The superior colliculus neurons which project to the dorsal and ventral lateral geniculate nuclei in the cat

Summary Cells in the cat superior colliculus which project to the ventral and dorsal lateral geniculate nuclei (VLG and DLG) have been labeled by retro-grade transport of horseradish peroxidase (HRP). We studied the depth, area, and morphology of each labeled neuron quantitatively. Our measurements show that the projection neurons to both VLG and DLG vary in laminar position, size, and morphology. Labeled cells projecting to both nuclei were concentrated within the superficial gray layer, but were also scattered through the optic layer and, after DLG injections, in the intermediate gray layer as well. Labeled cells in both groups varied greatly in size, ranging from 49–344 m² cross-sectional area (mean 143 m²) for the VLG group and from 31–398 m² (mean 165 m²) for the DLG group. The labeled cells also varied in morphology after both VLG and DLG injections. The majority had a granule or vertical fusiform morphology. There were fewer with a stellate morphology and almost none with a horizontal morphology. At least three types of superior colliculus cells thus appear to project to the ventral and dorsal lateral geniculate nuclei. These cell types likely give rise to distinct functional channels to these nuclei.Abbreviations A lamina A of the dorsal lateral geniculate nucleus - A1 lamina A1 of the dorsal lateral geniculate nucleus - C lamina C of the dorsal lateral geniculate nucleus - CM central medial nucleus - CMM medial mammillary nucleus - CP cerebral peduncle - D nucleus of Darkschewitsch - FCT central tegmental tract - H habenular nuclei - HPM medial habenulo-peduncular tract - LP lateral posterior nucleus - MG medial geniculate nucleus - MIN medial intralaminar nucleus - NCP nucleus of the posterior commissure - NR reticular nucleus - OT optic tract - P pulvinar nucleus - PC posterior commissure - R red nucleus - SG suprageniculate nucleus - SN substantia nigra - VLA ventral anterolateral nucleus - VLG ventral lateral geniculate nucleus - VPL ventral posterolateral nucleus - VPM ventral postero-medial nucleus This study was supported by USPHS Research Grant EY02973 from the National Eye Institute, a New Faculty Research Grant from the State of Tennessee, and USPHS Postdoctoral Training Grant GM-00202     

Rearrangements in the retino-geniculate projections of rats following ablation of the superior colliculus in infancy

Summary The superior colliculus was bilaterally or unilaterally ablated at different early postnatal ages in rats. When adult, each rat received a unilateral eye injection of Horesradish peroxidase to reveal the crossed and uncrossed retinal terminal fields within the dorsal lateral geniculate nucleus. Collicular ablation in the first seven days after birth, but not thereafter, produced a small hole or vacancy within the contralateral retinal terminal field which was occupied by an aberrant ipsilateral retinal terminal field. These rearrangements in the retino-geniculate projections occurred in the caudal quarter of the nucleus dorso-laterally just beneath the optic tract, solely ipsilateral to the ablated colliculus. Possible causes of the formation of these rearrangements are discussed, and similarities with other aberrant retinal projections following early damage to the visual system are considered.Abbreviations dLGN Dorsal geniculate nucleus - DTN Dorsal terminal nucleus of the accessory optic tract - HRP Horseradish peroxidase - LP Latero-posterior nucleus - NOT Nucleus of the optic tract - OT Optic tract - PO Olivary pretectal nucleus - PP Posterior pretectal nucleus - SC Superior colliculus - TMB Tetramethyl benzidine     

Effect of the superior colliculus on function of the contralateral lateral geniculate body in cats

Laboratory of Neurophysiology of Brain Integrative Activity and Section Brain and Behavior,, A. I. Karaev Institute of Physiology, Academy of Sciences of the Azerbaijan SSR, Baku. (Presented by Academician of the Academy of Medical Sciences of the USSR O. S. Adrianov.) Translated from Byulleten' Éksperimental'noi Biologii i Meditsiny, Vol. 111, No. 3, pp. 227–229, March, 1991.     

