Because the axons of retinal ganglion cells are the sole channels carrying information from the eye, the organization of their central projections is important in visual processing. However, their detailed destinations and patterns of synaptic distribution at the level of single, functionally identified cells are not known. Most anatomical studies involve populations of cells or fibres and do not examine their physiological properties; physiological studies involving intracellular recording and injection of marker substances into cell bodies of single cells do not reveal distant axon terminals because the markers stain the fibres for only a few millimetres from the perikarya. To examine the central projections of retinal ganglion cells we have impaled single optic tract fibres near their sites of termination and injected them iontophoretically with the marker enzyme horseradish peroxidase (HRP). We now report that this method has revealed the thalamic and midbrain ramifications of single physiologically characterized axons. The individual optic-tract fibres branch repeatedly, sending collaterals to the superior colliculus (SC), the medial interlaminar nucleus (MIN), and to one or more laminae within the dorsal lateral geniculate nucleus (LGNd). In different nuclei the single axons form arborizations of characteristically different shapes and distribute their synaptic terminals in columns (LGNd), sheets (MIN) or widely spread patches (SC).
Optic tract fibers and cell bodies in the lateral geniculate nucleus of the monkey were studied intracellularly with micropipette electrodes containing the marker enzyme horseradish peroxidase. Single optic-tract fibers always projected to only one of the six geniculate layers. The majority of the axons innervating the four parvocellular laminae were red/green opponent color units; their terminations formed cylindrical columns that were perpendicular to the layers. In similar fashion, the geniculate cells in the parvocellular layers were mostly red/green units with narrow, bipolar dendritic fields oriented normal to the laminar borders. The majority of the retinal axons ending in parvocellular layers 6 and 5 were on-center units; nearly all geniculate cells in these two laminae were also on-center neurons. In layers 4 and 3 most terminating optic-tract fibers, as well as the geniculate cells themselves, were off-center units. AU axons projecting to the magnocellular layers were broad-band units with spherical terminal arborizations. The magnocellular geniculate neurons, which were also broad band, had extensive spherical dendritic fields that often crossed laminar borders. Thus, the terminal patterns of each class of retinogeniculate axon closely resembled the dendritic orientations of the functionally related geniculate target cells.The ganglion cells in the retina of the monkey consist of several distinct functional classes (1). Nearly all of them have on-center or off-center receptive fields. On-center ganglion cells discharge in response to an increase in the illumination falling on their receptive field centers, whereas off-center cells fire when the light level decreases. The field centers of many of these ganglion cells receive input from only one of the three cone classes; in turn, their surrounds are connected with only one of the two remaining cone types. As a result of these synaptic connections, the cells are excited by certain colors and inhibited by others. Some ganglion cells have center/surround receptive fields but show no special interest in color; both their centers and surrounds receive summating inputs from all three cone types. Consequently, these ganglion cells have broad-band spectral sensitivities.Axons of the retinal ganglion cells project to the lateral geniculate nucleus (LGN) in the thalamus. Here are found the same functional classes seen in the retina, with no obvious changes in their physiological properties (2-4). In the retina the different ganglion cell types are often found next to one another, whereas in the LGN each functional class is rather strictly confined to certain layers. For instance, nearly all opponent color neurons are located in the four dorsal parvocellular layers, whereas most broad-band cells are limited to the two ventral magnocellular laminae (2, 4, 5). Within the parvocellular layers almost all neurons in laminae 6 and 5 are on-center cells, whereas layers 4 and 3 contain mostly off-center neurons (4). This laminar separation of the geniculate-cell ...
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