This study of the tree shrew, Tupaia belangeri, provides evidence for an intracollicular pathway that arises in the superficial gray layer and terminates in the optic layer. As a first step, Nissl, myelin, and cytochrome oxidase stains were used to identify the layers of the superior colliculus in the tree shrew. Second, anterograde and retrograde axonal transport methods were used to determine relationships between laminar borders and patterns of connections. Intraocular injections of wheat germ agglutinin conjugated to horseradish peroxidase showed that the border between the superficial gray and optic layers in the tree shrew is marked by a sharp decrease in the density of retinotectal projections. The optic layer also could be distinguished from the subjacent intermediate gray layer by differences in connections. Of the two layers, only the intermediate gray layer received projections following injections of wheat germ agglutinin conjugated to horseradish peroxidase within substantia nigra pars reticulata. Similarly, following injections of horseradish peroxidase or biocytin in the paramedian pons, the intermediate gray but not the optic layer contained labeled cells of origin for the main premotor pathway from the tectum, the predorsal bundle. Next, cells in the superficial gray layer were intracellularly injected with biocytin in living brain slices. Axons were traced from narrow and wide field vertical cells in the deep part of the superficial gray layer to the gray matter surrounding the fiber fascicles of the optic layer. Small extracellular injections of biocytin in brain slices showed that the optic layer gray matter contains a population of stellate cells that are in position to receive the input from the superficial layer. Finally, small extracellular injections of biocytin in the intermediate gray layer filled cells that sent prominent apical dendrites into the optic layer, where they may be directly contacted by the superficial gray layer cells. Taken together, the results support the hypothesis that the optic layer is functionally distinct from its adjacent layers, and may provide a link in the transfer of information from the superficial, retinal recipient, to the intermediate, premotor, layer of the superior colliculus.

No abstract

These experiments were designed to test the idea that the optic layer in the tree shrew, Tupaia belonged is functionally distinct and provides a link between the visuosensory superficial and the premotor intermediate layers of the superior colliculus. First, cells in the optic layer were intracellularly labeled with biocytin in living brain slices. Compared to cells in the adjacent lower part of the superficial gray layer, which have apical dendntes that ascend toward the tectal surface, optic layer cells have dendritic fields that are restricted for the most part to the optic layer itself The differences in dendritic-field location imply that superficial gray and optic layer cells have different patterns of input The axons of optic layer cells terminate densely within the optic layer and, in addition, project in a horizontally restricted fashion to the overlying superficial gray and subjacent intermediate gray layers. This pattern also is different from the predominantly descending interlaminar projections of lower superficial gray layer cells Next cells in the intermediate gray layer were labeled in order to examine the relationships between optic layer cells and these subjacent neurons that project from the superior colliculus to oculomotor centers of the brain stem Neurons in the upper part of the intermediate gray layer send apical dendrites into the optic layer and therefore can receive signals from the superficial gray layer either directly, from descending axons of lower superficial gray layer cells, or indirectly, through intervening optic layer cells. In contrast, lower intermediate gray layer cells have more radiate dendritic fields that are restricted to the intermediate gray layer. Thus, these lower cells must depend on descending projections from optic or upper intermediate gray layer cells for signals from the superficial gray layer Together, these results support the idea that the optic layer is a distinct lamina that provides ; link between the superficial and intermediate gray layers. They also are consistent with the traditional view that descending intracollicular projections play a role in the selection of visual targets for saccades.

Some models propose that the spatial and temporal distributions of premotor activity in the intermediate layer of the superior colliculus are shaped by neuronal ensembles that give rise to local excitatory and distant inhibitory connections. One function proposed for these connections is to mediate a "winner-take-all" network; the short-range excitatory connections build up the activity of neighboring cells that command orienting movements in one direction, whereas the wide-ranging inhibitory projections attenuate the activity of remote cells that command incompatible movements. We used in vitro photostimulation and whole-cell patch-clamp recording to test these models by measuring the spatial extent of synaptic interactions within the rat intermediate layer.

We have used photostimulation and whole cell patch-clamp recording techniques to examine local synaptic interactions in slices from the superior colliculus of the tree shrew. Uncaging glutamate 10-75 microm from the somata of neurons in the intermediate gray layer elicited a long-lasting inward current, due to direct activation of glutamate receptors on these neurons, and brief inward currents caused by activation of presynaptic neurons. The synaptic responses occurred as individual currents or as clusters that lasted up to several hundred milliseconds. Excitatory synaptic responses, which reversed at membrane potentials near 0 mV, could be evoked by uncaging glutamate anywhere within 75 microm of an intermediate layer neuron. Our results indicate the presence of extensive local excitatory circuits in the intermediate layer of the superior colliculus and support the hypothesis that such intrinsic circuitry contributes to the development of presaccadic command bursts.