Retinal ganglion cells that project to the superior colliculus and pretectum in the macaque monkey

Horseradish peroxidase was injected into the superior colliculus or pretectum or both in order to label, by retrograde axoplasmic transport, the retinal ganglion whose cells axons innervate the dorsal midbrain. The dendrites of ganglion cells were sufficiently well-labelled to reveal their overall morphological characteristics. It was therefore possible to compare the number and form of ganglion cells projecting to the midbrain with the total population of ganglion cells as revealed by optic nerve injections, and with ganglion cells labelled by injections in the lateral geniculate nucleus. We found that not more than 10% of all retinal ganglion cells project to the superior colliculus in the macaque monkey. This percentage varies little over the retina, being about 6% of all ganglion cells near the fovea and increasing slightly with eccentricity. The superior colliculus does not receive a projection from P beta cells and only a few P alpha cells terminate there. The majority of cells which project to the superior colliculus have a small- to medium-sized cell body and sparsely branched dendritic tree. We have called them P gamma and P epsilon cells by analogy with the gamma cells and epsilon cells in the cat's retina. Anatomically the P gamma and P epsilon cells are heterogeneous, which would be consistent with the physiological heterogeneity found for ganglion cells which project to the midbrain in monkeys.     

Control of conduction of afferent impulses through the lateral geniculate body by the superior colliculus in conscious rabbits

A. I. Karaev Institute of Physiology, Academy of Sciences of the Azerbaidzhan SSR, Baku. Translated from Byulleten' Éksperimental'noi Biologii i Meditsiny, Vol. 108, No. 10, pp. 387–389, October, 1989.     

Ultrastructural identification of synaptic terminals from cortical axons and from collateral axons of geniculo-cortical relay cells in the perigeniculate nucleus of the cat

Summary Electron microscopic analysis of sections of the perigeniculate nucleus (PGN) of the cat processed with horseradish peroxidase (HRP) histochemistry after massive injections of this enzyme in the visual cortex showed two types of synaptic terminals labeled with HRP reaction products. One type (RLD terminals) is characterized by round synaptic vesicles, large size, dark mitochondria and asymmetrical synaptic contacts with somata and dendrites. The second type (RSD terminals) is characterized by round synaptic vesicles, small size, dark mitochondria and asymmetrical synaptic contacts with dendrites. The HRP + RSD terminals, which were also found in the dorsal lateral geniculate nucleus (LGN), are interpreted as terminals of cortical origin both in the PGN and LGN, since previous studies have identified cortical terminals as being of RSD type in the LGN and in other thalamic nuclei. The HRP + RLD terminals are interpreted as synaptic terminals of collaterals axons of geniculo-cortical relay cells in the PGN labeled by retrograde transport of HRP from the cortex. In addition, in semithin and ultrathin sections somata in the PGN were never found labeled with HRP products indicating the absence of a PGN projection to the visual cortex.     

The GABA-immunoreactive neurons in the interlaminar regions of the cat lateral geniculate nucleus: light and electron microscopic observations

Summary GABA-immunoreactive cells located in the interlaminar zone between the A and A1 laminae of cat LGN were studied at the LM and EM levels. The mean perikaryal size of these neurons was larger than that of GABA-immunoreactive cells in the A-laminae of LGN. Interlaminar GABA+ cells examined in plastic semithin sections of LGN after massive injections of HRP in the striate and extrastriate visual cortex were not retrogradely labeled with reaction products (as previously reported for the GABA+ cells in the laminar regions of LGN) suggesting that these cells do not project to the visual cortex. Serial EM analysis of two partially reconstructed interlaminar GABA+ cells showed that they receive synaptic inputs from RLD terminals of axon collaterals of geniculo-cortical relay cells, from cortical (RSD) terminals, from inhibitory (F) axon terminals, and from other undetermined terminals, but not from retinal (RLP) axon terminals. These data suggest that the GABAergic cells in the interlaminar zones of LGN participate as interneurons in recurrent inhibitory circuits in LGN. The synaptic inputs to these cells and ultrastructural features, notably somatic spines and dendrites oriented predominantly orthogonal to the projection lines in LGN, are similar to those of neurons of the perigeniculate nucleus.     

