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.

Regeneration of Vestibular Otolith Afferents after Ototoxic Damage

“…Previously, we used identical lesion methods to examine hair cell repopulation and recovery of posture, head stability, and spatial orientation during regeneration Dickman and Lim, 2004). Several interesting parallels between our current morphological findings and vestibular-dependent behavioral recovery are worth mention.…”

“…Because only bouton afferents had regenerated at this point, these fibers must convey the required information to central circuits for the establishment of vestibulo-spinal stabilization of posture. However, some staggering and head tremor remained throughout stage 1 regeneration (Dickman and Lim, 2004). In fact, the most dramatic recoveries in both morphology and behavior were observed during stage 2 regeneration.…”

“…It is now firmly established that cochlear and vestibular sensory hair cells spontaneously regenerate after damage in fish, amphibians, and birds (Corwin and Cotanche, 1988;Rubel, 1992, 1993;Baird et al, 1993), and these regenerated hair cells are contacted by new afferent and efferent terminals (Ryals and Westbrook, 1994;Masetto and Correia, 1997b;Hennig and Cotanche, 1998). In addition, functional recovery of vestibular hair cells (Masetto and Correia, 1997a), afferent sensitivity to motion (Li and Correia, 1998;Boyle et al, 2002), and vestibular behavioral responses (Jones and Nelson, 1992;Carey et al, 1996;Goode et al, 1999;Dickman and Lim, 2004) all correlate with regenerative development in birds. However, little is known about how reinnervation progresses and whether regenerated afferents ultimately develop normal termination fields.…”

Hair cell regeneration: An exciting phenomenon . . . But will restoring hearing and balance be possible?

“…These reflexes, however, reappear as the hair cells regenerate [99][100][101][102]104]. More recently, Dickman and Lim trained adult pigeons to run along a long chamber and peck an illuminated key to receive a fluid reward [105]. Multiple behavioral measures for assessment of performance, posture, and head stability were quantified.…”

Recovery of Gaze Stability During Vestibular Regeneration

“…Thus the functional return observed was likely due to a synthesis of factors other than regeneration alone, such as residual hair cell function and nonlethal repair (Baird et al 2000;Matsui et al 2003). Recently we examined head stability, posture, and orientation recovery during regeneration in pigeons trained to negotiate a maze (Dickman and Lim 2004). We found that complete vestibular loss produced profound head instability and postural ataxia that slowly recovered according to a temporal sequence of events, including increased head stability, head-tremor reduction, return of postural stability, and finally recovery of orientation and navigational abilities (Dickman and Lim 2004).…”