Striatal projections from the cat visual thalamus.

Anterograde transport methods reveal an extensive thalamostriate projection from the extrageniculate visual thalamus. These projections distribute to approximately the same regions of the striatum innervated by the corticostriate projections from over a dozen higher visual cortical areas [visual-recipient sector; Updyke, B.V. (1993) J. Comp. Neurol., 327, 159-193.]. Like their cortical counterparts, the thalamostriate projections to the caudate distribute in a patchy manner that suggests potential overlap or intermingling spatial relationships between the two major afferents. All of the visually related thalamic nuclei projecting to the striatum receive ascending signals from the superior colliculus, suggesting that the constraints placed upon tectal processing by striatonigral control have important consequences for central perceptuomotor processing at the striatal and cortical levels.

The visual-oculomotor striatum of the cat: functional relationship to the superior colliculus.

The visual-recipient sector of the cat striatum receives corticostriate input from over 15 higher visual and oculomotor-related areas of the cortex and appears homologous with the physiologically characterized region of mixed visual and oculomotor inputs within the primate caudate nucleus. This area in the cat involves the dorsolateral caudate and a strip of the caudal putamen. In a first series of experiments, the former was injected with a retrograde tracer in several cats. Thalamostriate cells were found in extensive regions, including the intralaminar nuclei, certain motor-related nuclei, and, most notably, across much of the extrageniculate visual thalamus. In another set of experiments, anterograde tracers were also injected into the superior colliculus (SC), and labeled tectothalamic fibers were observed in all thalamic sites projecting to the visual-recipient striatum. These findings highlight for the first time the need for the SC to be considered in models of thalamostriate and visual/oculomotor-striatal function(s). Moreover, the data bring to light the fact that basal-ganglia outflow reaching the SC via striatonigro-nigrotectal circuitry is well positioned to modulate ascending tecto-thalamic-thalamostriatal signals destined for the visual-recipient striatum.

Corticocortical communication via the thalamus: ultrastructural studies of corticothalamic projections from area 17 to the lateral posterior nucleus of the cat and inferior pulvinar nucleus of the owl monkey.

Electron microscopic anterograde autoradiography has been used to analyze the morphology and postsynaptic relationships of area 17 cortical terminals in the lateral division of the lateral posterior nucleus (LPl) of the cat and medial division of the inferior pulvinar nucleus (IPm) of the owl monkey. Such terminals are thought to arise exclusively from layer 5 in the cat and primate (Lund et al. [1975] J. Comp. Neurol. 164:287-304; Abramson and Chalupa [1985] Neuroscience 15:81-95). All labeled terminals in both nuclei exhibited the morphology of ascending "lemniscal" afferents. That is, they contained round vesicles, were large, made asymmetrical synaptic and filamentous nonsynaptic contacts, and were classified as RLs. These cortical RLs also exhibited the postsynaptic relationships of lemniscal afferents. Thus, they were presynaptic to large dendrites within glial encapsulated glomeruli, where a majority was involved in complex synaptic arrangements called triads. They also were found adjacent to terminal profiles with pleomorphic vesicles but never adjacent to small terminals containing round vesicles. Our results suggest that the layer 5 projection from area 17 provides a functional "drive" for some LPl and IPm neurons. Information carried over this "re-entrant" pathway (Guillery [1995] J. Anat. 187:583-592) could be modified within the LPl and IPm by both cortical and subcortical pathways and subsequently conveyed to higher visual cortical areas, where it could be integrated with messages carried through the well-documented corticocortical pathways (Casagrande and Kaas [1994] Cerebral cortex New York: Plenum Press).

Cortical somatosensory and trigeminal inputs to the cat superior colliculus: light and electron microscopic analyses.

