Adaptation of spatio-temporal convergent properties in central vestibular neurons in monkeys

Abstract

The spatio-temporal convergent (STC) response occurs in central vestibular cells when dynamic and static inputs are activated. The functional significance of STC behavior is not fully understood. Whether STC is a property of some specific central vestibular neurons, or whether it is a response that can be induced in any neuron at some frequencies is unknown. It is also unknown how the change in orientation of otolith polarization vector (orientation adaptation) affects STC behavior. A new complex model, that includes inputs with regular and irregular discharges from both canal and otolith afferents, was applied to experimental data to determine how many convergent inputs are sufficient to explain the STC behavior as a function of frequency and orientation adaptation. The canal-otolith and otolith-only neurons were recorded in the vestibular nuclei of three monkeys. About 42% (11/26 canal-otolith and 3/7 otolith-only) neurons showed typical STC responses at least at one frequency before orientation adaptation. After orientation adaptation in side-down head position for 2 h, some canal-otolith and otolith-only neurons altered their STC responses. Thus, STC is a property of weights of the regular and irregular vestibular afferent inputs to central vestibular neurons which appear and/or disappear based on stimulus frequency and orientation adaptation. This indicates that STC properties are more common for central vestibular neurons than previously assumed. While gravity-dependent adaptation is also critically dependent on stimulus frequency and orientation adaptation, we propose that STC behavior is also linked to the neural network responsible for localized contextual learning during gravity-dependent adaptation.

Keywords: Canal-otolith and otolith-only neurons; four-component model; orientation adaptation; regular and irregular vestibular inputs; spatio-temporal convergence.

© 2018 The Authors. Physiological Reports published by Wiley Periodicals, Inc. on behalf of The Physiological Society and the American Physiological Society.

Figures

Figure 1

Photomicrographs of three frontal sections through the vestibular nuclei of two monkeys C101‐07 (A) and C102‐07 (B and C), showing some of the glial scars marking the electrode tracks (arrows) which yielded the unit recordings. In (A) C101‐07 the tracks are centered on the SV of both sides, and on the right side the two darker, fresh tracks (containing erythrocytes) mark the site of the DiO injection (arrow head). In (B) C102‐07 the unit recording tracks also pass through rostral SV, and the site of the DiO deposit can be seen in right MV (arrow head); (C) is a more rostral section of C102‐07 than B, and recording tracks are found in the rostral SV of both sides and on the border of the left rostral MV and LV lateral to nVI (arrowhead). Abbreviations are: 4v – fourth ventricle; BC – brachium conjunctivum; DN – dentate nucleus; DV – descending vestibular nucleus; LV – lateral vestibular nucleus; MV – medial vestibular nucleus; nVI – abducens nucleus; RB – restiform body; SV – superior vestibular nucleus.

Figure 2

(A) Diagram of spatial coordinate system and stimuli axes in 3‐D. (B) The position of the right labyrinth of a monkey in stereotaxic head coordinate system. (C) Modulation of the firing rate of a vestibular neuron (Unit#4) during rotation about a spatial vertical axis with the head tilted forward and backward in 15° increments. The figure shows FR modulations with 30° increments. (D, E) Temporal sensitivities and phases of the neuron plotted as function of head orientation and fitted by a cosine (dark line in D). This central vestibular neuron did not modulate relative to velocity with head tilted at 30° forward, but modulated maximally (0.26 ± 0.017 imp*s−1/deg*s−1) with head tilt backward at 65 ± 4°. That indicates input from ipsilateral VC; namely, this neuron had input from right posterior VC. Range of maximal spatial sensitivities relative to head orientation in pitch axis for different canal convergences in central neurons: single LC (tilt forward at 30 ± 15°, gray segment), single VC (tilt backward at 50 ± 15°, dark gray segment), LC and VC from different labyrinths (white segment), LC and VC from same labyrinth (light‐gray segments).

Figure 3

Determination of response vector orientation (RVO) in the central otolith‐related neurons (example of an otolith‐only neuron, Unit #3o). (A) Changes in neuronal firing rate (Unit FR) in response to 30° head tilts (Tilt) in various head orientations in yaw with regard to acceleration of gravity ag in head coordinates. Inset above shows orientation of ag fixed in space and relative to the head (upward arrows). Values below are the angles for each inset. Resting FR is neuronal spontaneous discharge in upright head position (white dashed line). (B) Unit FR from A, plotted as a function of the angle of ag in head coordinates (lower x‐scale) and converted to sensitivity. The head orientation in yaw is labeled on the upper x‐scale. The vertical dashed line indicates the location of the peak of the sinusoidal fit through the data (Smax). (C) Summary of the RVO computation. The angle corresponding to RVO was 335° in head horizontal plane.

