptic connections appear unmoved by such discordant visual experience.     

Development of connections to and from the visual cortex in the wallaby (Macropus eugenii)

The time course of the development of connections between the visual cortex and the main subcortical visual structures, as well as intrahemispheric and interhemispheric connections, has been studied in the marsupial wallaby (Macropus eugenii) to compare its development with that of placental mammals. Pouch young are born prior to retinal innervation of the primary visual centers and spend a protracted period of development in the pouch, making them ideal for visual, developmental studies. Horseradish peroxidase conjugated to wheatgerm agglutinin was injected into either the presumptive visual cortex or the superior colliculus in young of varying ages. Thalamocortical projections from the dorsal lateral geniculate and lateral posterior nuclei reach the presumptive visual cortex between 12 and 15 days after birth. Descending cortical connections form later. Corticogeniculate axons are first detected in the geniculate and lateral posterior nucleus at 48 days after birth, while corticocollicular axons first reach the superior colliculus at 71 days and, by 81 days, have innervated the superficial layers. Intrahemispheric and interhemispheric connections form even later. By 99 days intrahemispheric axons from area 17 have accumulated in visual association areas but are yet to invade layers III and IV, their major termination zones in adult, while axons projecting back to area 17 have also reached their target area. At this time interhemispheric axons from area 17 have begun to accumulate in the opposite visual cortex, although they have not invaded the cortical layers. By 111 days cortical cells projecting to the opposite visual cortex are first labelled. These have a more widespread distribution in area 17 at 111 and 122 days compared to the adult, where they are confined to the 17/18 border. The results show that the marsupial wallaby has a timetable of similar sequence, but different relative timing, in the formation of cortical connections compared to that of placental mammals. In the first half of the period between conception and eye opening, the timing in the wallaby precedes considerably that in placental mammals. Ascending connections from the thalamus develop relatively earlier in the wallaby but descending collicular connections are delayed until the same relative time that they appear in placental mammals.     

Development of the vestibular apparatus and central vestibular connections in a wallaby (Macropus eugenii)

We have studied the early development of the vestibular apparatus and its central connections in the tammar wallaby (Macropus eugenii) in order to determine whether the vestibular system anatomy is sufficiently mature at birth to assist in climbing to the pouch. Structural development was studied with the aid of hematoxylin and eosin stained sections and immunoreactivity for GAP-43, whereas the development of vestibular system connections was examined by carbocyanine dye tracing. At the time of birth, the otocyst has distinct utricle, saccule and semicircular canals with immature sensory regions receiving innervation by GAP-43 immunoreactive fibers. Vestibular nerve fibers can be traced into the brainstem to the developing vestibular nuclei, which are not yet cytoarchitectonically distinct. The vestibular nuclei do not contribute direct projections to the lower cervical spinal cord at birth; most bulbospinal projections in the newborn appear to be derived bilaterally from the gigantocellular, lateral paragigantocellular reticular and ventral medullary nuclei. A substantial bilateral projection to the vestibular ganglion and apparatus from the region of the gigantocellular and lateral paragigantocellular nuclei was seen at birth, but not in subsequent ages. This is similar to a projection seen in newborn Ameridelphians. By postnatal day (P) 5, the vestibular apparatus had extensive projections to all vestibular nuclei and neurons projecting in the lateral vestibulospinal tract could be identified in the lateral vestibular nucleus. Cytoarchitectonic differentiation of the vestibular nuclei proceeded over the next 3 to 4 weeks with the emergence of discrete parvicellular and magnocellular components of the medial vestibular nucleus by P19. GAP-43 immunoreactivity stayed high in the lateral vestibulospinal tract for several months after birth, suggesting that the development of this tract followed a prolonged timecourse. Our findings indicate that central and peripheral connections of the vestibular ganglion are present at birth, but that there is no direct projection from the vestibular nuclei to the cervical spinal cord until P5. Nevertheless, the possibility remains that an indirect projection between the vestibular nuclei and the medial reticular formation is present at birth and mediates control of the climb.     