Two different axonal transport tracers were used in single animals to test the hypothesis that the expansive intermediate gray layer of the cat superior colliculus (stratum griseum intermediale, SGI) is composed of sensorimotor domains. The results show that two sensory pathways, the trigeminotectal and the corticotectal arising from the fourth somatosensory area, commingle in patches across the middle tier of the SGI. Furthermore, the data reveal that tectospinal cells are distributed within these patches. Taken together, these results show a commingling of functionally related afferents and a consistent spatial relationship between these afferents and tectospinal neurons. These relationships indicate that the SGI consists of domains that can be distinguished by their unique combinations of afferent and efferent connections. The ultrastructural characteristics and synaptic relationships of these somatosensory afferent pathways suggest that they have distinct roles within the sensorimotor domain of the SGI. The trigeminotectal terminals are relatively small, contain round vesicles and make asymmetrical synapses on small, presumably distal, dendrites. We submit that these trigeminal terminals bestow the basic receptive field properties upon SGI neurons. In contrast, the somatosensory corticotectal terminals are relatively large, contain round vesicles, make asymmetrical synapses, participate in triads, and are presynaptic to proximal dendrites. We suggest that these cortical terminals bestow integrative abilities on SGI neurons.

Ultrastructural studies of the primate lateral geniculate nucleus: morphology and spatial relationships of axon terminals arising from the retina, visual cortex (area 17), superior colliculus, parabigeminal nucleus, and pretectum of Galago crassicaudatus.

The electron microscopic autoradiographic tracing method has been used to examine the morphology and postsynaptic relationships of five projections (retina, cortical area 17, superior colliculus (tectal), parabigeminal nucleus, and pretectum) to the dorsal lateral geniculate nucleus of the greater bush baby Galago crassicaudatus. Retinal terminals have been examined in the contralaterally innervated layer of each of the three matched pairs [parvi- (X-cell), magno- (Y-cell), and koniocellular (small, W-cell)] of geniculate layers. These terminals are large and contain pale mitochondria and round vesicles (RLPs). RLPs are presynaptic to juxtasomatic regions of parvi- and magnocellular neurons. In contrast, RLPs innervate more distal regions of koniocellular neurons. Labeled cortical, tectal, and parabigeminal terminals are relatively small and contain round vesicles and dark mitochondria. Cortical terminals in each of the three representative layers are presynaptic to small diameter dendrites. No convergence of cortical and retinal terminals has been seen in any layer. Labeled tectal and parabigeminal terminals are found primarily in the koniocellular layers, but the latter are also seen in all other layers. Tectal and parabigeminal terminals have been observed converging with retinal terminals on dendrites of some koniocellular neurons. Labeled pretectogeniculate terminals contain densely packed pleomorphic vesicles, dark mitochondria, and a dark cytoplasmic matrix. These terminals, which are present in each of the representative layers, are presynaptic to conventional dendrites and profiles containing loosely dispersed pleomorphic vesicles and a pale cytoplasmic matrix.

Ultrastructural studies of the primate parabigeminal nucleus: electron microscopic autoradiographic analysis of the tectoparabigeminal projection in Galago crassicaudatus.

The normal ultrastructure of the parabigeminal nucleus and the morphology and synaptic relationships of tectoparabigeminal terminals have been examined. Five different morphological types of terminals have been observed within the parabigeminal nucleus. Three of these profiles contain round vesicles and make asymmetrical synapses, while two contain pleomorphic vesicles and make symmetrical synapses. Electron microscopic autoradiographic data indicate that labeled tectoparabigeminal terminals represent only one of the three profiles containing round vesicles. Such terminals are primarily presynaptic to dendritic shafts, and several labeled profiles have been observed presynaptic to the same dendrite.

Corticotectal projections in the cat: anterograde transport studies of twenty-five cortical areas.