Relation of the parabigeminal nucleus to the superior colliculus and dorsal lateral geniculate nucleus in the hooded rat

Summary The retino-recipient layers of the superior colliculus project predominantly to the dorsal and ventral divisions of the ipsilateral parabigeminal nucleus, while receiving an input chiefly from the medial division of the contralateral nucleus. A variety of retrograde tracing techniques was used to confirm that there is a projection from the medial division of the parabigeminal nucleus to the contralateral dorsal lateral geniculate nucleus in normal adult hooded rats. Some parabigeminal cells branch to supply both dorsal lateral geniculate nucleus and retino-recipient layers of the superior colliculus.     

Delayed reduction in GABA and GAD immunoreactivity of neurons in the adult monkey dorsal lateral geniculate nucleus following monocular deprivation or enucleation

Summary GABA and glutamate decarboxylase (GAD) immunoreactivities were examined in dorsal lateral geniculate nuclei (LGN) of normal monkeys (Macaca fascicularis) and in monkeys that had one eye injected with tetrodotoxin (TTX) or one eye removed 5 days to 4 weeks prior to sacrifice. As seen in previous studies (Wong-Riley and Carroll 1984) monocular TTX injections or enucleation quickly reduced cytochrome oxidase (CO) staining in layers 2, 3 and 5 of the ipsilateral LGN and in layers 1,4 and 6 of the contralateral LGN. The reduction in CO staining was apparent at all survival times examined. By contrast, GABA and GAD immunostaining in the LGNs were qualitatively normal up to two weeks following enucleation or after 17 days of TTX injections. Quantitative and stereological analyses confirmed that the numerical density and proportion of GABA and GAD neurons do not change in the LGN following two weeks of denervation or deprivation, even though in the same monkeys a reduction in GABA immunostaining was found in deprived-eye columns of area 17. However, with longer survivals, of 3–4 weeks in duration, the number of GABA and GAD immunostained neurons in the deprived/denervated-eye laminae of the LGN was reduced by one-third. These findings demonstrate that the deprivation-induced reduction in GABA and GAD immunoreactivity is delayed in the LGN, by comparison with the visual cortex, and suggest that the effects in the LGN may be relayed through the cortex or that neurotransmitter levels may be regulated by different mechanisms in the two sites.     

The proportion and size of GABA-immunoreactive neurons in the magnocellular and parvocellular layers of the lateral geniculate nucleus of the rhesus monkey

Summary Neurons containing GABA-immunoreactivity in LGN of the macaque monkey were analyzed quantitatively in semithin (1 m) sections. The percentage of GABA(+) cells per unit area of the sections was 26% in the magnocellular layers and 19% in the parvocellular layers. However, the percentage of GABA(+) cells in a unit volume of LGN, calculated by a stereological method that takes into account the observed difference in size of labeled and unlabeled somata, was 35% in the magnocellular layers and 25% in the parvocellular layers. GABA(+) somata in the magnocellular layers were significantly larger than those in the parvocellular layers. The possible role of GABAergic cells in inhibitory mechanisms of receptive fields of parvo- and magnocellular neurons are discussed in the light of current knowledge of the physiology and neural circuits of macaque LGN.Supported by grants EY 02877 and HD 03352 from the National Institutes of Health     

Distribution of the tecto-thalamic projection neurons in the hereditary microphthalmic rat

