Visual and nonvisual auditory systems in mammals. Anatomical evidence indicates two kinds of auditory pathways and suggests two kinds of hearing in mammals.

Abstract

Examination of the structural organization of the auditory system of the brain stem shows that the system is composed of a number of separate ascending pathways. This suggests that there may be at least two auditory systems, analogous to the rod and cone pathways in vision. We examined this possibility by investigating the variation in relative size of the medial and lateral superior olivary nuclei in a number of different mammalian species. The lateral superior olive is present in the hedgehog (an insectivore), cat (acarnivore), and squirrel monkey a(primate), but the medial superior olive is absent in the hedgehog. In a group of animals of the same taxonomic order (rodents) the lateral superior olive was present in all species examined, but the medial superior olive was almost wholly absent in the mouse and very prominent in the chinchilla and guinea pig. The absence of the medial superior olive in some animals is surprising because recent anatomical and physiological work has implicated the nucleus in auditory localization. Because of this implication, the medial and lateral olivary nuclei were examined in three species of bat and one dolphin, all echolocating animals. The medial superior olive was absent in these animals, and the lateral superior olive was prominent. These observations support the idea that the medial and lateral superior olives are nuclei on two different ascending auditory systems. It was also noted that the medial superior olive was always well developed in animals with well-developed eyes, and this suggested that the nucleus is in some way related to the visual system. We examined this idea by studying the relation between the numbers of cells in the medial superior olive and in the nucleus of the 6th cranial nerve (one of the motor nuclei concerned with eye movement) in a number of mammalian species. An approximately linear function was found between the sizes of the 6th nucleus and of the medial superior olive in three primates with cone-cell retinas (squirrel monkey, man, and macaque) and four rodents with rod-cell retinas (mouse, rat, guinea pig, and chinchilla). The cell numbers for the ground squirrel (a rodent with cone-cell retina) fitted an extension of the primate curve, and the cell numbers for the cat (in whose retina rods predominate) fitted an extension of the rodent curve. Thus, it is clear that the medial superior olive is related to the visual system, and that it is present in animals with cone-cell fovea and retina (diurnalanimals) and animals with rod-cell retina (that is, nocturnal animals) having good vision. In nonvisual nocturnal animals the nucleus is small or absent. The medial superior olive is probably not concerned with auditory localization in the psychophysical sense but is probably concerned with the movement of head and eyes in the direction of a sound in space. Localization in the psychophysical sense and fine auditory discrimination probably depend upon the ascending pathway which includes the lateral superior olive.