Distribution and Morphology of Cortical Terminals in the Cat Thalamus from the Anterior Ectosylvian Sulcus.

Two main types of cortical terminals have been identified in the cat thalamus. Large (type II) have been proposed to drive the response properties of thalamic cells while smaller (type I) are believed to modulate those properties. Among the cat's visual cortical areas, the anterior ectosylvian visual area (AEV) is considered as one of the highest areas in the hierarchical organization of the visual system. Whereas the connections from the AEV to the thalamus have been recognized, their nature (type I or II) is presently not known. In this study, we assessed and compared the relative contribution of type I and type II inputs to thalamic nuclei originating from the AEV. The anterograde tracer BDA was injected in the AEV of five animals. Results show that (1) both type I and II terminals from AEV are present in the Lateral Posterior- Pulvinar complex, the lateral median suprageniculate complex and the medial and dorsal geniculate nuclei (2) type I terminals significantly outnumber the type II terminals in almost all nuclei studied. Our results indicate that neurons in the AEV are more likely to modulate response properties in the thalamus rather than to determine basic organization of receptive fields of thalamic cells.

Principal component and cluster analysis of layer V pyramidal cells in visual and non-visual cortical areas projecting to the primary visual cortex of the mouse.

The long-distance corticocortical connections between visual and nonvisual sensory areas that arise from pyramidal neurons located within layer V can be considered as a subpopulation of feedback connections. The purpose of the present study is to determine if layer V pyramidal neurons from visual and nonvisual sensory cortical areas that project onto the visual cortex (V1) constitute a homogeneous population of cells. Additionally, we ask whether dendritic arborization relates to the target, the sensory modality, the hierarchical level, or laterality of the source cortical area. Complete 3D reconstructions of dendritic arbors of retrogradely labeled layer V pyramidal neurons were performed for neurons of the primary auditory (A1) and somatosensory (S1) cortices and from the lateral (V2L) and medial (V2M) parts of the secondary visual cortices of both hemispheres. The morphological parameters extracted from these reconstructions were subjected to principal component analysis (PCA) and cluster analysis. The PCA showed that neurons are distributed within a continuous range of morphologies and do not form discrete groups. Nevertheless, the cluster analysis defines neuronal groups that share similar features. Each cortical area includes neurons belonging to several clusters. We suggest that layer V feedback connections within a single cortical area comprise several cell types.

Indirect pathway between the primary auditory and visual cortices through layer V pyramidal neurons in V2L in mouse and the effects of bilateral enucleation.

Visual cortical areas are activated by auditory stimuli in blind mice. Direct heteromodal cortical connections have been shown between the primary auditory cortex (A1) and primary visual cortex (V1), and between A1 and secondary visual cortex (V2). Auditory afferents to V2 terminate in close proximity to neurons that project to V1, and potentially constitute an effective indirect pathway between A1 and V1. In this study, we injected a retrograde adenoviral vector that expresses enhanced green fluorescent protein under a synapsin promotor in V1 and biotinylated dextran amine as an anterograde tracer in A1 to determine: (i) whether A1 axon terminals establish synaptic contacts onto the lateral part of V2 (V2L) neurons that project to V1; and (ii) if this indirect cortical pathway is altered by a neonatal enucleation in mice. Complete dendritic arbors of layer V pyramidal neurons were reconstructed in 3D, and putative contacts between pre-synaptic auditory inputs and postsynaptic visual neurons were analysed using a laser-scanning confocal microscope. Putative synaptic contacts were classified as high-confidence and low-confidence contacts, and charted onto dendritic trees. As all reconstructed layer V pyramidal neurons received auditory inputs by these criteria, we conclude that V2L acts as an important relay between A1 and V1. Auditory inputs are preferentially located onto lower branch order dendrites in enucleated mice. Also, V2L neurons are subject to morphological reorganizations in both apical and basal dendrites after the loss of vision. The A1-V2L-V1 pathway could be involved in multisensory processing and contribute to the auditory activation of the occipital cortex in the blind rodent.

Altered expression of parvalbumin and calbindin in interneurons within the primary visual cortex of neonatal enucleated hamsters.

