Responses of non-eye-movement central vestibular neurons to sinusoidal yaw rotation in compensated macaques after unilateral semicircular canal plugging

Abstract

After vestibular labyrinth injury, behavioral measures of vestibular performance recover to variable degrees (vestibular compensation). Central neuronal responses after unilateral labyrinthectomy (UL), which eliminates both afferent resting activity and sensitivity to movement, have been well-studied. However, unilateral semicircular canal plugging (UCP), which attenuates angular-velocity detection while leaving afferent resting activity intact, has not been extensively studied. The current study reports response properties of yaw-sensitive non-eye-movement rhesus macaque vestibular neurons after compensation from UCP. The responses at a series of frequencies (0.1-2 Hz) and peak velocities (15-210°/s) were compared between neurons recorded before and at least 6 wk after UCP. The gain (sp/s/°/s) of central type I neurons (responding to ipsilateral yaw rotation) on the side of UCP was reduced relative to normal controls at 0.5 Hz, ±60°/s [0.48 ± 0.30 (SD) normal, 0.32 ± 0.15 ipsilesion; 0.44 ± 0.2 contralesion]. Type II neurons (responding to contralateral yaw rotation) after UCP have reduced gain (0.40 ± 0.27 normal, 0.35 ± 0.25 ipsilesion; 0.25 ± 0.18 contralesion). The difference between responses after UCP and after UL is primarily the distribution of type I and type II neurons in the vestibular nuclei (type I neurons comprise 66% in vestibular nuclei normally; 51% ipsilesion UCP; 59% contralesion UCP; 38% ipsilesion UL; 65% contralesion UL) and the magnitude of the responses of type II neurons ipsilateral to the lesion. These differences suggest that the need to compensate for unilateral loss of resting vestibular nerve activity after UL necessitates a different strategy for recovery of dynamic vestibular responses compared to after UCP.

Keywords: brainstem; threshold; vestibular nucleus.

Fig. 1.

One example neuron (type I neuron prelesion) analyzed for direction threshold. The top traces are the response of the neuron (after Kaiser window filtering; black) and the head velocity (gray). The timing of the stimulus and response have been aligned by adjusting for the phase difference (in this example, 50° phase lead). deg, Degrees. The raster plot (middle) shows the actual spike times over 23 cycles. The table (bottom) shows the number of cycles in this example where there were more spikes for the bins immediately before or after the transition from excitatory to inhibitory or inhibitory to excitatory, respectively (sign test = + when the number of spikes is greater in the expected bin when comparing the bins immediately before or after the crossing). P values for 1-tailed sign test.

Fig. 2.

Responses of recorded neurons in the prelesion vestibular nuclei (top), ipsilesion nuclei (middle), and contralesion nuclei (bottom) at 0.5 Hz, ±60°/s. Open circles represent individual neurons, phase re: velocity is the θ measure, and gain is the radial distance from the center. For prelesion, all neurons represented as if on the right side (neurons recorded on the left with phases shifted ±180°). Red squares are the mean of gain and phase for prelesion neurons. Black, filled circles are postlesion mean responses. The contralesion mean type I response is obscured by the red square (lower left plot).

Fig. 3.

Bode plots showing gain (upper plots) and phase (lower plots) of type I (left) and type II (right) NEM neurons in the ipsilateral (top) and contralateral (bottom) nuclei after UCP compared with prelesion. Type is determined by response phase at 0.5 Hz, ±60°/s. Peak velocity 60°/s for all data. Individual neuron responses demonstrated by open, red squares for the NEM neurons before lesion and black circles for the NEM neurons after lesion. Mean prelesion values are demonstrated by thick, red line, and the post-UCP values are demonstrated by thick, black line. Prelesion data from both sides of the midline are combined with phases for neurons recorded on the opposite side adjusted by 180°. For prelesion data, there were 33, 41, 36, 79, 37, 46, 37, and 43 type I neurons reported and 18, 26, 23, 42, 23, 29, 23, and 29 type II neurons reported at 0.1, 0.2, 0.3, 0.5, 0.8, 1.0, 1.5, and 2.0 Hz, respectively. After UCP, the respective neurons shown at each of these same frequencies are 15, 17, 6, 20, 16, 18, and 8 for ipsilesion type I; 11, 11, 3, 18, 13, 17, 7, and 10 for ipsilesion type II; 29, 32, 15, 42, 32, 34, 19, and 21 for contralesion type I; and 20, 21, 8, 28, 21, 22, 10, and 12 for contralesion type II. Gain plots are log-log, phase plots log on x-axis only. Arrows denote statistically significant differences between prelesion and post-UCP groups. Data points are artificially offset horizontally to improve clarity.

Fig. 4.

Gain and phase vs. peak velocity for the 4 groups of NEM neurons after UCP compared with control data prelesion. Type is determined by response phase at 0.5 Hz, ±60°/s. All data at 0.5 Hz. Peak velocities at 15, 30, 60, 90, 120, 150, 180, and 210°/s. In all of the plots, the prelesion control data are shown by open, red boxes (individual responses) and thick, red line (average of responses). For the lesion data, the individual values (open, black circles) and the average values (thick, black lines) are shown. The control values reflect neurons on both sides of the brain stem, with phases for neurons recorded on the opposite side adjusted by 180°. For prelesion data, there were 18, 39, 80, 40, 32, 36, 35, and 30 type I neurons reported and 10, 22, 23, 12, 13, 12, 10, and 7 type II neurons reported at 15, 30, 60, 90, 120, 150, 180, and 210°/s, respectively. After UCP, the respective neurons shown at each of these same peak velocities are 3, 13, 20, 11, 9, 6, 6, and 6 for ipsilesion type I; 3, 8, 18, 6, 8, 5, 4, and 4 for ipsilesion type II; 10, 24, 42, 26, 17, 13, 13, and 12 for contralesion type I; and 7, 16, 28, 15, 10, 7, 6, and 5 for contralesion type II. Gain plots are log on x-axis only, and phase plots are linear. Arrows denote statistically significant differences between prelesion and post-UCP groups. Data points are artificially offset horizontally to improve clarity.

Fig. 5.

Gain and phase vs. frequency at peak velocity 60°/s comparing prelesion (current study; red), UCP (current study; black), and UL (Newlands and Wei 2013a; gray) mean responses. Error bars = SE. Data points are artificially offset horizontally to improve clarity. Prelesion and UCP averages as in Fig. 3, but gain scale is linear to improve clarity.

Fig. 6.

Gain and phase vs. peak velocity at 0.5 Hz comparing prelesion (current study; red), UCP (current study; black), and UL (Newlands and Wei 2013a; gray) mean responses. Error bars = SE. Data points are artificially offset horizontally to improve clarity. Prelesion and UCP averages as in Fig. 3, but gain scale is linear to improve clarity.

Fig. 7.

Schematic of basic circuitry in the vestibular nuclei and the potential sites of plasticity after UCP or UL. Filled triangles, inhibitory connections; open triangles, excitatory connections.