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

Abstract

Sadeghi SG, Minor LB, Cullen KE. Multimodal integration after unilateral labyrinthine lesion: single vestibular nuclei neuron responses and implications for postural compensation. J Neurophysiol 105: 661-673, 2011. First published December 8, 2010 doi:10.1152/jn.00788.2010. Plasticity in neuronal responses is necessary for compensation following brain lesions and adaptation to new conditions and motor learning. In a previous study, we showed that compensatory changes in the vestibuloocular reflex (VOR) following unilateral vestibular loss were characterized by dynamic reweighting of inputs from vestibular and extravestibular modalities at the level of single neurons that constitute the first central stage of VOR signal processing. Here, we studied another class of neurons, i.e., the vestibular-only neurons, in the vestibular nuclei that mediate vestibulospinal reflexes and provide information for higher brain areas. We investigated changes in the relative contribution of vestibular, neck proprioceptive, and efference copy signals in the response of these neurons during compensation after contralateral vestibular loss in Macaca mulata monkeys. We show that the time course of recovery of vestibular sensitivity of neurons corresponds with that of lower extremity muscle and tendon reflexes reported in previous studies. More important, we found that information from neck proprioceptors, which did not influence neuronal responses before the lesion, were unmasked after lesion. Such inputs influenced the early stages of the compensation process evidenced by faster and more substantial recovery of the resting discharge in proprioceptive-sensitive neurons. Interestingly, unlike our previous study of VOR interneurons, the improvement in the sensitivity of the two groups of neurons did not show any difference in the early or late stages after lesion. Finally, neuronal responses during active head movements were not different before and after lesion and were attenuated relative to passive movements over the course of recovery, similar to that observed in control conditions. Comparison of compensatory changes observed in the vestibuloocular and vestibulospinal pathways provides evidence for similarities and differences between the two classes of neurons that mediate these pathways at the functional and cellular levels.

Sequential [18F]FDG µPET whole-brain imaging of central vestibular compensation: a model of deafferentation-induced brain plasticity

“…The vestibular nuclei are embedded in sensorimotor networks, through which proprioceptive information reaches the vestibular nuclei from the central cervical and spinal trigeminal nucleus (Sato et al 1997). After unilateral labyrinthectomy, proprioceptive inputs to the vestibular nuclei are unmasked and enhanced (Sadeghi et al 2011;Beraneck and Idoux 2012;Jamali et al 2013). Patients with vestibular neuritits displayed an enhanced sensitivity to ipsilesional neck vibration and a gray matter volume increase of the gracile nucleus (Strupp et al 1998;zu Eulenburg et al 2010).…”

Getting ahead of oneself: Anticipation and the vestibulo-ocular reflex

“…The basic pathway underlying the reflex is remarkably simple: a 3-neuron arc that links receptors and primary neurons located in the inner ear to the extraocular muscles of the eye (Lorente de No, 1933). Numerous studies over the past 50 years have characterized the connectivity and discharge properties of the peripheral neurons in the inner ear (Goldberg and Fernandez, 1971c; Goldberg and Fernandez, 1971b; Goldberg and Fernandez, 1971a); secondary vestibular neurons in the vestibular nuclei (Precht and Shimazu, 1965; Precht and Baker, 1972; Fuchs and Kimm, 1975a; Buttner and Waespe, 1981; Tomlinson and Robinson, 1984; McCrea et al, 1987; Scudder and Fuchs, 1992; Stahl and Simpson, 1995; Ris et al, 1995a; Phillips et al, 1996; Serafin et al, 1999; Gdowski and McCrea, 1999; Roy and Cullen, 2001; Cullen and Roy, 2004; Roy and Cullen, 2004; Beraneck and Cullen, 2007), and plasticity and motor learning within the VOR pathways (Gonshor and Jones, 1976; Lisberger et al, 1994; Lisberger, 1994; Miles and Lisberger, 1981a; Sadeghi et al, 2010; Sadeghi et al, 2011). Measurement of eye movements produced by the VOR is an essential component of contemporary clinical tests of vestibular function, largely based on methods established by Barany for which he received the Nobel Prize in 1914 (for an example of Barany’s teachings translated into English, see Ibershoff and Copeland, 1910; for a review of clinical applications, see Leigh and Zee, 2006; Baloh and Halmagyi, 1996).…”

Vestibular control of the head: possible functions of the vestibulocollic reflex

“…For example, while it is robust in animals that make minimal eye movements such as pigeons (Gioanni 1988) or owls (Money and Correia 1972), its contribution to head stabilization has been described as less significant in macaque monkeys and humans—species that have large (~50°) oculomotor ranges (Guitton et al 1986; Sadeghi et al in press). For example, when human subjects are distracted by mental arithmetic, the most substantial part of active yaw-axis stabilization at low frequencies (<1 Hz) is generated by longer-latency voluntary mechanisms, suggesting that the VCR contribution is negligible (Guitton et al 1986; Keshner and Peterson 1995).…”