PMC

Spontaneous firing rates of NEM and EM neurons are state dependent. A, Representative NEM neuron's activity during transitions from default to flight state (left) and from flight to default state (right). Gray lines indicate airflow onset (ON) and offset (OFF). B, Mean (±SEM) spontaneous firing rates measured for each neuron during default (solid bars) and flight (hatched bars) states. A subset of neurons with the lowest spontaneous firing rates (inset) exhibited rectification during modulated firing in response to sinusoidal rotation. Spont, Spontaneous.

Sample behavioral and neuronal responses to rotational motion during two behavioral states: default state (left column) and simulated flight (right column). All data were recorded during y-axis (pitch) rotation (0.5 Hz, 20°/s). Representative EM (head-fixed), air-on (head-fixed), and NEM (head-free) neuronal responses are shown in the top, second, and third row panels, respectively. Stimulus angular velocity (S_PITCH), head-on-body velocity (H_PITCH), and tail-on-body velocity (T_PITCH) are shown in the bottom three panels and were recorded simultaneously with the NEM cell under head-free conditions. Neural waveforms are shown in gray, and corresponding IFRs are overlaid as black dots.

Frontal airflow triggers a change in a pigeon's behavioral state. A, Default state (air-off). B, Flight state (air-on). (Credit: Marcy Hartstein, MedPIC, Washington University School of Medicine, St. Louis, MO.) C, Recording electrode tracks for the 10-wire electrode array penetrating through the vestibular nuclei of four birds. Solid lines indicate the track of one array that had split into two clusters of electrodes during the penetration. Dashed lines indicate the approximate tracks from three other animals, based on histological verification. Cb, Cerebellum; Ld, dorsal lateral vestibular nucleus; Lv, ventral lateral vestibular nucleus; M, medial vestibular nucleus; S, superior vestibular nucleus.

Neuronal responses to head-fixed preferred cardinal axis rotation during two behavioral states. A, Mean (±SEM) IFR gain values for each neuronal category (air-on, red: n = 8; NEM, blue: n = 13; EM, green: n = 6) during default (solid symbols) and flight (open symbols) states, plotted as a function of stimulus frequency (15°/s peak) and peak velocity (0.5 Hz). B, Mean (±SEM) IFR phase values for each neuron, color coded by neuronal category. Neurons are ordered bottom to top by increasing spontaneous firing rate, with air-on neurons (red) at bottom (with arbitrary within-group ordering), then NEM (blue) and EM (green) neurons (using same ordering as shown in B). Phases were recorded during head-fixed rotational motion about that neuron's preferred axis (square = x-axis, circle = y-axis, triangle = z-axis) during default (solid symbols) and flight (open symbols) states, averaged across stimulus frequency and velocity. Note that phase values of −90° and 0° correspond to responses that are in phase with stimulus angular position and velocity, respectively. Spont, Spontaneous.

Comparison of gains and spike counts for NEM and EM neurons during default (air-off) and flight (air-on) states. All data were recorded during head-fixed rotational motion along a given neuron's preferred cardinal axis (x/y/z) of rotation. Each data point corresponds to a single neuron's response to a specific combination of stimulus velocity (5–20°/s) and frequency (0.25–1 Hz), presented in the presence and absence of airflow. Each symbol shape of a particular color corresponds to the available data for a single neuron, and symbol color indicates whether the neuron had a significantly higher value (red), lower value (blue), or no change in value (black) between behavioral states, based on the results of a Wilcoxon matched-pair test. A, Gain values (spk/s per °/s) from steady-state sinusoidal fits to the IFR. B, Mean + half-cycle spike counts.

Comparison of responses to rotational (tilt) and translational (apparent tilt) stimuli. A, B, Representative air-on neuron response to head-fixed 0.5 Hz tilt (A, pitch, 20°/s) and translation (B, fore–aft, 0.1G). Stimulus traces (bottom of each panel) show angular velocity (black) and linear acceleration (gray) components of each stimulus. Neural responses are shown for the same air-on neuron during default (Air Off) and flight (Air On) states. Neural waveforms are shown in gray, and the corresponding IFR values are overlaid in red. C, Comparison of rotational and translational gain values across neurons, expressed relative to apparent tilt velocity (see Materials and Methods). Data are plotted for all air-on (red, n = 8), EM (green, n = 1), and NEM (blue, n = 9) neurons for which data were available, and all appropriate data from a single neuron were included (responses to either one or two motion axes per unit). Circles, Pitch rotation/fore–aft translation; squares, roll rotation/lateral translation. Data points inside of the gray box (C) belong to a single NEM neuron identified as an outlier (see Results).