In the present study, we tested the hypothesis that the expression of calcium binding proteins (CaBPs), parvalbumin (PV), calretinin (CR) and calbindin (CB), is dependent upon sensory experience as emphasized in visual deprivation and deafferentation studies. The expression of CaBPs was studied in interneurons within the primary and extrastriate visual cortices (V1, V2M, V2L) and auditory cortex (AC) of adult hamsters enucleated at birth. The effects of enucleation were mainly confined to area V1 where there was a significant volume reduction (26%) and changes in the laminar distribution of PV and CB immunoreactive (IR) cells. The density of PV-IR cell bodies was significantly increased in layer IV and reduced in layer V. Moreover, the density of CB-IR neurons was inferior in layer V of V1 in enucleated hamsters (EH) compared to controls. These results suggest that some features of the laminar distribution of specific CaBPs, in primary sensory cortices, are dependent upon or modulated by sensory input.

Complex motion selectivity in PMLS cortex following early lesions of primary visual cortex in the cat.

In the cat, the analysis of visual motion cues has generally been attributed to the posteromedial lateral suprasylvian cortex (PMLS) (Toyama et al., 1985; Rauschecker et al., 1987; Rauschecker, 1988; Kim et al., 1997). The responses of neurons in this area are not critically dependent on inputs from the primary visual cortex (VC), as lesions of VC leave neuronal response properties in PMLS relatively unchanged (Spear & Baumann, 1979; Spear, 1988; Guido et al., 1990b). However, previous studies have used a limited range of visual stimuli. In this study, we assessed whether neurons in PMLS cortex remained direction-selective to complex motion stimuli following a lesion of VC, particularly to complex random dot kinematograms (RDKs). Unilateral aspiration of VC was performed on post-natal days 7-9. Single unit extracellular recordings were performed one year later in the ipsilateral PMLS cortex. As in previous studies, a reduction in the percentage of direction selective neurons was observed with drifting sinewave gratings. We report a previously unobserved phenomenon with sinewave gratings, in which there is a greater modulation of firing rate at the temporal frequency of the stimulus in animals with a lesion of VC, suggesting an increased segregation of ON and OFF sub-regions. A significant portion of neurons in PMLS cortex were direction selective to simple (16/18) and complex (11/16) RDKs. However, the strength of direction selectivity to both stimuli was reduced as compared to normals. The data suggest that complex motion processing is still present, albeit reduced, in PMLS cortex despite the removal of VC input. The complex RDK motion selectivity is consistent with both geniculo-cortical and extra-geniculate thalamo-cortical pathways in residual direction encoding.

Distribution, morphology, and synaptic targets of corticothalamic terminals in the cat lateral posterior-pulvinar complex that originate from the posteromedial lateral suprasylvian cortex.

The lateral posterior (LP) nucleus is a higher order thalamic nucleus that is believed to play a key role in the transmission of visual information between cortical areas. Two types of cortical terminals have been identified in higher order nuclei, large (type II) and smaller (type I), which have been proposed to drive and modulate, respectively, the response properties of thalamic cells (Sherman and Guillery [1998] Proc. Natl. Acad. Sci. U. S. A. 95:7121-7126). The aim of this study was to assess and compare the relative contribution of driver and modulator inputs to the LP nucleus that originate from the posteromedial part of the lateral suprasylvian cortex (PMLS) and area 17. To achieve this goal, the anterograde tracers biotinylated dextran amine (BDA) or Phaseolus vulgaris leucoagglutinin (PHAL) were injected into area 17 or PMLS. Results indicate that area 17 injections preferentially labelled large terminals, whereas PMLS injections preferentially labelled small terminals. A detailed analysis of PMLS terminal morphology revealed at least four categories of terminals: small type I terminals (57%), medium-sized to large singletons (30%), large terminals in arrangements of intermediate complexity (8%), and large terminals that form arrangements resembling rosettes (5%). Ultrastructural analysis and postembedding immunocytochemical staining for gamma-aminobutyric acid (GABA) distinguished two types of labelled PMLS terminals: small profiles with round vesicles (RS profiles) that contacted mostly non-GABAergic dendrites outside of glomeruli and large profiles with round vesicles (RL profiles) that contacted non-GABAergic dendrites (55%) and GABAergic dendritic terminals (45%) in glomeruli. RL profiles likely include singleton, intermediate, and rosette terminals, although future studies are needed to establish definitively the relationship between light microscopic morphology and ultrastructural features. All terminals types appeared to be involved in reciprocal corticothalamocortical connections as a result of an intermingling of terminals labelled by anterograde transport and cells labelled by retrograde transport. In conclusion, our results indicate that the origin of the driver inputs reaching the LP nucleus is not restricted to the primary visual cortex and that extrastriate visual areas might also contribute to the basic organization of visual receptive fields of neurons in this higher order nucleus.

