The primate visual system consists of at least two processing streams, one passing ventrally into temporal cortex that is responsible for object vision, and the other running dorsally into parietal cortex that is responsible for spatial vision. How information from these two streams is combined for perception and action is not understood. Visually guided eye movements require information about both feature identity and location, so we investigated the topographic organization of visual cortex connections with frontal eye field (FEF), the final stage of cortical processing for saccadic eye movements. Multiple anatomical tracers were placed either in parietal and temporal cortex or in different parts of FEF in individual macaque monkeys. Convergence from the dorsal and ventral processing streams occurred in lateral FEF but not in medial FEF. Certain extrastriate areas with retinotopic visual field organizations projected topographically onto FEF. The dorsal bank of the superior temporal sulcus projected to medial FEF; the ventral bank, to lateral FEF, and the fundus, throughout FEF. Thus, lateral FEF, which is responsible for generating short saccades, receives visual afferents from the foveal representation in retinotopically organized areas, from areas that represent central vision in inferotemporal cortex and from other areas having no retinotopic order. In contrast, medial FEF, which is responsible for generating longer saccades, is innervated by the peripheral representation of retinotopically organized areas, from areas that emphasize peripheral vision or are multimodal and from other areas that have no retinotopic order or are auditory.
1. The purpose of this study was to analyze the response properties of neurons in the frontal eye fields (FEF) of rhesus monkeys (Macaca mulatta) and to compare and contrast the various functional classes with those recorded in the supplementary eye fields (SEF) of the same animals performing the same go/no-go visual tracking task. Three hundred ten cells recorded in FEF provided the data for this investigation. 2. Visual cells in FEF responded to the stimuli that guided the eye movements. The visual cells in FEF responded with a slightly shorter latency and were more consistent and phasic in their activation than their counterparts in SEF. The receptive fields tended to emphasize the contralateral hemifield to the same extent as those observed in SEF visual cells. 3. Preparatory set cells began to discharge after the presentation of the target and ceased firing before the saccade, after the go/no-go cue was given. These neurons comprised a smaller proportion in FEF than in SEF. In contrast to their counterparts in SEF, the preparatory set cells in FEF did not respond preferentially in relation to contralateral movements, even though most responded preferentially for movements in one particular direction. The time course of the discharge of the FEF set cells was similar to that of their SEF counterparts, except that they reached their peak level of activation sooner. The few preparatory set cells in FEF tested with both auditory and visual stimuli tended to respond preferentially to the visual targets, whereas, in contrast, most set cells in SEF were bimodal. 4. Sensory-movement cells represented the largest population of cells recorded in FEF, responding in relation to both the presentation of the targets and the execution of the saccade. Although some of these sensory-movement cells resembled their counterparts in SEF by exhibiting a sustained elevation of activity, most of the FEF sensory-movement cells gave two discrete bursts, one after the presentation of the target and another before and during the saccade. Like their counterparts in SEF, the sensory-movement cells tended to be tuned for saccades into the contralateral hemifield, but this tendency was more pronounced in FEF than in SEF. The FEF sensory-movement cells discharged more briskly, with a shorter latency relative to the presentation of the target, than their counterparts in SEF. In addition, the FEF sensory-movement neurons reached their peak activation sooner than SEF sensory-movement neurons. Most FEF sensory-movement cells exhibited different patterns of activation in response to visual and auditory targets.(ABSTRACT TRUNCATED AT 400 WORDS)
The degree of parallel processing in frontal cortex-basal ganglia circuits is a central and debated issue in research on the basal ganglia. To approach this issue directly, we analyzed and compared the corticostriatal projections of two principal oculomotor areas of the frontal lobes, the frontal eye field (FEF) and the supplementary eye field (SEF). We first identified cortical regions within or adjacent to each eye field by microstimulation in macaque monkeys and then injected each site with either 35S-methionine or WGA-HRP conjugate. We analyzed the corticostriatal projections and also the interconnections of the pairs of cortical areas. We observed major convergence of the projections of the FEF and the SEF within the striatum, principally in the caudate nucleus. In cross sections through the striatum, both projections were broken into a series of discontinuous input zones that seemed to be part of complex three-dimensional labyrinths. Where the FEF and SEF projection fields were both present, they overlapped patch for patch. Thus, both inputs were dispersed within the striatum but converged with one another. Striatal afferents from cortex adjacent to the FEF and the SEF did not show convergence with SEF and FEF inputs, but did, in part, converge with one another. For all pairs of cortical areas tested, the degree of overlap in the corticostriatal projections appeared to be directly correlated with the degree of cortical interconnectivity of the areas injected. All of the corticostriatal fiber projections observed primarily avoided immunohistochemically identified striosomes. We conclude that there is convergence of oculomotor information from two distinct regions of the frontal cortex to the striatal matrix, which is known to project into pallidonigral circuits including the striatonigrocollicular pathway of the saccadic eye movement system. Furthermore, functionally distinct premotor areas near the oculomotor fields often systematically projected to striatal zones adjacent to oculomotor field projections, suggesting an anatomical basis for potential interaction of these inputs within the striatum. We propose that parallel processing is not the exclusive principle of organization of forebrain circuits associated with the basal ganglia. Rather, patterns of both convergence and divergence are present and are likely to depend on multiple functional and developmental constraints.
