Two distinct populations of tectal neurons have unique connections within the retinotectorotundal pathway of the pigeon (Columba livia)

The tectofugal pathway is a massive ascending polysynaptic pathway from the tectum to the thalamus and then to the telencephalon. In birds, the initial component of this pathway is known as the tectorotundal pathway; in mammals, it is known as the tectopulvinar pathway. The avian tectorotundal pathway is highly developed; thus, it provides a particularly appropriate model for exploring the fundamental properties of this system in all amniotes. To further define the connectivity of the tectorotundal projections of the tectofugal pathway, we injected cholera toxin B fragment into various rotundal divisions, the tectobulbar projection, and the ventral supraoptic decussation of the pigeon. We found intense bilateral retrograde labeling of neurons that stratified within layer 13 and, in certain cases, granular staining in layer 5b of the optic tectum. Based on these results, we propose that there are two distinct types of layer 13 neurons that project to the rotundus: 1) type I neurons, which are found in the outer sublamina of layer 13 (closer to layer 12) and which project to the anterior and centralis rotundal divisions, and 2) type II neurons, which are found in the inner sublamina of layer 13 (closer to layer 14) and which project to the posterior and triangularis rotundal divisions. Only the labeling of type I neurons produced the granular dendritic staining in layer 5b. An additional type of tectal neuron was also found that projected to the tectobulbar system. We then injected Phaseolus vulgaris-leucoagglutinin in the optic tract and found that the retinal axons terminating within tectal layer 5b formed narrow radial arbors (7-10 microm in diameter) that were confined to layer 5b. Based on these results, we propose that these axons are derived from a population of small retinal ganglion cells (4.5-6.0 microm in diameter) that terminate on the distal dendrites of type I neurons. This study strongly indicated the presence of a major bilateral oligosynaptic retinotectorotundal pathway arising from small retinal ganglion cells projecting to the rotundus with only a single intervening tectal neuron, the proposed type I neuron. We suggest that a similar organization of retinotectopulvinar connections exist in reptiles and in many mammals.