Visual pathways following cerebral hemispherectomy.

The anatomical consequences of unilateral cerebral hemispherectomy in some animal models are reviewed. We have shown that the retinogenigulate pathway undergoes severe degenerative changes in hemispherectomized monkeys, greater than those shown in cats and we proposed that remaining retinal terminals to the dorsal lateral geniculate nucleus have little potential for conveying visual information any further. All subdivisions of the pulvinar undergo severe degeneration following hemispherectomy showing that the ascending tectofugal pathway is also shut off. On the other hand, the retina subserving the blind field is not depleted of ganglion cells which still send normal appearing terminals to the midbrain pretectum and superior colliculus. Visual information from the blind hemifield can thus gain access to the brain and could potentially reach the contralateral cerebral cortex through the midbrain commissure and possibly through thalamic commissural cells.

When the auditory cortex turns visual.

We studied visually guided behavior and the visual response properties of single auditory cortex (A1) neurons in neonatally operated hamsters with surgically induced, permanent, ectopic retinal projections to auditory thalamic nuclei and to visual thalamic nuclei which normally receive little direct retinal input. The surgically induced retino-thalamo-cortical pathways can mediate visual guided behaviors whose normal substrate, the pathway from the retina to the primary visual cortex via the primary thalamic visual nucleus, is missing. The visually evoked response properties of A1 neurons resemble in many respects those of neurons in V1 of normal hamsters: many A1 neurons have well-defined visual receptive fields and preferences for orientation or direction of movement. In addition, some visually responsive cells in A1 are bimodal--they also respond to auditory stimuli. The visually responsive neurons in A1 probably account for the capacity of the auditory cortex to mediate visual behavior in 'rewired hamsters'.

Anatomical sparing in the superior colliculus of hemispherectomized monkeys.

Using the monkey as a model for human hemispherectomy, the effects of early removal of a whole cerebral hemisphere on the cytoarchitecture and cytochrome oxidase histochemistry of the superior colliculus (SC) were evaluated. Results show that the SC ipsilateral to the cortical lesion suffers a 29.9% average volume reduction and a 32.7% total loss of neurons compared to the contralateral SC. Neuronal densities and metabolic activity are similar in normal and hemispherectomized monkeys. Furthermore, the ipsi- and contralesional SC receive retinal inputs as revealed with intraocular injections of tritiated proline. These data suggest that the superior colliculus retains functional capabilities following hemispherectomy in monkey.

Quantitative analysis of the retinal ganglion cell layer in the ostrich, Struthio camelus.

The total number, distribution and peak density of ganglion cells were evaluated in the Nissl-stained retina of the ostrich (Struthio camelus). The mean (n = 4) total number of retinal ganglion cells (RGC) was estimated at 2,274,128 (s.d. = 273, 152). The ostrich retina exhibited a prominent horizontal visual streak along which a central area located nasal to the pecten had a peak density of 9,500 cells/mm2. A high concentration of cells with a peak density of 2,646 cells/mm2 was also observed in the temporal retina, slightly dorsal to the visual streak. The results further showed that the ostrich eye has a 15-mm pupil entrance diameter, its mean axial length is 39.81 mm, the estimated retinal magnification factor is 0.4075 mm/deg and the maximum visual acuity along the well-defined visual streak was estimated to be 19.32 cycles/deg. The latter component of the retina might subserve vision along the horizon while the temporal region mediates binocular processing. The data also showed that the degree of retinal illumination in this bird could be comparable to that noted in some nocturnal species. The findings in this study suggest that the ostrich might not be restricted to diurnal activity.

Retinal projections to the pregeniculate nucleus in the hemispherectomized monkey.

Intraocular injections of tritiated proline were used to test the hypothesis that unilateral removal of all visual cortical areas results in increased distribution of retinal terminals in the pregeniculate nucleus (PGN) of the thalamus in monkeys. Following hemispherectomy, retinal input to the ipsilateral PGN was reduced by an average of 18.5% when compared to its contralateral homologue, which corresponded to the reduction in nuclear volume (19.3%). Our results show that removal of cortical afferents to the external layer of the PGN does not induce invasion of retinal projections into this region of the nucleus.

Surgically created neural pathways mediate visual pattern discrimination.

