Different neural strategies for multimodal integration: comparison of two macaque monkey species

Abstract

The integration of neck proprioceptive and vestibular inputs underlies the generation of accurate postural and motor control. Recent studies have shown that central mechanisms underlying the integration of these sensory inputs differ across species. Notably, in rhesus monkey (Macaca mulata), an Old World monkey, neurons in the vestibular nuclei are insensitive to passive stimulation of neck proprioceptors. In contrast, in squirrel monkey, a New World monkey, stimulation produces robust modulation. This has led to the suggestion that there are differences in how sensory information is integrated during self-motion in Old versus New World monkeys. To test this hypothesis, we recorded from neurons in the vestibular nuclei of another species in the Macaca genus [i.e., M. fascicularis (cynomolgus monkey)]. Recordings were made from vestibular-only (VO) and position-vestibular-pause (PVP) neurons. The majority (53%) of neurons in both groups were sensitive to neck proprioceptive and vestibular stimulation during passive body-under-head and whole-body rotation, respectively. Furthermore, responses during passive rotations of the head-on-body were well predicted by the linear summation of vestibular and neck responses (which were typically antagonistic). During active head movement, the responses of VO and PVP neurons were further attenuated (relative to a model based on linear summation) for the duration of the active head movement or gaze shift, respectively. Taken together, our findings show that the brain’s strategy for the central processing of sensory information can vary even within a single genus. We suggest that similar divergence may be observed in other areas in which multimodal integration occurs.