Posture, head stability, and orientation recovery during vestibular regeneration in pigeons

Abstract

Compensatory behavior such as oculomotor, gaze, and postural responses that occur during movement largely depend upon a functioning vestibular system. In the present study, the initial loss and subsequent recovery of postural and head stability in pigeons undergoing vestibular regeneration were examined. Adult pigeons were trained to manipulate a straight run chamber to peck an illuminated key for fluid reward. Six behavioral measures assessing performance, posture, and head stability were quantified. These included run latency, steps (walking), path negotiation (lane changes), gaze saccades, head bobs, and head shakes. Once normative values were obtained for four birds, complete lesion of all receptor cells and denervation of the epithelia in the vestibular endorgans were produced using a single intralabyrinthine application of streptomycin sulfate. Each bird was then tested at specific times during regeneration and the same behavioral measures examined. At 7 days post-streptomycin treatment (PST), all birds exhibited severe postural and head instability, with tremors, head shakes, staggering, and circling predominating. No normal trial runs, walking, gaze saccades, or head bobs were present. Many of these dysfunctions persisted through 3-4 weeks PST. Gradually, tremor and head shakes diminished and were replaced with an increasing number of normal head bobs during steps and gaze saccades. Beginning at 4 weeks PST, but largely inaccurate, was the observed initiation of directed steps, less staggering, and some successful path negotiation. As regeneration progressed, spatial orientation and navigation ability increased and, by 49 days PST, most trials were successful. By 70 days PST, all birds had recovered to pretreatment levels. Thus, it was observed that ataxia must subside, coincident with normalized head and postural stability prior to the recovery of spatial orientation and path navigation recovery. Parallels in recovery were drawn to hair cell regeneration and afferent responsiveness, as inferred from present results and those in other investigations.

Figure 1

Straight run behavioral chamber. A 1.75-m behavioral run was used to train the birds using operant conditioning to negotiate along a straight path, peck an illuminated key, and receive water reinforcement. A holding pen was located at one end of the chamber and separated from the path walkway by a Plexiglas divider. Run lanes were marked along the length of the chamber by grid lines. An illuminated pecking key was located at the other end of the chamber, with a fluid receptacle placed adjacent to the key. All trials were computer controlled.

Figure 2

Scanning electron micrographs of regenerating receptor cells in the semicircular canal crista and utricular macula. A–C. Regeneration in the anterior canal cristae. No stereocilia (receptor cells) are present in the epithelium at 4 days PST (A). Low density of receptors during early regeneration at 14 days PST, with most receptor cells located in the peripheral regions of the epithelium (B). At 63 days PST (C), receptor cell density has increased. All scale bars = 100 μm. D–F. Regeneration in the utricular maculae. Some early regenerating hair cells are present in the central and peripheral regions of the macula, with few hair cells present in the striola region at 14 days PST (D). By 42 days PST (E), the receptor cell density has increased, but the striola region still contains fewer cells than extrastriola regions. The density of receptor cells has increased for all regions to nearly 80% of normal at 84 days PST (F). Scale bars = 50 μm.

Figure 3

Circling and head shake behavior of streptomycin-treated birds. A. As illustrated in the cartoon drawings from left to right, early (5–7 days) PST birds exhibited a staggered or broken circling behavior when attempting to stand. The balance posture shifted frequently from leg to leg as the body turned. Head movements were frequent and chaotic. Many head thrusts were observed in the upward and backward direction, particularly during the turning behavior. B. As illustrated in the cartoon drawings from left to right, PST birds exhibited frequent, rapid side-to-side head shake movements that often contained an upwardly directed component.

Figure 4

Latency, number of steps, and number of lane changes as a function of recovery days following streptomycin treatment. The latency (top) was measured as the time between key illumination and key peck when the bird must negotiate the 1.5-m run. The number of steps (middle) was counted during the trial, when directed toward the goal key peck. The lane changes (bottom) were measured as the body crossed one of the three longitudinal lanes from the holding pen to the illuminated key in the run. The averaged responses for 10 trials on each testing day posttreatment are shown for each of four birds. Normal pretreatment values obtained for each bird are shown at the end.

Figure 5

Number of head gaze saccades, head bobs, and head shakes as a function of recovery days following streptomycin treatment. The number of head gaze saccades (top) was measured when they occurred as a normal saccadic gaze movement. Head bobs (center) are a natural behavioral movement that occurs in pigeons during walking (and other behaviors, but not when standing in one location). Head shakes were observed only in treated birds and could be either side to side or upward and backward movements. The averaged responses for 10 trials on each testing day posttreatment are shown for each of four birds. Normal pretreatment values obtained for each bird are shown at the end.