1. The purpose of this study was to describe the response properties of neurons in the supplementary motor area (SMA), including the supplementary eye fields (SEF) of three rhesus monkeys (Macaca mulatta) performing visually guided eye and forelimb movements. Seven hundred thirty single units were recorded in the dorsomedial agranular cortex while monkeys performed a go/no-go visual tracking task. The unit activity associated with rewarded, task-related movements was compared with that associated with unrewarded, spontaneous movements executed in the intertrial interval or when the task was not running. A number of neuronal response types were identified. 2. Sensory cells were characterized by their response to the visual and/or auditory target stimuli combined with no discharge associated with eye or forelimb movements. New information was provided about the receptive fields of the visual cells; they varied in size and, although many included the ipsilateral hemifield, they tended to emphasize the contralateral. A significant proportion of the visually responsive cells had receptive fields restricted to within 8 degrees of the fovea. The response latency was relatively long (greater than 90 ms) and variable. 3. Preparatory set cells were activated from the appearance of the target until the presentation of the go/no-go cue. This subpopulation ceased firing 50-100 ms before the movement was initiated. These cells tended to respond best in relation to contralateral movements. The response latency was similar to that of the sensory cells, although some of these units began to discharge in anticipation of predictable target presentations. These neurons were not active before unrewarded, spontaneous saccades. 4. Sensory-movement cells comprised the largest population of neurons identified in SMA. They were active from the appearance of the target until after the execution of the saccade. These neurons tended to respond preferentially in association with contraversive saccades. The latency of response to the target was significantly longer than that of the sensory cells. There was a large amount of variability in the time to reach the peak level of activation, and this population of units generally became inactivated shortly after the saccade was initiated. Although there were counterexamples, most sensory-movement cells responded equally in association with visually and auditory guided movements. In addition, these neurons were not active in relation to self-generated eye movements made during the intertrial intervals. 5. Pause-rebound cells were identified by their suppression at the appearance of the target and subsequent discharge associated with the saccade. These units tended to respond preferentially to contralateral targets.(ABSTRACT TRUNCATED AT 400 WORDS)
Most retinal ganglion cells (Levick and Thibos, 1982) and cortical cells (Leventhal, 1983; Leventhal et al., 1984) subserving peripheral vision respond best to stimuli that are oriented radially, i.e., like the spokes of a wheel with the area centralis at the hub. We have extended this work by comparing directly the distributions of orientations represented in topographically corresponding regions of retina and visual cortex. Both central and peripheral regions were studied. The relations between the orientations of neighboring ganglion cells and the manner in which the overrepresentation of radial orientations is accommodated in the functional architecture of visual cortex were also studied. Our results are based on an analysis of the orientations of the dendritic fields of 1296 ganglion cells throughout the retina and the preferred orientations of 1389 cells located in retinotopically corresponding regions of cortical areas 17, 18, and 19 in the cat. We find that horizontal and vertical orientations are overrepresented in regions of both retina and visual cortex subserving the central 5 degrees of vision. The distributions of the orientations of retinal ganglion cells and cortical cells subserving the horizontal, vertical, and diagonal meridians outside the area centralis differ significantly. The distribution of the preferred orientations of the S (simple) cells in areas 17, 18 and 19 subserving a given part of the retina corresponds to the distribution of the dendritic field orientations of the ganglion cells in that part of retina. The distribution of the preferred orientations of C (complex) cells with narrow receptive fields in area 17 but not C cells with wide receptive fields in areas 17, 18, or 19 subserving a given part of the retina matches the distribution of the orientations of the ganglion cells in that part of retina. The orientations of all of the alpha-cells in 5-9 mm2 patches of retina along the horizontal, vertical, and oblique meridians were determined. A comparison of the orientations of neighboring cells indicates that other than a mutual tendency to be oriented radially, ganglion cells with similar orientations are not clustered in the retina. Reconstructions of electrode penetrations into regions of visual cortex representing peripheral retina indicate that columns subserving radial orientations are wider than those subserving nonradial orientations. Our results provide evidence that the distribution of the preferred orientations of simple cells in visual cortex subserving any region of the visual field matches the distribution of the orientations of the ganglion cells subserving the same region of the visual field.(ABSTRACT TRUNCATED AT 400 WORDS)
