Cortical influences on the vestibular nuclei of the cat

Abstract

Our goal was to study potential substrates for cortical modulation of vestibular reflexes in the cat. In initial experiments, injections of wheat-germ-agglutinate-horseradish-peroxidase into Deiters' nucleus and the rostral descending nucleus revealed bilateral colonies of retrogradely filled neurons in cortical areas 6, 2, and 3a (about 60 cells per colony). In cats anesthetized with chloralose-urethane, we stimulated areas 2 and 3a with trains of pulses while recording from ipsilateral vestibular-nucleus neurons, which were characterized by their responses to sinusoidal tilts and tested for the presence of antidromic responses to stimulation of the upper cervical cord. A majority of the neurons was affected by cortical stimulation, showing either facilitation, inhibition, or a mixture of the two. Stimulation in area 2 was more effective than stimulation in area 3a. Despite the anatomic presence of direct cortico-vestibular projections, properties of facilitation and inhibition suggest that both were evoked by polysynaptic pathways. Cortical effects were broadly distributed to vestibular neurons without regard to responses of these neurons to sinusoidal tilts. There was no significant difference between effects on lateral and medial vestibulospinal tract neurons, but, as a group, vestibulospinal neurons were much more likely to be affected by cortical stimulation than neurons not antidromically activated from the C2 segment. We conclude that, by their influence on vestibulospinal neurons, neurons in cortical areas 2 and 3a should be able to modulate, in behaving animals, vestibular reflexes acting on the neck and limbs.

The thalamocortical vestibular system in animals and humans

“…The corticofugal influence on vestibular nuclei is further supported by electrophysiological recordings in vestibular nuclei while different vestibular cortical areas are electrically stimulated. Stimulation of areas 2 and 3a (Wilson et al, 1999), area 4 (Licata et al, 1987;Licata et al, 1990) and the FEF (Fukushima et al, 1984) modified the responses of vestibular nuclei neurons. Wilson et al (1999) showed that these responses are complex and can manifest as facilitation or inhibition of the vestibular neurons response, or by a combination of these effects.…”

“…Stimulation of areas 2 and 3a (Wilson et al, 1999), area 4 (Licata et al, 1987;Licata et al, 1990) and the FEF (Fukushima et al, 1984) modified the responses of vestibular nuclei neurons. Wilson et al (1999) showed that these responses are complex and can manifest as facilitation or inhibition of the vestibular neurons response, or by a combination of these effects. In addition, on the basis of the latency and properties of the effects, they proposed that corticofugal control of the vestibular nuclei would be evoked by polysynaptic pathways.…”

“…Anatomical studies using retrograde tracer injections into the vestibular nuclei, or anterograde tracer injections into the vestibular cortical areas, have been conducted in different monkey species (Akbarian et al, 1993(Akbarian et al, , 1994FaugierGrimaud and Ventre, 1989;Guldin et al, 1993;Ventre and Faugier-Grimaud, 1988), in the cat (Wilson et al, 1999) and in the rat (Nishiike et al, 2000). These studies showed that vestibular nuclei receive direct monosynaptic projections from PIVC, areas 2v, 3av, 7, VPS area (in area T3), premotor cortex (area 6), and anterior cingulate cortex (areas 23/6).…”

Immunoreactivity for calcium-binding proteins defines subregions of the vestibular nuclear complex of the cat

“…Fourth, cells of origin of efferent pathways are not uniformly distributed within a nucleus. For example, the vestibulospinal neurons in the inferior and medial nuclei are found only in restricted regions (Rose et al 1996;Wilson and Schor 1999). The same principles apply to all of the other connections of the VNC (reviews in Wilson and Melvill Jones 1979;Gerrits 1990;Barmack 2003).…”

“…Second, no major output arises from cells confined to only one of the nuclei. For example, vestibulospinal fibers arise from cells in the inferior and medial vestibular nuclei as well as from the lateral nucleus (Peterson and Coulter 1977;Akaike 1983;Bankoul and Neuhuber 1992;Donevan et al 1992;Rose et al 1996;McCrea et al 1999;Wilson and Schor 1999). Third, within each nucleus, afferent fibers from different sensory structures are not uniformly distributed but found in restricted regions (Imagawa et al 1995;Naito et al 1995).…”