Retrograde transport studies have shown that widespread areas of the cerebral cortex project upon the superior colliculus. In order to explore the organization of these extensive projections, the anterograde autoradiographic method has been used to reveal the distribution and pattern of corticotectal projections arising from 25 cortical areas. In the majority of experiments, electrophysiological recording methods were used to characterize the visual representation and cortical area prior to injection of the tracer. Our findings reveal that seventeen of the 25 cortical areas project upon some portion of the superficial layers (stratum zonale, stratum griseum superficiale, and stratum opticum, SO). These cortical regions include areas 17, 18, 19, 20a, 20b, 21a, 21b, posterior suprasylvian area (PS), ventral lateral suprasylvian area (VLS), posteromedial lateral suprasylvian area (PMLS), anteromedial lateral suprasylvian area (AMLS), anterolateral lateral suprasylvian area (ALLS), posterolateral lateral suprasylvian area (PLLS), dorsolateral lateral suprasyvian area (DLS), periauditory cortex, cingulate cortex, and the visual portion of the anterior ectosylvian sulcus. While some of these corticotectal projections target all superficial laminae and sublaminae, others are more discretely organized in their laminar-sublaminar distribution. Only the corticotectal projections arising from areas 17 and 18 are exclusively related to the superficial layers. The remaining 15 pathways innervate both the superficial and intermediate and/or deep layers. The large intermediate gray layer (stratum griseum intermedium; SGI) receives projections from almost every cortical area; only areas 17 and 18 do not project ventral to SO. All corticotectal projections to SGI vary in their sublaminar distribution and in their specific pattern of termination. The majority of these projections are periodic, or patchy, and there are elaborate (double tier, bridges, or streamers) modes of distribution. We have attempted to place these findings into a conceptual framework that emphasizes that the SGI consists of sensory and motor domains, both of which contain a mosaic of connectionally distinct afferent compartments (Illing and Graybiel, '85, Neuroscience 14:455-482; Harting and Van Lieshout, '91, J. Comp. Neurol. 305:543-558). Corticotectal projections to the layers ventral to SGI, (stratum album intermediale, stratum griseum profundum, and stratum album profundum) arise from thirteen cortical areas. While an organizational plan of these deeper projections is not readily apparent, the distribution of several corticotectal inputs reveals some connectional parcellation.

Ultrastructural studies of retinal, visual cortical (area 17), and parabigeminal terminals within the superior colliculus of Galago crassicaudatus.

The morphology and synaptic relationships of anterogradely labeled retinal, visual cortical (area 17), and parabigeminal terminals have been analyzed within the superficial gray (stratum griseum superficiale) of Galago crassicaudatus. Our data regarding the retinocollicular projection reveal two populations of terminals based upon size. The population of smaller terminals are found in clusters, while the larger occur in isolation. Both populations of retinocollicular terminals form synapses primarily with dendritic spines, but synapses upon pale vesicle filled (PVF) profiles and dendritic shafts also occur. Corticotectal terminals contain round vesicles and make asymmetrical synapses, primarily onto dendritic spines; few form synapses with PVF profiles. Our findings suggest the possibility that there are two populations of corticotectal terminals based upon differences in size and morphology. Parabigeminotectal profiles contain densely packed round vesicles and make asymmetrical synapses. These terminals, which are exclusively cholinergic in Galago, are presynaptic to dendrites of various sizes. Convergence of retinal and cortical terminals has been observed. This convergence occurs on distinctly separate regions of the postsynaptic membrane. In contrast, convergence of retinal and parabigeminal terminals occurs on the same region of the postsynaptic cell(s).

Connectional studies of the primate lateral geniculate nucleus: distribution of axons arising from the thalamic reticular nucleus of Galago crassicaudatus.

Anterograde and retrograde transport methods have been used to explore the interconnections between the thalamic reticular nucleus (TRN) and the dorsal lateral geniculate nucleus of Galago crassicaudatus. We first defined the region of the TRN, which is connected to the lateral geniculate nucleus, by examining the distribution of geniculo-TRN axons, cortico-TRN axons arising from area 17, and the location of TRN-geniculate neurons. Following an intraocular injection of 3H-proline/3 H-leucine, trans-synaptically transported protein is present bilaterally within the lateral portion of the caudal TRN. This same caudal and lateral region is also targeted by cortico-TRN axons and contains neurons which project upon the lateral geniculate nucleus. Light microscopic anterograde transport methods were used to analyze the distribution of TRN-geniculate axons. Our data reveal that all layers and interlaminar zones of the dorsal lateral geniculate nucleus contain TRN axons. Electron microscopic-autoradiographic data support and extend our light microscopic findings by revealing labeled TRN terminals within all geniculate layers. These TRN profiles are the same size throughout the geniculate and exhibit morphological characteristics similar to F1 terminals described by others. That is, they possess predominantly pleomorphic vesicles, a dark cytoplasmic matrix, dark mitochondria, and symmetrical synaptic contacts. Two additional features of TRN terminals have been observed in some profiles. These include dense-core vesicles and a dense, punctate cytoplasmic matrix, which is sometimes associated with the postsynaptic specialization. In addition to their morphology and size, the postsynaptic targets of TRN terminals are similar within the three sets (parvi-, magno-, and koniocellular) of geniculate layers. TRN profiles terminate upon dendrites of all sizes and somata. These findings suggest that the TRN modulates the retino-geniculocortical pathway and that this modulation is occurring in all three streams.

