EXCITATORY AND INHIBITORY INPUTS FROM SACCULAR AFFERENTS TO SINGLE VESTIBULAR NEURONS IN THE CAT

Connections from saccular afferents to vestibular neurons were studied by means of intracellular recordings of excitatory (E) and inhibitory (I) post-synaptic potentials (PSPs) in vestibular neurons after focal stimulation of the saccular macula in decerebrated cats. Focal stimul ation was given to the saccular macula in two ways, in which the polar ity of stimulus current via a pair of electrodes was changed. In group A, one of the electrodes was inserted into the ventral and the other into the dorsal edge of the saccular macula. The focal stimulation was across the striola so that the reversal of morphological polarization in hair cells was bridged by the pulse stimulus. In 22/36 vestibular neurons tested, the stimulation of the saccular macula evoked monosyna ptic (less than or equal to 1.2 ms) EPSPs, including EPSP-IPSP sequenc es, with one polarity of stimulation, and disynaptic (greater than or equal to 1.5 ms) IPSPs when the polarity of the stimulus current was c hanged. In 14/36 neurons, the response pattern was the same regardless of the stimulus polarity; EPSPs (12/36) or IPSPs (2/36). In group B, a pair of electrodes was inserted into the dorsal edge of the saccular macula, so that the striola was not bridged by the current stimulus. In all of the vestibular neurons tested, the response pattern was alwa ys the same regardless of the polarity: mono-(22/31) and disynaptic (3 /31) EPSPs or disynaptic IPSPs(6/31). In addition, the saccular nerve was stimulated after removing the macula in some cats (group C). The s timulation of the saccular nerve evoked EPSPs in 62 vestibular neurons (including EPSP-IPSP sequences in 31 neurons) and IPSPs in 19 vestibu lar neurons. Convergence between the saccular nerve and other vestibul ar nerves was studied by the intracellular recording of PSPs. Fifty-si x percent (18/32) of the saccular-activated neurons had excitatory and /or inhibitory potentials evoked after stimulation of the utricular ne rve and the horizontal and anterior semicircular canal nerves, and 44% ( 19/43) of the neurons received inputs from the posterior semicircul ar canal nerve. The results support the hypothesis that saccular affer ents from one population of hair cells activate vestibular neurons mon osynaptically and that afferents from another population of hair cells located on the opposite side of the striola appear to project to the same vestibular neurons disynaptically via inhibitory interneurons. Ne ural circuits from saccular afferents to vestibular neurons, which we term cross-striolar inhibition, thus may provide a mechanism for incre asing the sensitivity to vertical linear acceleration. The circuit des cribed is provided not only with high sensitivity but also with input noise-resistant characteristics.