Neurogenesis and identification of developing layers in the visual cortex of the wallaby (Macropus eugenii)

Birthdates of the neurons that comprise the layers of the mature visual cortex in the wallaby (Macropus eugenii) have been determined with the aid of tritiated thymidine autoradiography. The laminar positions of cells, identified by their birthdates, have then been followed at early stages during development and compared with previously published data on the distribution of thalamocortical afferents and corticothalamic projecting cells (Sheng et al. [1991] J. Comp. Neurol. 307:17-38). Neurons are born in a deep to superficial sequence typical of other mammals. The loosely packed zone of cells, which develops at the base of the thin compact zone of cells at the superficial margin of the cortical plate early in development, was identified as being part of the cortical plate. Afferents did not wait below this zone but grew into the developing cortical layers immediately after the cells that form these layers began accumulating in the loosely packed zone, starting with layer 6 on postnatal day 22 (P22). The genesis of layer 4 did not begin until P32, and these cells reached the superficial cortical plate at P54 and entered the loosely packed zone by P65. Cells of layers 5 and 6 formed the initial projection to the thalamus. Despite the protracted development of the wallaby and the large discrepancy between the time of thalamic ingrowth and genesis of layer 4, there was no extended waiting period for afferents in the subplate.     

Morphological development of afferent segregation and onset of synaptic transmission in the trigeminothalamic pathway of the wallaby (Macropus eugenii)

A light and electron microscopic study has been made of the time of formation of whisker-related patterns in trigeminothalamic afferents and the onset of synapse formation between afferents and cells in the ventroposteromedial nucleus (VPM) of the marsupial mammal, the wallaby, by labelling afferents with a carbocyanine dye. A parallel in vitro study was made of the functional development of the trigeminothalamic pathway to the VPM. Evoked synaptic responses could be recorded in the VPM from the time that afferents first reached the VPM at postnatal day 15 (P15). At all stages, the excitatory response comprised both N-methyl-D-aspartate- and non-N-methyl-D-aspartate-mediated components. At P40, the response decreased markedly in duration, coinciding with the onset of synaptogenesis. This implies that transmission is occurring prior to synapse formation, probably through transmitter release from growth cones. At P50, synaptic responses became dominated by a fast, non-N-methyl-D-aspartate potential, and this coincided with the first appearance of whisker-related patterns in the VPM. A gamma-aminobutyric acid (subtype A)-mediated, inhibitory component was also present from the time of afferent arrival. These findings support the idea that functional interactions between afferents and their targets may play a role in pattern formation in the somatosensory thalamus. J. Comp. Neurol. 399:47–60, 1998. © 1998 Wiley-Liss, Inc.     

Development of the brachial spinal cord in the marsupial Macropus eugenii (tammar wallaby).

The development of the brachial spinal cord was studied in the marsupial Macropus eugenii (tammar wallaby) on postnatal days 1-34. On day 1 the spinal cord was histologically immature, with a deep central canal, proliferating neuroepithelium and roof and floor plates. The lateral motor column had formed, and forelimb muscles contained primary myotubes. The spinal cord gradually attained a mature appearance between days 1-34. The results confirm the suitability of the wallaby spinal cord for studies of early mammalian development.     

Retinocollicular synaptogenesis and synaptic transmission during formation of the visual map in the superior colliculus of the wallaby (Macropus eugenii)