Spatial relationships of axons arising from the substantia nigra, spinal trigeminal nucleus, and pedunculopontine tegmental nucleus within the intermediate gray of the cat superior colliculus.

We have utilized two different anterograde transport methods (Phaseolus vulgaris leucoagglutinin [PHA-L] immunocytochemistry and autoradiography) in the same experiment to compare the sublaminar location and arrangement of tectopetal axons arising from the substantia nigra pars reticulata, the spinal trigeminal nucleus, and the pedunculopontine tegmental nucleus. Our findings reveal that the nigrotectal projection terminates in a patchy fashion within three horizontally oriented sublaminae of the stratum griseum superficiale (SGI), the dorsal, middle and ventral. The middle tier of nigrotectal axons exhibits an exquisite, puzzle-like, complementary spatial relationship with trigeminotectal axons. In contrast, axons arising from the pedunculopontine tegmental nucleus overlap with patches of nigrotectal axons within the middle tier. Thus the middle tier of the SGI consists of domains of overlapping nigral and pedunculopontine tegmental inputs which interdigitate with domains rich in somatosensory inputs.

The parabigeminogeniculate projection: connectional studies in eight mammals.

Anterograde and retrograde tracing methods have been used to analyze the origin and distribution of parabigeminogeniculate axons in the gray squirrel, the gopher, the rat, the opossum, the cat, the greater bushbaby, the squirrel monkey and the macaque monkey. Our findings reveal that parabigeminogeniculate axons most heavily innervate regions of the lateral geniculate that are also targeted by axons arising from the superior colliculus (tectogeniculate). These geniculate layers and zones of parabigeminal and tectal overlap contain small cells, and in several species are associated with the small W cell retino-geniculocortical pathway. In addition to the dense input to small-celled layers and zones, parabigeminal axons in several species also innervate regions of the lateral geniculate nucleus that are relatively free of tectogeniculate axons and that are associated with the medium (X) and large (Y) cell streams. Finally, our data reveal that the laterality of parabigeminogeniculate pathways varies across mammals, being primarily crossed in the gray squirrel, the gopher, the rat, and the opossum, bilateral in the cat, and primarily ipsilateral in the three primates.

Projection of the mammalian superior colliculus upon the dorsal lateral geniculate nucleus: organization of tectogeniculate pathways in nineteen species.

Anterograde and retrograde transport methods have been used to analyze the projection of the superior colliculus upon the dorsal lateral geniculate nucleus in 19 mammalian species. Our retrograde findings reveal that tectogeniculate neurons are relatively small, and lie dorsally within the superficial gray. These small tectogeniculate neurons are spatially related to a dense tier of W-cell retinal input. Our anterograde tracing results show that tectogeniculate axons are visuotopically distributed to small-celled regions of the lateral geniculate in all nineteen species. In the majority of these species, the small-celled, tectally innervated regions of the lateral geniculate lie adjacent to the optic tract and contain W-cell-like neurons. Our findings suggest that neuroanatomical demonstration of the tectogeniculate projection is a relatively simple and straightforward way of revealing regions of the lateral geniculate which contain W-cells. This is true even in species in which the lateral geniculate lacks obvious cellular laminae, and in regions of the lateral geniculate where W-cells are few in number. The present data are especially interesting in light of the cortical projections of tectally innervated, small-celled regions of the lateral geniculate to the patches or puffs within layer III of area 17. Since these regions of small-celled geniculocortical axons are co-extensive with zones ("blobs") rich in cytochrome oxidase, it might be that information carried over the tectogeniculate circuitry plays an important role in the functions of the blob system.

Nigrotectal projections in the primate Galago crassicaudatus.

The pattern of the nigrotectal projection in Galago crassicaudatus was determined using retrograde and anterograde transport methods. These experiments revealed that pars reticulata and pars lateralis of the substantia nigra project to all layers of the ipsilateral and contralateral superior colliculus, except to layer I. The nigrotectal projection is not homogeneous, but is concentrated in particular collicular layers and sublayers, and the intensity and laminar distribution of the projection varies along the rostral-caudal dimension of the superior colliculus. The ipsilateral and contralateral nigrotectal projections are generally similar, except that a tier of dense label which is prominent in the ventral part of much of the ipsilateral layer IV is not obvious contralaterally; moreover, the contralateral projection is much sparser than the ipsilateral. Deposits of tracers at different medial-lateral locations within the substantia nigra did not result in different laminar patterns of anterogradely transported label in the superior colliculus. Based on the known connections and functions of the collicular layers and sublayers, the pattern and distribution of the nigrotectal projection suggests that the substantia nigra may use this pathway to gain access to particular components of vision- and visuomotor-related networks.