Combined lesions of retinal targets and ascending auditory pathways can induce, in developing animals, permanent retinal projections to auditory thalamic nuclei and to visual thalamic nuclei that normally receive little direct retinal input. Neurons in the auditory cortex of such animals have visual response properties that resemble those of neurons in the primary visual cortex of normal animals. Therefore, we investigated the behavioral function of the surgically induced retino-thalamo-cortical pathways. We showed that both surgically induced pathways can mediate visually guided behaviors whose normal substrate, the pathway from the retina to the primary visual cortex via the primary thalamic visual nucleus, is missing.

Retinogeniculate projections following early cerebral hemispherectomy in the vervet monkey.

The effects of early, unilateral cerebral hemispherectomy on retinogeniculate projections were studied in the vervet monkey (Cercopithecus aethiops sabeus). Hemispherectomy eliminates all geniculocortical pathways and thus removes cortical factors involved in the survival of retinogeniculate projections. Complete removal of the left cerebral cortex was performed in two monkeys at 6 months and 8 months of age. After a post-surgical survival period of 50 months (SHG3) and 45 months (SHG4), both animals and a normal adult monkey received intraocular injections of [3H]proline (5 mCi) in the left eye and WGA-HRP (100 microliters, 5%) in the right eye. The dorsal lateral geniculate nucleuseuron (LGNd) ipsilateral to the hemispherectomy was on average 73% smaller than the contralateral LGNd. The magno- and parvocellular layers ipsilateral to the cortical ablation in both hemispherectomized subjects received a layered, eye-specific pattern of retinal input. This suggests that retinogeniculate projections could be sustained in the absence of geniculate relay cells.

Relative size of the hyperstriatum ventrale is the best predictor of feeding innovation rate in birds.

Within the avian telencephalon, the dorsal ventricular ridge (DVR) contains higher order and multimodal integration areas. Using multiple regressions on 17 avian taxa, we show that an operational estimate of behavioral flexibility, the frequency of feeding innovation reports in ornithology journals, is most closely predicted by relative size of one of these DVR areas, the hyperstriatum ventrale. Neither phylogeny, juvenile development mode, nor species sampled account for the relationship. Similar results are found when the hyperstriatum ventrale is lumped with a second DVR structure, the neostriatum. In simple correlations, size of the wulst and the striatopallidal complex is associated with feeding innovation rate, but the two structures are eliminated from the multiple regressions. Our results parallel those on primates showing a correlation between innovation rate and neocortex size and support the idea that the mammalian neocortex and the neostriatum-hyperstriatum ventrale complex in birds have similar integrative roles.

Stereological evaluation of substantia nigra cell number in normal and hemispherectomized monkeys.

The assessment of the anatomical consequences of cortical lesions on subcortical visual relays is necessary to further understand residual visual capacities. Unbiased stereological techniques were used to evaluate cell numbers in the substantia nigra (SN), a structure involved in the control of saccadic eye movements. Cell numbers were very similar in the ipsi- and contralateral SN of the hemispherectomized animal (329,926 vs. 310,248). These numbers are close to what was observed in the normal monkey (300,130 and 320, 859). In one case, part of the striatum was lesioned in addition to the cerebral hemisphere. Noticeable effects were observed in the SN ipsilateral to the cortical lesion: volume was reduced by 30.5% while the number of neurons, compared to the contralateral side, dropped by 43.2% (186,644 vs. 328,757). These results suggest that due to its anatomical sparing following hemispherectomy the SN, in addition to other subcortical structures, is in a prime position to modulate the spared saccadic behaviors seen after massive cortical injuries.

Transneuronal degeneration of retinal ganglion cells in early hemispherectomized monkeys.

Transneuronal retrograde cell changes in the retina of the primate have been well documented after lesions to striate cortex, but little is known about the effects of hemispherectomy, a surgical procedure used in humans for the treatment of intractable epilepsy. In order to follow the time course of this degenerative process, we examined the retinae of six monkeys who underwent a total hemispherectomy at various postnatal ages with a survival period of 4 years. We demonstrate that transneuronal retrograde degeneration in the retina following hemispherectomy is inversely correlated with age at the time of the lesion. This degeneration is maximal when the lesion is induced within the first 4-6 months of life and less pronounced from 8 months to adulthood.

Size and distribution of retinal ganglion cells in the St. Kitts green monkey (Cercopithecus aethiops sabeus).