Summary Tecto-thalamic projections in the hereditary bilaterally microphthalmic rat were studied by means of WGA-HRP injection into the dorsal lateral geniculate nucleus (LGNd) and the lateroposterior thalamic nucleus (LP). Histological study in the mutant rats showed that whereas LGNd and superficial layers of the superior colliculus (SC) suffered from a remarkable reduction in size, LP had no histological changes as compared to the normal animals. Unilateral injection of the tracer into the microphthalmic LGNd showed that WGA-HRP positive neurons were present mostly in the ipsilateral str. griseum superficiale (SGS) of the SC. However, the number of labeled SGS neurons of the microphthalmic animals was about 3% of the normal. Although cell bodies of the normal tecto-LGNd neurons in the SGS were spindle-form in shape and issued one or two proximal dendrites from each pole, the microphthalmic tecto-LGNd neurons showed an irregular contour and their dendrites were not so intensively labeled. Unilateral injections of WGA-HRP into the LP revealed that the tecto-LP neurons were mainly distributed in the ipsilateral str. opticum of the colliculus. (SO) in both normal and microphthalmic animals. However, the number of labeled SO cells in the microphthalmic rat was about one-half of the normal. Furthermore, the size of labeled tecto-LP neurons was smaller than that of the normal ones, and they showed irregular round to oval cell bodies with equivocally labeled dendrites, in contrast to the normal tecto-LP neurons with polygonal cell bodies extending three or more dendrites in a radial fashion. These results indicate that there exist the tecto-LGNd and -LP projection neurons in the microphthalmic rat and that their laminally segregated projection is fundamentally preserved. However, the number of the tecto-thalamic projection neurons, especially of the tecto-LGNd cells, was markedly diminished in the mutant tectum compared to normals.Abbreviations CST cortico-spinal tract - DRN dorsal raphe nucleus - DTN dorsal tegmental nucleus - LGNd pars dorsalis of the lateral geniculate nucleus - LLN nucleus of the lateral lemniscus - LM medial lemniscus - LP lateroposterior thalamic nucleus - MGN medial geniculate nucleus - MRF midbrain reticular formation - OT optic tract - P pretectal area - PAG periaqueductal gray - PB parabigeminal nucleus - PN pontine nuclei - PCS superior cerebellar peduncle - SGS superficial gray layer of the superior colliculus - SO stratum opticum of the superior colliculus - SN substantia nigra - Vm motor nucleus of the trigeminar nerve - Vs sensory nucleus of the trigeminar nerve     

Morphology of geniculocortical axons in turtles of the genera Pseudemys and Chrysemys

Summary An analysis has been made of the morphology of axons in the geniculocortical pathway of turtles using the anterograde transport of horseradish peroxidase in both in vivo and in vitro preparations. Following injections of HRP into the dorsolateral thalamus, labeled axons could be traced from the dorsal lateral geniculate complex to the telencephalon. They are unbranched and free of varicosities within the diencephalon. They travel in the dorsal peduncle of the lateral forebrain bundle, through the basal telencephalon and dorsally into the pallial thickening. Many axons are situated deep in the pallial thickening and bear numerous varicosities that often appear apposed to the proximal dendrites or somata of neurons retrogradely labeled by thalamic injections of horseradish peroxidase. Individual axons continue from the pallial thickening into the dorsal cortex where they shift dorsally and bear varicosities as they course from lateral to medial in the superficial third of layer 1. These data indicate that the terminal zone of the dorsal lateral geniculate complex within the telencephalon of turtles is more extensive in the mediolateral direction than previously believed. Geniculate axons bear varicosities both within the pallial thickening as well as the dorsal cortex, but have different relationships to potential postsynaptic elements in the two areas. Geniculocortical axons overlie somata and proximal dendrites of neurons in the pallial thickening, but intersect the distal dendrites of neurons in the dorsal cortex.     

Neocortical connections with perihippocampal and periamygdalar regions in the hedgehog tenrec