Neuroanatomical studies of the nigrotectal projection in the cat.

We have used retrograde and anterograde transport methods to analyze the nigrotectal projection in the cat. This projection arises from both pars reticulata (SNr) and pars lateralis (SNl) and distributes to all cellular laminae of the superior colliculus. This extensive nigrotectal innervation is not a simple, single circuit. Rather it appears to consist of several parallel channels, with each taking origin from a particular zone of the substantia nigra and terminating within specific collicular laminae and/or sublaminae. For instance, only neurons within the SNl project to the stratum griseum superficiale; such neurons also project diffusely to all other tectal laminae. Cells in the most lateral portion of the SNr project to a horizontal, patchy tier in the interface region between the stratum opticum and the stratum griseum intermediate (SGI). Finally, more medially placed neurons within the SNr project to a horizontal patchy tier within the middle of the SGI and to a wedge-shaped locus in the stratum griseum profundum. Our findings provide an anatomical substrate for electrophysiological data (Karabelas and Moschovakis: J. Comp. Neurol. 239: 309-329, '85) showing a widespread distribution of nigrorecipient tectal neurons in the cat.

Projections from the parabigeminal nucleus to the dorsal lateral geniculate nucleus in the tree shrew Tupaia glis.

The parabigeminal nucleus receives its major input from the superficial layers of the superior colliculus via the tectoparabigeminal projection. An extensive reciprocal parabigeminotectal pathway has also been observed. This close connectional association between the superficial gray and the parabigeminal nucleus is reflected in the collicularlike response characteristics of parabigeminal neurons (see Sherk: Brain Res. 145:375-379, '78, J. Neurophysiol. 42:1640-1655, 1656-1668, '79a,b, for review). Further documentation of the connectional relationship between the superior colliculus and the parabigeminal nucleus comes from the present data. Thus, our retrograde and anterograde transport findings reveal an extensive projection from the parabigeminal nucleus to layers 3 and 6 and several interlaminar zones of the contralateral dorsal lateral geniculate nucleus. These same layers and interlaminar zones receive tectogeniculate axons and have been shown to contain small cells that project to layers 1 and 3 of area 17. In addition to the distribution of parabigeminal axons to tectally innervated, small-celled zones, considerable parabigeminal input also reaches layers 1 and 5 of the tree shrew lateral geniculate nucleus. Each of these layers is the ipsilaterally (i.e., retinal) innervated component of a matched pair (layers 1 and 2 are considered magnocellular, while 4 and 5 are parvicellular), and it has been shown that layer 1 projects to lamina IVa of area 17, while layer 5 projects to lamina IVB. When the total distribution of parabigeminogeniculate axons is considered, it is apparent that the cells of origin of each of the major (small-celled, parvi- and magnocellular) geniculocortical channels receives parabigeminal input. Such an extensive distribution of parabigeminal axons within the lateral geniculate nucleus suggests that the information they convey might play an important role in geniculocortical function(s).

Laminar distribution of tectal, parabigeminal and pretectal inputs to the primate dorsal lateral geniculate nucleus: connectional studies in Galago crassicaudatus.

We have studied the distribution of 3 extraretinal, subcortical inputs to the dorsal lateral geniculate nucleus of the prosimian primate Galago. Our connectional findings reveal that axons arising from the superior colliculus and the parabigeminal nucleus influence the W-cell system via their innervation of the two small-celled geniculate laminae (internal and external koniocellular) and the interlaminar zones; parabigeminal axons also innervate each of the 4 non-tectally innervated layers. Pretectal axons, on the other hand, distribute mainly to the parvocellular laminae and thus influence primarily the X-cell system.

Hypothalamic and ventral thalamic projections to the superior colliculus in the cat.