Figure 4

Responses of a canal–otolith convergent neuron (Unit #5) during sinusoidal rotations about an earth‐horizontal (pitch/roll) axis with different head orientations in yaw plane. (A) Modulation of unit FR for oscillations at 0.2 Hz with peak tilt amplitude of 23°. (B, C) Modulations of unit FR for oscillations at 0.05 Hz with peak tilt amplitude of 80° and 23°, respectively. Each unit was tested at 15° increments in yaw axis. The figure shows FR modulations with 30° increments for oscillations before orientation adaptation re‐gravity. Inset on the right is an angle cartoon of relative head orientation in yaw to the axis of oscillations. Stimulus velocity (solid line) and stimulus position (dotted line) during oscillations at different tested frequencies and peak tilt amplitudes are shown on the bottom traces. Bold curves in each panel represent the sinusoidal fits of the data (A–C). The vertical dashed line indicates a time of the head peak velocity, the asterisks the peaks of the neuronal responses, which varied with the head orientation in yaw plane. Sensitivity (D, E, F) and phase (G, H, I) of the neuron are calculated with respect to velocity and plotted as a head orientation in yaw plane to the axis of oscillation before (A, B, C, open symbols) and after (filled symbols) head re‐orientation for 2 h. The changes in temporal sensitivity and phase as a function of head orientation in yaw were well approximated using the two‐component model (Eg. 1) comprising regular canal and otolith inputs (bold dashed gray curves in D–I, data before). The data were also fitted by the four‐component or complex model (Eq.4) before (solid black curves) and after (dashed black curves) orientation adaptation re‐gravity. (J) Summary polar plot that shows orientation of RVO (arrows) and canal‐related input (drumsticks) experimentally determined (black) and the two‐component model predicted for 0.2 Hz (solid gray) and for oscillations at 0.05 Hz with peak amplitude of 80° (dashed gray) and 23° (dashed light gray). (K) Calculation of slopes (α) using phase changes versus head orientations in yaw for non‐STC (filled squares) and typical STC (open diamonds) responses. Open squares show phase changes of non‐STC behavior for unit modulation at 0.2 Hz with peak amplitude of 23° (A), where unit modulates only to velocity having two levels of phases, ±180° (open squares) thereby the phases can be converted to similar level (filled squares). Open diamonds show phase changes of STC response for the unit modulation at 0.05 Hz with peak amplitude of 23° (C), where phases monotonically change in yaw plane from in‐phase with head velocity to head position and cannot be converted to same level. Each phase curve plotted vs. head orientation was approximated by linear function: y = A+ α*x, where α – slope of linear function was examined. For non‐STC responses the slope of phase curve was 0.0015 (dotted line) and for STC responses the slope was 1.09 (solid line). The range of temporal phases within ±45° relative to velocity stimulus is shown in gray segments, those for position stimulus is shown in white segments.

Figure 5

(A, B) Sensitivities and phases obtained from canal–otolith convergent neurons (Unit #15 in A a–d and Unit #11 in B a–f) by oscillations about earth‐horizontal axis at 0.2 Hz and 0.05 Hz in different head orientations in yaw plane relative to the axis of oscillation (abscissa). Open symbols are experimental data; gray dashed curve is two‐component model fits through the data, while solid curve is four‐component model fit. Ae, Bg, Insets show orientations of the semicircular canal (drumsticks) and RVO (arrows) that were experimentally measured (black) and predicted by the two‐component model for 0.2 Hz (solid gray) and for oscillations at 0.05 Hz with peak amplitude of 50° (dashed gray) and 23° (dashed light gray), respectively.

Figure 6

Sensitivities (A, C) and phases (B, D) obtained from an otolith‐only neuron (Unit #1o) by oscillations about earth‐horizontal axis at 0.2 Hz and 0.05 Hz with peak tilt amplitude of 23° in different head orientations in yaw plane (abscissa). Symbols are experimental data obtained before (open circles) and after (filled circles) orientation adaptation; curves are two‐component model fits through the data. (E) Orientation of the dynamic/irregular otolith input (dashed arrows) and RVO (solid arrows) that were model predicted before (black) and after (gray) orientation adaptation. (F) Correlation of experimentally determined (abscissa) and two‐component model‐predicted (ordinate) orientation of static/regular otolith inputs is shown for all otolith‐only neurons tested at 0.2 Hz (open circles) and at 0.05 Hz (filled circles).

Figure 7

(A–D) Canal–otolith neurons (Units #1, #2, #4, #9) tested before (open symbols) and after (filled symbols) orientation adaptation. Sensitivities (A–C a & c, Da) and phases (A–C b & d, Db) plotted as head orientation in yaw plane (abscissa) during oscillations at 0.2 Hz and 0.05 Hz with different peak tilt velocities. Curves are the model fit through the data obtained before (solid lines) and after (dashed lines) orientation adaptation, with the four‐component model fit (black lines) and two‐component model fit (gray lines). (A–C f, Dd) RVO determined before (black solid curve) and after (black dashed curve) orientation adaptation. Note that experimentally determined canal‐related (black drumstick on inset above A‐C e, Dc) and otolith‐related inputs were closer to a single plane before (black arrow) compared to after (gray arrow) orientation adaptation re‐gravity for 2 h.