The perihippocampal fields represent the most important regions connecting the neocortex and the hippocampus in rat, cat and monkey but little is known about their presence and connectivity in species with poorly differentiated brain. Using axonal tracer substances we have recently studied the distribution of cortical cells projecting to the hippocampus in the hedgehog tenrec. In the present study we determined the regions of the paleocortex and the rhinal cortex connected with the neocortex, and provide a tentative view of the site and the extent of the tenrecs entorhinal, perirhinal and postrhinal/parahippocampal fields. It is shown that only the dorsal portions of the posterior rhinal cortex may be considered equivalent to the perirhinal and postrhinal fields of higher mammals, while a considerable expanse of the ventral rhinal cortex may be part of the entorhinal area (its so-called dorsal portion) connected with both the dentate gyrus and the neocortex. A few cells projecting to the neocortex were also noted in the dorsal-most portion of the three-layered paleocortex (ventral entorhinal portion). These cells were linearly arranged and reminiscent of the neocortical projecting cells in the entorhinal layer 4/5 in more differentiated mammals. The main portion of the paleocortex caudal to the corpus callosum remained unlabeled following neocortical and hippocampal tracer injections. Unexpectedly, the area in the most ventral paleocortex adjacent to the amygdala also projected to the neocortex, particularly the tenrecs somatosensorimotor cortex.Abbreviations Ay amygdala - BDA biotinylated dextran amine - CA cornu ammonis - Cbl cerebellum - cc corpus callosum - ERhD/V dorsal/ventral portion of entorhinal cortex - Et Echinops telfairi - Hip hippocampus - M cell group M - NCx neocortex - OfB olfactory bulb - PCx subrhinal paleocortex (D, I, P, V refer to dorsal, intermediate, posterior and ventral portions of PCx, the numbers to the zones involved) - pⁱ, p^m, p^s perikarya labeled in superficial (s) and intermediate (i) positions of PCx or the multiform (m) layer of RCx - ppc proportional prosencephalic coordinates - PRh perirhinal cortex (possibly including equivalents of the postrhinal cortex in more differentiated species) - PSbE presubiculum - RCx rhinal cortex (additional numbers refer to zones) - Sbi subiculum - Tu tuberculum olfactorium - XCx poorly characterized area caudally adjacent to RCx - WGA-HRP wheat germ agglutinin conjugated to horseradish peroxidase     

Ontogenesis of receptive field characteristics in the dorsal lateral geniculate nucleus of the rabbit

Summary The responses of rabbit dorsal lateral geniculate neurons to light or optic nerve shock were tested for 415 units in 43 rabbit pups 2–20 days of age. Units were driven by optic nerve shock at the youngest ages tested, but could not be driven by light until postnatal day six. Examples of each of the three prominent categories of receptive fields found in the adult were first observed at 8 days of age. Cells with receptive field properties not characteristic of the dorsal lateral geniculate nucleus of the adult were encountered until 17 days of age. The percentage of neurons with uniform and motion sensitive receptive fields approached adult levels soon after eye opening (11–12 days) but the percentage of cells with concentric receptive fields showed a steady increase throughout the neonatal period studied. The relevance of our data to the development of the visual response in the dorsal lateral geniculate nucleus and striate cortex is discussed.     

Effect of bilateral enucleation on the development of layers in the dorsal lateral geniculate nucleus

Previous results in tree shrew (Tupaia glis) have demonstrated that retinal afferents in the dorsal lateral geniculate nucleus segregate prenatally and that cell layers segregate postnatally (Brunso-Bechtold &Casagrande, 1980). In the present study, we examined the effect of bilateral enucleation at birth on the cytoarchitectural differentiation of these cell layers in the tree shrew lateral geniculate nucleus. The enucleated animals were killed at several postnatal ages up to maturity, their brains embedded in celloidin, and sections stained with thionin. The main result was that interlaminar spaces failed to form. Nevertheless, several cellular and cytoarchitectural features characteristic of normal layers were apparent; these included staining intensity, packing density and cell orientation.It can be concluded that the presence of retinal afferents appears necessary for the formation of interlaminar spaces in the lateral geniculate nucleus but not for the differentiation of all characteristics which define the layers.     

The effect of acetylcholine on the visual response of lagged cells in the cat dorsal lateral geniculate nucleus

We examined the influence of acetylcholine (ACh) on the visual response properties of lagged cells in the dorsal lateral geniculate nucleus of anaesthetised cats. By means of electrophysiological techniques, the response of single cells was recorded before, during and after ionophoretic application of ACh. ACh evoked a clear enhancement of the visual response. The initial suppression that a visual stimulus evokes in lagged cells was resistant to the effects of ACh. The characteristic anomalous response component of lagged cells was also present during application of ACh. The difference in latency to half-rise and to half-fall of the visual response that is found between lagged and non-lagged cells was maintained during application of ACh. Taken together, the results support previous evidence from experiments with brain stem stimulation that the fundamental visual response characteristics of lagged cells are state independent.     

