Topography of cortico-striatal connections in man: anatomical evidence for parallel organization.

Tracing studies in non-human primates support the existence of several parallel neuronal circuits involving cerebral cortex, basal ganglia and thalamus. Distinct functional loops were proposed to underlie multiple aspects of normal and pathological behaviour in man. We present here the first anatomical evidence for separate corticostriatal systems in humans. Neural connections of the sensorimotor and prefrontal cortex to the striatum were studied in one human brain using the Nauta method for anterogradely degenerating axons. Axons originating from a lesion in the left sensorimotor cortex, including the face area, were found to terminate in the superolateral part of the ipsilateral putamen, forming a narrow band in its posterior part. Inside the band, the distribution of degenerating axons was inhomogeneous; high-density clusters of approximately 2.5 mm in diameter were separated by regions with less dense cortical projections. Axons originating from a small lesion in the fundus of the right superior frontal sulcus were found in the upper part of the ipsilateral caudate nucleus. The existence of discrete and anatomically segregated terminal patches originating from distinct cortical regions suggests parallel organization of cortico-striatal connections in man.

Patterns of calcium-binding proteins in human inferior colliculus: identification of subdivisions and evidence for putative parallel systems.

The subdivisions of human inferior colliculus are currently based on Golgi and Nissl-stained preparations. We have investigated the distribution of calcium-binding protein immunoreactivity in the human inferior colliculus and found complementary or mutually exclusive localisations of parvalbumin versus calbindin D-28k and calretinin staining. The central nucleus of the inferior colliculus but not the surrounding regions contained parvalbumin-positive neuronal somata and fibres. Calbindin-positive neurons and fibres were concentrated in the dorsal aspect of the central nucleus and in structures surrounding it: the dorsal cortex, the lateral lemniscus, the ventrolateral nucleus, and the intercollicular region. In the dorsal cortex, labelling of calbindin and calretinin revealed four distinct layers.Thus, calcium-binding protein reactivity reveals in the human inferior colliculus distinct neuronal populations that are anatomically segregated. The different calcium-binding protein-defined subdivisions may belong to parallel auditory pathways that were previously demonstrated in non-human primates, and they may constitute a first indication of parallel processing in human subcortical auditory structures.

Commissural connections of human superior colliculus.

The superior colliculus of higher mammals is a laminated structure of the midbrain that receives visual input in superficial layers, and visual, auditory and somatosensory input in deep layers. The superior colliculi on either side are interconnected via the intercollicular commissure, which has been proposed to play a role in visual transfer and gaze orienting. Intercollicular connections have been anatomically demonstrated in various species including macaque monkeys but not in man. Here we describe the organization of commissural connections of the superior colliculus in man. A single injection of the carbocyanine tracer 1,1'-dioctadecyl-3,3,3',3'-tetramethylindocarbocyanine perchlorate was made into the superior colliculus in five post-mortem brains. Contralateral to the injection, labelled axons formed a dense bundle in the deep collicular layers and isolated axons were present in the superficial layers. Synaptic-like boutons were found in all collicular layers. Injections placed at different rostro-caudal levels revealed a roughly topographical organization; the bulk of the labelled axons were found opposite to the injection, with a progressive decrease in labelling at more rostral and caudal levels. Our results demonstrate that superficial and, to a larger extent, deep layers participate in intercollicular connections, and suggest that visual information crosses at the collicular level.

Intrinsic connectivity of human auditory areas: a tracing study with DiI.

The human supratemporal plane contains the primary as well as several other auditory areas. We have investigated the intrinsic connectivity of these areas by means of antero- and retrograde labelling with the carbocyanin dye DiI (1,1'-dioctadecyl-3,3,3',3'-tetramethylindocarbocyanine perchlorate). A total of 30 injections was placed in both hemispheres of four freshly fixed postmortem brains. Labelled neurons and axons were found in cortex around the injection. The retrograde labelling varied from faint to Golgi-like; most of the retrograde labelled neurons were layers II-III pyramids and only a few were nonpyramidal neurons. Labelled axons were dense in all layers near the injection site, while they became relatively rare in layer IV further away. The tangential spread of labelling differed among auditory areas. On Heschl's gyrus (corresponding to the primary auditory cortex and cytoarchitectonic areas TD and part of TB) intrinsic connectivity involved a relatively narrow part of cortex. They spread over larger parts of cortex in plana polare and temporale (areas TG, TA and the remaining part of TB). A number of injections also produced anisotropic labelling patterns. These results reveal differences in intrinsic connectivity between auditory areas. They suggest that intrinsic connections within the primary auditory area, area TD and part of TB that is on Heschl's gyrus, involve mainly nearby units or modules, probably with similar coding properties, whereas in surrounding areas, connections spread over more distant units and may play an important role in the integration of different auditory features.

Spatial properties and direction selectivity of single neurons in area 21b of the cat.

