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., macaca 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.

Multimodal Integration After Unilateral Labyrinthine Lesion: Single Vestibular Nuclei Neuron Responses and Implications for Postural Compensation

“…In this way, VO neurons and PVP neurons in rhesus monkeys are comparable after lesion (compare with Sadeghi et al 2010). Similar findings have been reported in studies performed in the vestibular nuclei of normal cats (Kasper et al 1988), squirrel monkeys (Gdowski et al 2001), and cynomolgus monkeys (Sadeghi et al 2009). …”

“…As such, VO neurons are similar to VOR interneurons (i.e., PVP neurons) in that neck inputs are unmasked only after lesion (Sadeghi et al 2010). Interestingly, in both studies, the percentage of neck-sensitive neurons observed after lesion (ϳ50%) was comparable to that observed in normal conditions in other species (Gdowski et al 2001;Kasper et al 1988;Sadeghi et al 2009). We suggest that the acute appearance of neck proprioceptive signals in the vestibular nuclei neurons of rhesus monkeys after lesion reveals neck-vestibular connections that are present before lesion, but make silent synapses on vestibular nuclei neurons that become active only when vestibular inputs are decreased.…”

“…The estimated coefficients Sv vest and Sa vest were then used to calculate each unit's modulation sensitivity [(spikes/s)/(°/s)] and phase shift (deg) relative to head velocity (Sadeghi et al 2009(Sadeghi et al , 2010. Note that because VO neurons are insensitive to eye movements, no eye-movement term was included in the regression model.…”

“…Because neuronal responses typically led rather than lagged body velocity, our formalization of the model included velocity and acceleration terms. Similar to vestibular sensitivities, the estimated coefficients were then used to calculate each unit's modulation sensitivity [(spikes/s)/(°/s)] and phase shift (deg) relative to velocity of body rotation (Sadeghi et al 2009). Similar to previous studies (e.g., Wilson and Schor 1999), we used a sensitivity threshold of 0.1 (spike/s)/(°/s) to divide neurons into responsive and unresponsive to neck proprioceptor stimulation.…”

Behavioral State Modulates the Activity of Brainstem Sensorimotor Neurons

“…In fact, many of the moderately active NEM neurons also responded in phase with stimulus position, preferred pitch and roll rotations, and modulated their firing rate with tail movements. Whether these neurons are also related to postural responses is unknown; however, NEM cells in other species have often been associated with vestibulospinal pathways (McCrea et al, 1999;Boyle, 2001;Sadeghi et al, 2009).…”