The development of the nasotemporal division in cat retina was studied. We find that in the normally pigmented neonatal cat significant numbers of ganglion cells of all types in temporal retina project to the contralateral dorsal lateral geniculate nucleus (LGNd); far fewer cells in temporal retina project contralaterally to the LGNd in the normal adult. Thus, most of these cells must be eliminated during development. Experimental interruption of one optic tract in the neonate results in the retrograde degeneration of the ipsilaterally projecting ganglion cells in the temporal retina ipsilateral to the lesion. Consequent to the loss of the ipsilaterally projecting cells in this hemiretina, many of the ganglion cells projecting to the intact contralateral LGNd, which are normally eliminated, survive. Also, unlike in the normal cat, in which very few of the small ganglion cells in temporal retina project contralaterally to the thalamus, in optic tract sectioned (OTX) cats, significant numbers of the smallest ganglion cells in the temporal retina ipsilateral to the lesion project contralaterally to the intact thalamus. In order to make a quantitative comparison of the distributions of ipsilaterally and contralaterally projecting cells in the temporal retinae of normal cats, OTX cats, and neonatal kittens, it was necessary to determine the position of the vertical meridian in all animals. We defined the vertical meridian as the median edge (Stone, 1966). The median edge was determined from the distribution of the most nasally located, ipsilaterally projecting cells in temporal retina. The results indicate that the angle of the vertical meridian (median edge) with respect to the area centralis and optic disc is specified before birth and does not differ in normal cats, OTX cats, or neonatal kittens. Since the location of the vertical meridian does not change with age in postnatal life and is not affected by optic tract section, corresponding regions of retina in the different groups could be compared. A quantitative analysis of ganglion cell density in the temporal retina contralateral to the section, ipsilateral to the intact hemisphere, indicated that there was a reduction in the population of ipsilaterally projecting ganglion cells that was complementary to the abnormally large number of contralaterally projecting cells surviving in the temporal retina ipsilateral to the lesion.(ABSTRACT TRUNCATED AT 400 WORDS)
The morphology of ganglion cell dendritic trees varies across the cat retina. Evidence is presented that the variation in two attributes of ganglion cell dendritic structure can be accounted for by specific aspects of the topography of the adult and developing retina. The first attribute considered was the displacement of the center of the dendritic field from the cell body in the plane of the retina. The results of this study provide evidence that most ganglion cell dendritic fields are displaced away from neighboring cells, i.e., down the retinal ganglion cell density gradient. Because of the systematic dendritic displacement locally, the centers of the dendritic fields are arranged in a more precise mosaic than are their cell bodies. The second attribute considered was the elongation and orientation of the dendritic fields. From approximately embryonic day 50 to postnatal day 10 the cat retina undergoes a process of maturation (reviewed by Rapaport and Stone: Neuroscience 11:289-301, '84) that begins at the area centralis and spreads over the retina in a horizontally elongated wave. We found that the elongation and orientation of retinal ganglion cell dendritic fields is significantly correlated with the shape of the wave of maturation. The orientation of a dendritic field is not predicted by the direction of its displacement nor is it directly related to the distribution of neighboring retinal ganglion cells. These results indicate that the displacement of a ganglion cell's dendritic field from its cell body results from mechanisms different from those responsible for the orientation of the dendritic field. Factors that may be responsible for these two attributes of ganglion cell dendritic morphology are discussed.
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