The receptive field properties of single units were assessed in area 21b of the cat visual cortex. Visual cells in this area were binocular and showed relatively large receptive fields. Most cells were strongly sensitive to the direction of drifting gratings. The mean value of the half-widths of the direction tuning curves (32 degrees ) suggests broader direction tunings than are typically found in other visual areas. The spatial frequency tuning functions were either band-pass or low-pass. Cells responded optimally to low spatial frequencies (mean =0.08c/deg) and also showed low spatial resolution (mean =0.29c/deg.). The estimated values of spatial bandwidths (mean=2.2 octaves) suggest that area 21b cells act as relatively good spatial filters. Although some cells exhibited a low contrast threshold, most cells began to respond at intermediate or high contrast values (mean threshold =15.5%). Temporal frequency tuning functions were mostly band-pass and usually broad (mean temporal bandwidth=3.3 octaves). Cells were found that responded optimally to various temporal frequencies (mean optimal temporal frequency=3.2Hz), although the majority preferred a temporal frequency below 4Hz.These results suggest that visual properties (receptive fields sizes, spatial resolution and orientation/direction selectivity) of cells in area 21b differ from those of cells previously observed in the adjoining area 21a. These differences provide evidence in support of functional distinction between these two visual areas.

Thalamic projections of the fusiform gyrus in man.

Previous retrograde degeneration studies have shown that human extrastriate visual cortex receives projections from the pulvinar, but their precise topographical organization remained unknown. We report on the distribution of thalamic projections originating in the fusiform gyrus, as studied with the Nauta method for anterogradely degenerating axons, in a case of right fusiform gyrus infarction. Ipsilaterally to the lesion, high density of afferents was found in the inferior pulvinar nucleus and a low density in the medial pulvinar nucleus as well as in the postero-inferior part of the reticular nucleus; no degenerating fibres were found in the lateral geniculate body. Degenerating axons were completely absent in the contralateral thalamus. Thus, there is a precise topographic relationship between parts of the extrastriate cortex and the pulvinar, suggesting segregated thalamocortical pathways for different parts of the extrastriate cortex. As in nonhuman primates, the human inferior temporal cortex has no direct output to the lateral geniculate body.

Spatial and temporal matching of receptive field properties of binocular cells in area 19 of the cat.

The spatial and temporal properties of single neurons were investigated in area 19 of the cat. We evaluated the matching of binocular receptive field properties with regard to the respective strength of the ipsilateral and contralateral inputs. Results indicate that most cells in area 19 are well tuned to spatial and temporal frequencies and exhibit relatively low contrast threshold (mean=6.8%) when assessed using optimal parameters and tested through the dominant eye. Spatial resolution (mean=0.75 c/degree), optimal spatial frequencies (mean=0.16 c/degree) were relatively low and spatial bandwidths (mean=2.1 octaves) were broader as compared to those of cells in area 17 but comparable to those of cells in other extrastriate areas. On the other hand temporal resolution (mean=10.7 Hz), optimal temporal frequency (mean=4.5 Hz) and temporal bandwidths (mean=2.9 octaves) were higher and broader than in primary visual cortex. A significant relationship exists between most of the cell's properties assessed through either eye. For some parameters, such as spatial and temporal resolution, ocular dominance was shown to be significantly related to the extent of matching between the two eyes. For these parameters, binocular cells that exhibited a balanced ocular dominance were generally well matched with regard to the receptive field properties of each eye whereas the largest mismatches were found in cells that were more strongly dominated by one eye. These results suggest that visual input contributes to the activation of cells in area 19 in a redundant manner, possibly attesting to the multiplicity of parallel pathways to this area in the cat.

Spatial resolution and contrast sensitivity of single neurons in area 19 of split-chiasm cats: a comparison with primary visual cortex.

Electrophysiological recordings were carried out in the callosal recipient zone of area 19 in normal and split-chiasm cats and, for comparison purposes, at the border of areas 17 and 18 of split-chiasm cats. The influences of retinothalamic and callosal inputs on a single cortical neurons were thereby evaluated. Extracellular recordings of single cells were made in anaesthetized and paralysed cats in the zone representing the central visual field. Receptive field properties were assessed using sine wave gratings drifting in optimal directions. Results showed that in area 19 and areas 17/18 one-third of the cells were binocularly driven after section of the optic chiasm. In area 19, the spatial resolution and contrast sensitivity of cells driven via the dominant eye were similar in the normal and split-chiasm groups. In areas 17/18 and area 19 of split-chiasm cats, binocular cells showed significant interocular matching of their receptive field properties (spatial resolution and contrast threshold), although small differences were observed. These small interocular differences were related to the cell's ocular dominance rather than to the signal transmission route (thalamic or callosal).

Spatial and temporal frequency tuning and contrast sensitivity of single neurons in area 21a of the cat.

The spatial and temporal selectivities of single neurons in area 21a of the adult cat were investigated using sinusoidal gratings. Optimal spatial frequencies and visual acuity (high cut-off frequency) were fairly low and spatial bandwidth was mainly narrow. Contrast threshold was generally low but a substantial number of cells were only excited by high contrast stimuli. The temporal selectivity suggests that cells responded to a wide range of temporal frequencies.