Orientation bias of neurons in the lateral geniculate nucleus of macaque monkeys

Abstract

The purpose of this investigation was to analyze the influence of stimulus orientation on the responses of individual neurons in the monkey's lateral geniculate nucleus (LGN). Our specific goals were to assess the prevalence and the degree of orientation tuning in the monkey LGN and to determine if the preferred stimulus orientations of LGN neurons varied as a function of receptive-field position. The primary motivation for this research was to gain insight into the receptive-field configuration of LGN neurons and consequently into the neural mechanisms which determine the spatial organization of LGN receptive fields in primates. In both the parvocellular and magnocellular layers, the responses of the majority of individual neurons to sine-wave gratings varied as a function of stimulus orientation. The influence of stimulus orientation was, however, highly dependent on the spatial characteristics of the stimulus; the greatest degree of orientation bias was observed for spatial frequencies higher than the cell's optimal spatial frequency. On a population basis, the degree of orientation bias was similar for all major classes of LGN neurons (e.g. ON vs. OFF center; parvocellular vs. magnocellular) and did not vary systematically with receptive-field eccentricity. At a given receptive-field location, LGN neurons, particularly cells in the parvocellular laminae, tended to prefer either radially oriented stimuli or stimuli oriented more horizontally than their polar axis. Our analyses of the orientation-dependent changes in spatial-frequency response functions, which was based on the Soodak et al., (1987; Soodak, 1986) two-dimensional, difference-of-Gaussian receptive-field model, suggested that the orientation bias in LGN neurons was due to an elongation of the receptive-field center mechanism which in some cases appeared to consist of multiple subunits. Direct comparisons of the orientation-tuning characteristics of LGN cells and their retinal inputs (S potentials) indicated that the orientation bias in the monkey LGN reflects primarily the functional properties of individual retinal ganglion cells. We conclude that orientation sensitivity is a significant property of subcortical neurons in the primate's geniculo-cortical pathway.