Spontaneous retinal activity has been implicated in the development of the topographic map in the superior colliculus (SC) but a direct demonstration that it reaches the colliculus is lacking. Here we investigate when the retinocollicular projection is capable of transmitting information from the retina in a marsupial mammal, the wallaby (Macropus eugenii). The projection develops postnatally, allowing in vivo analysis throughout development. Quantification of retinocollicular synaptogenesis has been combined with electrophysiology of the development and characteristics of retinocollicular transmission, including in vivo and in vitro recording in the same animals. Prior to postnatal day (P) 12-14 in vitro recording detected only presynaptic activity in retinal axons in the colliculus, in response to stimulation of the optic nerve. Postsynaptic responses, comprising both N-methyl-d-aspartate (NMDA) and non-NMDA responses, were first detected in vitro at P12-14 and retinal synapses were identified. In contrast, postsynaptic responses to optic nerve stimulation could not be detected in vivo until P39, around the time that retinal axons begin arborizing. Around this age density and numbers of total synapses began increasing in the retinorecipient layers of the colliculus. By P55-64, the numbers of retinal synapses had increased significantly and density and numbers of retinal and total synapses continued to increase up to P94-99. During this time the map is undergoing refinement and degenerating axons and synapses were present. The discrepancy between in vitro and in vivo onset of functional connections raises the question of when retinal activity reaches collicular cells in the intact, unanaesthetized animal and this will require investigation.     

Retinal projections to the superior colliculus and dorsal lateral geniculate nucleus in the tammar wallaby (Macropus eugenii): I. Normal topography

The topography of retinal projections to the superior colliculus and dorsal lateral geniculate nucleus of a wallaby, the tammar (Macropus eugenii), was investigated by an anatomical method. Small laser lesions were made in the retinas of experimental animals, and the remaining retinal projections were visualized by means of horseradish-peroxidase histochemistry. The position of each lesion was correlated with the position of the filling defects in the terminal label. The whole of the retina projects to the contralateral superior colliculus. The nasal retina is represented caudally, and the temporal retina rostrally. The ventral retina is represented medially, and the dorsal retina laterally. There is a projection to the ipsilateral superior colliculus, but it is patchy and its topography could not be determined by this method. The retinotopic map in the contralateral dorsal lateral geniculate nucleus has the nasal retina represented rostrally and the temporal retina caudally in the nucleus. The dorsal retina is represented ventrally, and the ventral retina is represented dorsally. It appears that the whole of the retina projects contralaterally, and in addition the temporal retina projects ipsilaterally. The maps of visual space through the two eyes were shown to be in topographic register in the binocular region by making a deposit of HRP in the visual cortex. This resulted in a column of retrogradely labeled cells in the nucleus. This column crossed the laminae, which are innervated by the ipsilateral and contralateral eye at right angles.     

Partition of function in the morphological subdivisions of the lateral geniculate nucleus of the tammar wallaby (Macropus eugenii).

Extra-cellular recordings from single cells in the dorsal lateral geniculate nucleus (dLGN) of the tammar wallaby, Macropus eugenii, were made to find out whether the stratification of the nucleus could be correlated with the receptive field properties of units. Retinofugal fibres terminate in the lateral geniculate nucleus of the wallaby in nine interleaved eye-specific layers. These may be grouped into a lateral alpha segment of six laminae and a medial beta segment of three, in which the cells are less densely packed. Ninety percent of the geniculate neurons recorded from in the alpha segment gave brisk responses to stimulation of their receptive fields. Cells with sluggish responses predominated in the beta segment, but there was also a sizable minority of cells with brisk responses that were indistinguishable from those recorded in the alpha segment. In contrast, other response properties were rarely differentiated in individual layers. Thus, in most layers, the numbers of cells with transient or sustained responses were not significantly different, and this was also true for cells with ON- or OFF- responses. For each of these response pairings, however, the numbers of one type (ON- and transient) predominated in every layer. The accumulation of this laminar distinction lead to significant differences in the alpha and beta segments and in the nucleus as a whole. We conclude that cells in the individual layers of the dLGN of the tammar wallaby show no evidence of having receptive field properties in common that might correlate with separate functional streams. There is a functional segregation of receptive field properties between the alpha and beta segments. The organization of these two segments resembles that of the A and the C layers of the dLGN in cats and, possibly, the magnocellular and koniocellular components of the dLGN in primates. These broad similarities in functional partition of the dLGN of different species suggests that this aspect of the organization of the nucleus is independent of lifestyle.