The present report describes the organization of collicular afferents that arise within either the hypothalamus or the ventral thalamus. Following the placement of large injections of WGA-HRP into the superior colliculus of the cat, retrogradely labeled neurons are located within the reticular nucleus of the thalamus, the zona incerta, the fields of Forel, and throughout the hypothalamus. Although the dorsal hypothalamic area contains the largest number of labeled hypothalamic neurons, labeled cells are also found within the periventricular, paraventricular, dorsomedial, ventromedial, posterior, lateral, and anterior hypothalamic nuclei. A strikingly similar pattern of distribution of labeled neurons is also observed following placement of small injections of WGA-HRP that are restricted within the stratum griseum intermedium (SGI). In contrast, hypothalamic and ventral thalamic labeling is not seen after placement of injections within the stratum griseum superficiale. Following the placement of injections of tritiated anterograde tracers within the dorsal hypothalamic area, transported label is organized in two bands of clusters over the SGI. When injections of tritiated tracers are placed within the zona incerta, terminal label is also located over the SGI; however, the distribution of silver grains does not appear as clusters or distinct puffs. On the basis of the comparison of the cellular types that give rise to these projections and the differences in terminal distribution, we suggest that the hypothalamic and ventral thalamic projections to the superior colliculus are totally separate and unrelated pathways. The functional implications of the hypothalamotectal pathway are also discussed.

The trigemino-olivary projection in the cat: contributions of individual subnuclei.

Anterograde autoradiographic methods were used to determine the projection of the principal sensory trigeminal nucleus and of each of the three spinal trigeminal subnuclei to the inferior olivary complex in the cat. Our data reveal that the principal sensory trigeminal nucleus does not contribute to the trigemino-olivary pathway. Each spinal trigeminal subnucleus has a unique contribution to this pathway: pars oralis projects sparsely to the border between the dorsal accessory and principal olives (DAO-PO), pars interpolaris projects mostly to the rostral medial DAO, and pars caudalis projects mostly to the rostral medial part of the ventral leaf of PO and slightly to the caudal medial accessory olive. In the light of recent physiological and anatomical findings, our data indicate that information from each spinal trigeminal subnucleus reaches a different segment of the contralateral inferior olivary complex, which in turn distributes differentially to the cerebellar cortex.

Transient tectogeniculate projections in neonatal kittens: an autoradiographic study.

By using anterograde transport autoradiography, the present experiments demonstrated that the pattern of tectogeniculate projections in young (birth-14 postnatal days) kittens is strikingly different from that present in adult cats. Rather than being confined to the ventral C laminae, the neonatal projection extended across all layers of the lateral geniculate nucleus. This projection, like that in the adult cat, originates from cells in superficial laminae and is visuotopically organized. Thus, labeling only a portion of the superior colliculus with tritiated leucine produced a topographically appropriate strip of labeling in the ipsilateral lateral geniculate nucleus that encompassed all laminae and was especially dense in all interlaminar zones. Transported label also invaded the medial interlaminar nucleus (MIN). The loss of tectogeniculate projections in the neonate from MIN and the dorsal laminae and interlaminar zones of the lateral geniculate nucleus does not appear to begin until 1-2 weeks postnatal. Once initiated, however, the process is nearly completed by 21 days postnatal. It is not yet known whether the loss of these "anomalous" projections is due to the pruning of axonal collaterals, cell death, or a combination of the two processes. However, by comparing these data with those from other laboratories, it does appear that the loss of tectogeniculate projections depends on the presence of the two eyes and may reflect the differential laminar distribution of W-, X-, and Y-cell types. The protracted postnatal anatomical maturation of tectogeniculate projections differs substantially from the earlier maturing patterns apparent in all other tectofugal pathways.

Subcortical connections of area 17 in the tree shrew: an autoradiographic analysis.

The present anterograde autoradiographic study reveals several targets of the striate cortex (area 17) of the tree shrew which were not previously observed in studies which used anterograde degeneration methods; our data also confirm several previous findings. The results are discussed in the context of these projections modulating ascending visual information (claustrum, lateral intermediate nucleus, pulvinar, dorsal lateral geniculate, cells of the external medullary lamina, reticular nucleus of the thalamus, superficial collicular layers, and the anterior and posterior pretectal nuclei) or visuomotor information (putamen, caudate, ventral lateral geniculate, pontine gray, and the anterior and posterior pretectal nuclei).