State-dependent sensorimotor processing: gaze and posture stability during simulated flight in birds

Abstract

Vestibular responses play an important role in maintaining gaze and posture stability during rotational motion. Previous studies suggest that these responses are state dependent, their expression varying with the environmental and locomotor conditions of the animal. In this study, we simulated an ethologically relevant state in the laboratory to study state-dependent vestibular responses in birds. We used frontal airflow to simulate gliding flight and measured pigeons' eye, head, and tail responses to rotational motion in darkness, under both head-fixed and head-free conditions. We show that both eye and head response gains are significantly higher during flight, thus enhancing gaze and head-in-space stability. We also characterize state-specific tail responses to pitch and roll rotation that would help to maintain body-in-space orientation during flight. These results demonstrate that vestibular sensorimotor processing is not fixed but depends instead on the animal's behavioral state.

Hummingbirds control hovering flight by stabilizing visual motion

“…However, evidence from fictive flight preparations of other birds and insects indicates that they can change how senses are integrated and that different neuron populations are emphasized in different behaviors. An example of variable sensory integration comes from restrained pigeons that exhibit different head stabilization reflexes and tail responses to visual and vestibular perturbations during simulated flight than during resting conditions (16,17). At the level of sensory neurons, cells of the avian accessory optic system are divided into populations that differ in maximum sensitivity to either fast or slow motion (14,18,19).…”

Behavioral State Modulates the Activity of Brainstem Sensorimotor Neurons

“…Behavioral procedures used in these experiments have been described previously (McArthur and Dickman, 2011). In brief, the animal was secured to a restraint arm mounted to a six degrees-of-freedom hydraulic motion platform (Rexroth-Bosch) using a minimal restraint that left the animal's wings, tail, and legs free to move (see Fig.…”

“…To test the effect of behavioral state on neural responses to motion, we delivered rotational and translational motion in the absence of airflow and during an airflow-simulated gliding flight condition. Flight-state simulation has been described previously in detail (McArthur and Dickman, 2011). In brief, airflow was delivered to the animal's frontal surface using a blower hose fixed to the motion platform.…”

“…All analyses were performed using custom scripts in Matlab (Mathworks). Head and tail movement signals were converted to rotation vectors in Cartesian coordinates, as described previously (McArthur and Dickman, 2011). Action potentials were sorted off-line using commercial software implementation (Spike2, Cambridge Electronic Design) of semiautomated spike shape template matching, and any putative single units for which this procedure could not be reliably implemented (due to significant changes in spike shape across files or to a low signal-to-noise ratio) were discarded.…”

“…During flight, active gaze and posture stabilization are critical, as turbulence threatens perception and performance (Brown, 1963;Erichsen et al, 1989;Warrick et al, 2002). This is reflected in state-dependent vestibular gaze-and posture-stabilizing responses (McArthur and Dickman, 2011). Eye [vestibulo-ocular (VOR)] and head [vestibulocollic (VCR)] responses to rotation had significantly higher gains during simulated flight.…”