The reciprocal connections of the suprageniculate nucleus and the superior colliculus in the rat

Reciprocally bilateral connections between the superior colliculus and the suprageniculate nucleus have been studied in the rat, using the anterograde and retrograde transport techniques of HRP. In those cases where the HRP deposit was restricted to the superficial layers of the colliculus, anterogradely labeled fibers and retrogradely labeled neurons were observed in the ipsilateral suprageniculate nucleus. However, upon HRP injection extended into the intermediate layers of the colliculus, the number of labeled fibers and neurons was not only increased ipsilaterally but were also observed in the contralateral suprageniculate nucleus. The density of the labeled fibers and the number of labeled neurons was always greater in the ipsilateral side. These results show that the suprageniculate nucleus and the superior colliculus are connected reciprocally and bilaterally, with an ipsilateral dominance.     

The study of Golgi stained cells and of experimental degeneration under the electron microscope: a direct method for the identification in the visual cortex of three successive links in a neuron chain.

A direct method is presented which makes it possible to identify, from synapse to synapse, three successive links of a neuron chain. The potentialities of the method are shown by examples of the termination of specific afferents in the visual cortex. Following unilateral lesion of the lateral geniculate nucleus in the rat, the distribution of degenerating geniculocortical boutons was studied on two Golgi-stained cells in layer IV of the primary visual cortex. One of the cells was definitely a small pyramidal cell; the other was identified as a spiny stellate (although the possibility that it too was a small pyramidal cell was not rigorously excluded). Both cells received monosynaptic input from the specific afferents as proved by the existence of degenerating boutons synapsing on their dendritic spines. The axonal arborizations of both Golgi-stained cells were traced at the electron microscopic level in thin section series in order to identify the postsynaptic structures contacted by their boutons. All boutons studied established asymmetrical contacts and about 50% of the synapses given by the impregnated boutons were found on smooth dendritic shafts of stellate cells, the rest on spines. The results obtained suggest a neuron circuit involving, successively, the visual afferents, spiny interneurons or monosynaptic visual target pyramidal cells and nonspiny stellate cells.It is suggested that a similar approach might provide direct information about the connectivity in neuron networks in many other parts of the central nervous system hitherto defying elucidation with conventional methods.     

Synaptogenesis in the dorsal lateral geniculate nucleus of the rat

Summary Synapse formation and maturation were examined in the rat dorsal lateral geniculate nucleus (dLGN) from birth to adulthood. Examination of animals, whose ages were closely spaced in time, showed that the maturation of the synaptic organization of the nucleus takes place chiefly during the first 3 weeks of postnatal life. This period of maturation may be divided into 3 broad stages. During the first stage, which spans the first 4 days of life, there are only a few immature synapses scattered throughout the nucleus; occasionally aggregates of 3 or 4 synapses are encountered. Dendrodendritic synapses first appear at the end of this stage. The second stage, which lasts from the end of the first stage through day 8, is characterized by intensive synaptogenesis as well as extensive growth and degeneration. For the first time, large boutons resembling retinal terminals form multiple synaptic contacts with dendrites and dendritic protrusions; these synaptic arrangements are partially covered by glial processes.A feature characteristic of the developing dLGN during the first 2 postnatal weeks, and particularly during the second stage, is the presence of membrane specializations that resemble vacant postsynaptic densities. These specializations, which may be unapposed or opposite another neuronal process, decrease in frequency as the number of synapses increases. It is not known whether these densities are converted to synapses or whether they result from loss of presynaptic elements.The third stage in the process of synaptogenesis, which spans a period between days 10 and 20, is characterized by myelination and by the diminution of growth cones, degenerating profiles and vacant postsynaptic densities. There is also a very significant increase in the number and maturation of synapses including synaptic glomeruli. However, it is not until the end of this stage that synapses appear qualitatively indistinguishable from synaptic arrangements identified in adult animals.     

Plasticity of relay neurons in dorsal lateral geniculate nucleus of the adult cat: Morphological evidence

Dendrites of relay neurons in the subcortical visual center (lateral geniculate nucleus) of adult cats develop presynaptic sites following chronic disconnection from the visual cortex. The capability of otherwise exclusively postsynaptic dendrites to be transformed into presynaptic dendrites indicates a remarkable plasticity of the relay cells. It is suggested that the ‘axonization’ of relay neuronal dendrites which enables the neuron to establish new synaptic connections in replacement of those lost in the cortex is a main factor in the survival of the axotomized nerve cell.