Structure-function relationships in the primate superior colliculus. I. Morphological classification of efferent neurons

Neurons in the superior colliculus (SC) of anesthetized paralyzed squirrel monkeys were injected intracellularly with horseradish peroxidase (HRP) to establish a morphological classification of tectal efferent neurons in this species. These neurons were physiologically identified by their antidromic responses following stimulation of the contralateral predorsal bundle or SC. These cells also responded with postsynaptic potentials to stimulation of the ipsilateral substantia nigra and cerebral peduncle and the contralateral tectum. 2. Quantitative light microscopic analysis of the somatodendritic profiles and axonal trajectories of 27 recovered cells revealed the existence of three major groups of tectal efferent neurons: L (n = 7), X (n = 8), and T (n = 12). 3. L neurons are small or medium size cells with relatively elaborate dendritic trees and are located mainly in the superficial layers of the SC. They participate in the ipsilateral descending and dorsal ascending tectofugal bundles. Intrinsic collaterals of L axons deploy a large number of boutons both near the parent cell body and more ventrally within the deeper tectal layers. 4. X neurons are mostly large in size and multipolar in shape with relatively complex dendritic trees. Their cell bodies are situated mainly in the stratum griseum intermedium and occasionally in the stratum opticum. Axons of X neurons participate in the crossed descending and ipsilateral ventral ascending projections of the SC. In addition, the axonal system of about half of the X neurons includes recurrent collaterals. 5. T neurons are located mainly in the ventral stratum opticum and the dorsal stratum griseum intermedium. They have small or medium-sized, trapezoid or ovoid cell bodies and relatively simple radiating or vertical dendritic trees. Their axons usually participate in two of the major tectofugal bundles besides providing a commissural component and recurrent collaterals. 6. Morphological details revealed in the present study support the notion that distinct tectofugal axonal systems originate from efferent neurons of the primate SC that differ both as to their location in the tectum as well as the appearance of their somata and dendritic trees. The resulting morphological classification of tectal efferent cells provides a framework for the analysis of tectal function in terms of populations of identified neurons.