Bottlebrush dendritic endings and large dendritic fields: motion-detecting neurons in the tectofugal pathway

Abstract

In avian and mammalian brains, visual information from the retina is conveyed to the telencephalon via two separate pathways: the thalamofugal and the tectofugal pathways. Recently, Karten et al. ([1997] J. Comp. Neurol. 387:449-465) examined a portion of the tectofugal pathway, the projection from the optic tectum to the nucleus rotundus thalami, in pigeons. They defined two distinct subpopulations of tectal neurons projecting from the stratum griseum centrale (SGC; tectal layer 13) to specific divisions of the rotundus. The goal of this study in chick was to verify the existence of the type I and type II SGC neurons, as defined by Karten et al., and then examine in greater detail the connectivity and morphology of these SGC neurons. Furthermore, our results suggest how the unique morphological characteristics of SGC neurons contribute to the large receptive fields (20-50 degrees) found in physiological recordings and the SGC neuronal response to extremely small (ca. 0.05 degree), fast-moving (100 degrees/second) stimuli. By injecting retrograde tracer into various divisions of the chick rotundus, we verified that, indeed, the chick did possess type I and type II SGC neurons, as well as a "new" type of SGC neuron, type III, that is not found in the pigeon. We then used intracellular cell-filling techniques to define further these three types of SGC neurons. Our examination revealed the following: Type I SGC neurons had large, circular dendritic fields (average diameter, 1,725 microns) composed of smooth dendrites and ending in spine-rich, bottlebrush endings located in retinorecipient tectal layer 5b; type II SGC neurons had elliptical dendritic fields (average 1,447 microns) and dendritic endings located never more superficially than tectal layer 8; and type III SGC neurons had large dendritic fields (average 1,800 microns) of unknown shape and bottlebrush dendritic endings located in retinorecipient tectal layer 4. We suggest that the neuronal features of the SGC neurons (i.e., bottlebrush dendritic endings and large dendritic fields) are key morphological characteristics for the detection of motion within the tectofugal pathway. Furthermore, because neurons with similar morphology have also been found in the tecta of both mammals and reptiles, we suggest that these neuronal features are fundamental components of a phylogenetically conserved system used for the "extrastriate" detection of motion in vertebrates.