Excitatory and inhibitory interactions of extraocular and dorsal neck muscle afferents in the cat frontal cortex

Abstract

Excitatory and inhibitory responses of 318 neurons to extraocular and dorsal neck muscle afferent stimulation were recorded extracellularly in the frontal cortex of 34 chloralose-anesthetized cats. Electrical stimulation of the oculomotor nerve to the ipsilateral and contralateral superior rectus muscle of the eye elicited single-cell responses in 33 and 40% of more than 160 cells tested, respectively, and stimulation of the abducens nerve to the lateral rectus muscle elicited responses in 47% of 161 cells tested, at latencies of 7 to 50 ms. Responses to a branch of the ipsilateral and contralateral biventer cervicis/complexus nerve of the dorsal neck were observed in 42 and 64% of more than 150 cells tested, respectively, and 32% of 165 cells responded to the contralateral rectus capitis dorsalis major/obliquus capitis caudalis nerve, at latencies of 5 to 47 ms. Inhibitory effects were evaluated extracellularly by observing the effect of electrical nerve stimulation against a background of glutamate-induced excitation of cells in the frontal cortex. Stimulation of extraocular muscle nerves inhibited activity in 20 of 93 cells, and dorsal neck muscle afferent fibers had inhibitory effects on 20 of 64 cells tested. Excitatory and inhibitory convergence between afferent fibers from one extraocular and one or more dorsal neck muscles was observed in 60% of 234 cells tested, and was higher than the degree of convergence between some pairs of extraocular muscle nerves, or between pairs of dorsal neck muscle nerves. The highest degree of convergence was between extraocular muscle afferent fibers and those from longitudinally extended dorsal neck muscles, which cause large head deviations upon contraction. The interacting effects of dorsal neck and extraocular muscle afferent fibers at comparable latencies in the cat frontal cortex suggest an involvement of these regions in coordinated eye and head movement.