Vestibular nucleus neurons respond to hindlimb movement in the conscious cat

Abstract

The limbs constitute the sole interface with the ground during most waking activities in mammalian species; it is therefore expected that somatosensory inputs from the limbs provide important information to the central nervous system for balance control. In the decerebrate cat model, the activity of a subset of neurons in the vestibular nuclei (VN) has been previously shown to be modulated by hindlimb movement. However, decerebration can profoundly alter the effects of sensory inputs on the activity of brain stem neurons, resulting in epiphenomenal responses. Thus, before this study, it was unclear whether and how somatosensory inputs from the limb affected the activity of VN neurons in conscious animals. We recorded brain stem neuronal activity in the conscious cat and characterized the responses of VN neurons to flexion and extension hindlimb movements and to whole body vertical tilts (vestibular stimulation). Among 96 VN neurons whose activity was modulated by vestibular stimulation, the firing rate of 65 neurons (67.7%) was also affected by passive hindlimb movement. VN neurons in conscious cats most commonly encoded hindlimb movement irrespective of the direction of movement (n = 33, 50.8%), in that they responded to all flexion and extension movements of the limb. Other VN neurons overtly encoded information about the direction of hindlimb movement (n = 27, 41.5%), and the remainder had more complex responses. These data confirm that hindlimb somatosensory and vestibular inputs converge onto VN neurons of the conscious cat, suggesting that VN neurons integrate somatosensory inputs from the limbs in computations that affect motor outflow to maintain balance.

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.…”

“…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.…”

“…A series of experiments from our laboratory showed that the activity of a population of VN neurons is modulated by hindlimb movement (Arshian et al 2014; McCall et al 2016), building upon earlier work demonstrating that VN neurons respond to electrical stimulation of hindlimb nerves (Wilson et al 1966; Jian et al 2002; McCall et al 2013). This evidence leads to speculation that some VN neurons integrate limb somatosensory and labyrinthine inputs to adjust vestibulospinal outflow in accordance with limb state when a postural perturbation occurs (Arshian et al 2014).…”