Hindlimb movement modulates the activity of rostral fastigial nucleus neurons that process vestibular input

Abstract

Integration of vestibular and proprioceptive afferent information within the central nervous system is a critical component of postural regulation. We recently demonstrated that labyrinthine and hindlimb signals converge onto vestibular nucleus neurons, such that hindlimb movement modulates the activity of these cells. However, it is unclear whether similar convergence of hindlimb and vestibular signals also occurs upstream from the vestibular nuclei, particularly in the rostral fastigial nucleus (rFN). We tested the hypothesis that rFN neurons have similar responses to hindlimb movement as vestibular nucleus neurons. Recordings were obtained from 53 rFN neurons that responded to hindlimb movement in decerebrate cats. In contrast to vestibular nucleus neurons, which commonly encoded the direction of hindlimb movement (81% of neurons), few rFN neurons (21%) that responded to leg movement encoded such information. Instead, most rFN neurons responded to both limb flexion and extension. Half of the rFN neurons whose activity was modulated by hindlimb movement received convergent vestibular inputs. These results show that rFN neurons receive somatosensory inputs from the hindlimb, and that a subset of rFN neurons integrates vestibular and hindlimb signals. Such rFN neurons likely perform computations that participate in maintenance of balance during upright stance and movement. Although vestibular nucleus neurons are interconnected with the rFN, the dissimilarity of responses of neurons sensitive to hindlimb movement in the two regions suggest that they play different roles in coordinating postural responses during locomotion and other movements which entail changes in limb position.

Neurons in the pontomedullary reticular formation receive converging inputs from the hindlimb and labyrinth

“…2. Responses to hindlimb movement were categorized as in previous studies (Arshian et al 2014; McCall et al 2015; McCall et al 2016). The firing rate of omnidirectional neurons changed similarly during both flexion and extension movements of the hindlimb, but returned to baseline levels when the limb was held in the new position (Fig.…”

“…Interestingly, many neurons in CNS sites that participate in postural control exhibit omnidirectional responses to passive hindlimb movement, including 77% of neurons in the rostral fastigial nucleus of decerebrate cats (McCall et al 2015), 51% of neurons in the caudal vestibular nuclei (51%) in conscious cats (McCall et al 2016), and 61% of pmRF neurons in conscious cats. Thus, it is common for the activity of brainstem and cerebellar neurons to be modulated during limb movements in any direction.…”

“…Neuronal recordings were obtained from 7 animals after decerebration and the removal of anesthesia. The other four felines were instrumented for chronic single-unit recordings using procedures described previously (Miller et al 2008a; Miller et al 2008b; McCall et al 2015). …”

“…1). As described in previous publications, this stimulus paradigm provides for flexion and extension movements of the limb only about the hip and knee joints (Arshian et al 2014; McCall et al 2015; McCall et al 2016). The hindlimb is secured to the servo-controlled motor in a position comfortable for the animal with roughly orthogonal angles about the hip and knee joint; this position is referred to as midline (neutral) (Fig.…”

“…To determine if hindlimb movement resulted in an appreciable change in neuronal firing, spike counts were binned in 0.1 sec intervals and composite response histograms were generated, as in previous studies (Arshian et al 2014; McCall et al 2015; McCall et al 2016). Each ramp segment was then analyzed for a change in activity relative to the baseline.…”