The organization of projections of the retinorecipient and nonretinorecipient nuclei of the pretectal complex and layers of the superior colliculus to the lateral pulvinar and medial pulvinar in the macaque monkey
Authors: Benevento Louis A. , Standage Gregg P. 
Published: January 2005

The organization of five projections from the retinorecipient and non‐retinorecipient layers of the superior colliculus (SC) and nuclei of the pre‐tectum to the lateral pulvinar, medial pulvinar, and dorsal lateral geniculate nucleus (DLG) of the thalamus in the macaque monkey were established by using both anterograde autoradiographic and retrograde horseradish perox‐idase tracing techniques. Some projections from these midbrain regions to the inferior pulvinar are also described as are projections to the thalamus from the tectorccipient parabigeminal nucleus. First, the retinorecipient and nonretinorecipient pretectal nuclei and SC layers were determined by Nissl stains, myelin stains, and the distribution of label resulting from intraocular injections of tritiated amino acids. The possible projections of these pre‐tectal nuclei, layers of the SC (as well as the parabigeminal nucleus), to the pulvinar and DLG were then determined by both horseradish peroxidase and autoradiographic tracing methods. The retinal projections to the SC extend throughout layers II‐l, II‐2, II‐3, and dorsal III with obvious patches in layers II‐l and II‐2 as described before by others. There were a number of pretectal nuclei which also had connections with the retina. In the nomenclature adopted, these include the sublentiform nucleus, the nucleus of the optic tract (not to be confused with the thalamic limitansnucleus), the posterior (orprincipal) pretectalnucleus, and the laminatedolivary nucleus (with a head and tail). The nucleus of the posterior commissure and the nucleus of the pretectal area do not receive retinal projections.

The retinorecipient midbrain regions which project to the pulvinar are as follows. Aside from a complicated multifocal projection to the inferior pulvinar, the superficial retinorecipient SC layers project to three terminal foci or zones in one or more of the lateral pulvinar subdivisions alpha, beta, and gamma (Rezak and Benevento, 1977). Focus 1 lies mainly along the dorso‐ventral lateral border of subdivisions of PL‐gamma and PL‐beta, extending ventrally to PL‐alpha, and arises from SC layers II‐3 and III. Focus 2 occu‐pies the lateral 20–50% of PL‐alpha and arises from SC layers II‐2, II‐3, and III. There is a topographical arrangement to the SC projections to foci 1 and 2 which may reflect a representation of more than two visual quadrants in the lateral pulvinar.

Focus 3, which consists of several clusters, is located medially in PL‐gamma and PL‐beta and overlaps their mutual border with the medial pul‐vinar. Focus 3 is complicated as it is made up of a mixed input from the retinorecipient (superficial) and nonretinorecipient (deep) SC layers. The portion of focus 3 located along the medial edge of the lateral pulvinar arises mainly from SC layers II‐2, II‐3, and III, while the portion of the focus located along the adjacent lateral edge of the medial pulvinar arises mainly from SC layersIV, V, and VI. These projections to the pulvinar from the superficial SC differ in their origins from those to the DLG which arise mainly from smaller cells in SC sublayer II‐1. The nonretinorecipient SC projections to the pulvinar arise mainly from the deep layers, i.e., IV, V, and VI, and end in focus 4 within the medial pulvinar and the caudal oral pulvinar. The projection from the deep SC layer to the medial half of focus 3 in the medial pulvinar has already been described above.

A pretectal projection to the lateral pulvinar from the retinorecipient region consisting of the nucleus of the optic tract, the sublentiform nucleus, and the posterior pretectal nucleus (collectively called SL in our previous study, Benevento et al., 1977b) was confirmed. This projection forms a focus (focus 5) in the dorsal shoulder of the rostral lateral pulvinar, which extends over foci 1 and 3. Our HRP data indicate that these pretectal nuclei might have convergent projections with the SC to foci 1 to 4 and the DLG. How‐ ever, because of the problem of interruption of fibers of passage, this inter‐ pretation of convergent projections should be viewed with caution. The HRP studies also indicate that the parabigeminal nucleus, which is inter‐ connected with the SC, projects to the thalamus, as it contained a modest number of labelled cells after injections of the inferior pulvinar and focus 2 in PL‐alpha, but only a sparse number after injections of the DLG and focus 1.

These results suggest that direct retinal influences can be relayed to visually responsive association cortex via retino‐tectal‐lateral pulvinar, retino‐pretectal‐lateral pulvinar, and retino‐tecto‐parabigeminal‐lateral pulvinar routes in addition to the retino‐tectal‐geniculate and retino‐tectal‐inferior pulvinar routes. In addition, visuomotor and polysensory information influences thalamocortical systems via projections from the deep layers of the SC to the medial pulvinar. When these findings are compared with the known organization of pulvinocortical interconnections one can conclude that the cortex of all four neocortical lobes can be influenced rather directly by the midbrain. The response properties of the various cortical visual areas, thus, need not depend solely upon the corticocortical projections.