Physiology of peripheral neurons innervating otolith organs of the squirrel monkey. I. Response to static tilts and to long-duration centrifugal force

Abstract

1. The response to static tilts was studied in peripheral otolith neurons in the barbiturate-anesthetized squirrel monkey (Saimiri sciureus). Each unit was characterized by a functional polarization vector, which defines the axis of greatest sensitivity. A circumstantial criterion was used to assign units to the inferior (IN) or superior (SN) vestibular nerves. The former neurons should innervate the sacculus, the latter mainly the utriculus. Confirming pasting experiments, the polarization vectors for SN units lay near the plane of the utricular macula, those for IN units near the plane of the saccular macula. The polarization vectors for IN units were compared in two groups of animals. In one group, the vestibular nerve was intact; in the other, the superior nerve was sectioned. No differences were found and this, together with other observations, demonstrate that the sacculas in mammals functions mainly (if not solely) as an equilibrium organ. 2. The resting discharge of otolith neurons averages some 60 spikes/s, the sensitivity some 30-40 spikes/s-g. IN units tend to have slightly lower sensitivities than do SN units. IN units with upwardly directed (+Z) vectors have substantially higher resting discharges than do units with downwardly directed (-Z) vectors. The +Z units are also characterized by more linear force-response relations. 3. There is a strong positive relation between the resting discharge and sensitivity of units characterized by regular steady-state discharge patterns. A weaker, but statistically significant, relation is demonstrable for irregular units. It is suggested that the relation seen in regular units is the result of the neurons differing from one anothrer in terms of a receptor bias, a transduction gain, or both. Only the mechanism based on transduction gain is thought to be operative among the population of irregular units. 4. Centrifugal-force trapezoids were used to study the response adaptation to prolonged stimulation. Adaptation was more conspicious in irregular units and was characterized by perstimulus response declines and poststimulus secondary responses. For regular units, adaptive properties were similar during excitatory and inhibitory responses. For irregular units, response declines were larger during excitatory stimuli, secondary responses larger following inhibitory stimuli. Typically, response declines were most rapid at the start of the force plateau. A few units, all of them irregular, exhibited a delayed adaptation with response declines beginning only after a constant force had been maintained for 10-20 s. 5. Excitatory responses of regular units are almost always larger than inhibitory responses. This is so during both the dynamic and static portions of force trapezoids. A similar asymmetry is seen in the dynamic response of irregular units; static response asymmetries of the latter units are more variable.

Vestibular Signals in Primate Thalamus: Properties and Origins

“…4, net accel traces). As shown previously (Fernandez and Goldberg, 1976;Angelaki and Dickman, 2000;Angelaki et al, 2004), primary otolith afferents encode the net gravitoinertial acceleration, modulating similarly during translation or tilt, and transmit no motion information during the tilt minus translation condition. This was also the case for some thalamic cells (e.g., cell 1).…”

“…One of the cells (1) modulated similarly during the translation and tilt stimuli (note that the amplitude of the two movements was adjusted such that the components of linear acceleration along the interaural axis were identical) (see Materials and Methods). Thus, this cell's response could be explained by selective activation of otolith afferents, which have been shown to encode net linear acceleration regardless of whether the stimulus arises from actual translation or tilt relative to gravity (Fernandez and Goldberg, 1976;Angelaki et al, 2004). In contrast, cell 2 responded very differently during the translation and tilt stimuli.…”

Neuronal thresholds and choice-related activity of otolith afferent fibers during heading perception

“…First, how does the heading sensitivity of otolith afferents compare with central vestibular neurons? Are central vestibular neurons more sensitive than afferents because they have greater average modulation amplitudes than afferents (16)(17)(18)(19)(20)(21)(22)(23), or do changes in response variability counteract these differences in response gain? Second, do otolith afferents show choice-related activity, and how do CPs of afferents compare with CPs measured in central neurons and cortical areas?…”

Directional Asymmetries and Age Effects in Human Self-Motion Perception

“…The medial area of the utricle is larger than the lateral area in humans (Rosenhall 1972) and three quarters of the neurons respond preferentially to ipsilateral tilt in monkeys (Fernandez and Goldberg 1976). Transient linear motion produces a linear VOR (LVOR) which is commonly asymmetric at high accelerations in healthy humans (Lempert et al 1998;Crane et al 2003) and more asymmetric after an acute unilateral vestibular lesion, although symmetry returns to the normal range over time (Lempert et al 1998).…”