The topographical distribution of density and the soma size of retinal ganglion cells (RGCs) were studied in the St. Kitts green monkey (Cercopithecus aethiops sabeus). The total number of RGCs, estimated from light microscopic analysis of wholemounted and of transversely sectioned retinae, ranged between 1,183,721 and 1,273,715 (mean 1,228,646). These estimates are comparable to the number of optic nerve fibres (1,220,000) estimated from semithin sections. The topographic distribution of RGCs shows a strong centroperipheral gradient. The soma size distribution of RGCs in Nissl-stained flatmounts falls within a range of between 5.7 microm and 22.9 microm and is comparable to other primate species. Somata of RGCs were found to be generally smaller within the fovea than in peripheral regions. Ganglion cells, as reported for other diurnal primates, are nonuniformly distributed with a slight nasotemporal elongation of isodensity contours, and they exhibit nasotemporal asymmetry in the frequency distribution of soma size. The topography of the RGC distribution of this semiarboreal, ground-dwelling monkey is similar to what has been found in other diurnal Old World species.

Transneuronal retrograde degeneration of retinal ganglion cells following cerebral hemispherectomy in cats.

We have assessed the extent of transneuronal retrograde degeneration of retinal ganglion cells (RGCs) following the removal of a whole cerebral hemisphere at postnatal age 16 and 25 days. In the P16 animal, the nasal retina contralateral to the lesion suffered a 41% cell loss, whereas cell loss in the temporal retina ipsilateral to the lesion was 33%. Cell loss was greater in nasal retina and mainly included medium sized cells (200-600 microns2). In the P25 animal overall there was no evidence for ganglion cell loss.

Embryonic brain growth in two shorebirds: Charadrius vociferus and Gallinago gallinago.

The sizes of six brain regions and of the whole brain were measured for a series of embryonic killdeer, Charadrius vociferus, and common snipe, Gallinago gallinago, to examine (1) the allometric relationship between whole brain and body mass through ontogeny, (2) whether the longer incubation period of the killdeer corresponds to a larger brain at hatch, (3) whether different brain regions grow independently in size through ontogeny, and (4) whether relative size of particular brain regions relates to relative importance of hatching behavior or to the relative importance of behaviors in the adult. Although snipe are generally less precocial at hatch than killdeer, and hence are predicted to have lower allometric coefficients, the allometric relationships between brain and body mass for the two species were not significantly different and were comparable to those for other birds and mammals. The onset of the rapid growth phase of the whole brain, and each region, was very early in the snipe; as a consequence, brain sizes in both species are similar at hatch, despite the shorter incubation period of snipe. In hatchlings of both species, the brain comprises about 7% of body mass. The telencephalon grows most rapidly, the diencephalon and myelencephalon grow more slowly, and the optic tectum grows steadily throughout the embryonic period. The telencephalon of the hatchling snipe is relatively larger than that of hatchling killdeer and exhibits a large nucleus basalis, typical of tactile foragers, although snipe do not forage tactily until adulthood. The relatively large optic tectum of hatchling killdeer corresponds to the highly visual method of foraging of hatchlings. However, the degree to which brain regions grow in the embryonic period, with the exception of the optic tectum and cerebellum in killdeer, appears to relate very closely to their eventual size in adults, with large brain regions growing less in the embryonic period than small brain regions.

Neural bases of residual vision in hemicorticectomized monkeys.

In this series of studies, we have attempted to characterize anatomically the organization of the retinofugal pathways in monkeys that underwent the surgical removal in infancy of the entire left cerebral hemisphere. Hemidecordication in baby monkeys produced a transneuronal retrograde degeneration of the retinal ganglion cells (RGCs) that affected mainly the foveal rim. Although the density of RGCs in this region was drastically diminished, the soma sizes of the surviving cells remained normal. The lateral geniculate nucleus (dLGN) ipsilateral to the removed cortex was dramatically reduced in size although it still showed normal layering. There was a marked reduction in the number of neurons in both the parvocellular and magnocellular layers and a heavy gliosis. By contrast, the superior colliculus ipsilateral to the lesion was remarkably well preserved: although slightly reduced in volume, it showed little gliosis and a metabolic activity, as revealed by cytochrome oxidase histochemistry, similar to the superior colliculus contralateral to the lesion. Behavioral perimetry indicated a partial sparing of vision up to 45 degrees in the 'blind' hemifield. We argue that the preservation of the retino-tectal pathway mediates most of the residual visual functions found in the 'blind field' of hemispherectomized human subjects.