Somatosensory feedback modulates the respiratory motor program of crystallized birdsong.

Abstract

Birdsong, like human speech, involves rapid, repetitive, or episodic motor patterns requiring precise coordination between respiratory, vocal organ, and vocal tract muscles. The song units or syllables of most adult songbirds exhibit a high degree of acoustic stereotypy that persists for days or months after the elimination of auditory feedback by deafening. Adult song is assumed to depend on central motor programs operating independently from immediate sensory feedback. Nothing is known, however, about the possible role of mechanoreceptive or other somatosensory feedback in the motor control of birdsong. Even in the case of human speech, the question of "how and when sensory information is used in normal speaking conditions...remains unanswered" and controversial [Smith, A. (1992) Crit. Rev. Oral Biol. Med. 3, 233-267]. We report here evidence for somatosensory modulation of ongoing song motor patterns. These patterns include the respiratory muscles that, in both birdsong and speech, provide the power for vocalization. Perturbing respiratory pressure by a brief, irregularly timed injection of air into the cranial thoracic air sac during song elicited a compensatory reduction in the electrical activity of the abdominal expiratory muscles, both in hearing and deafened adult northern cardinals (Cardinalis cardinalis). This muscle response was absent or reduced during quiet respiration, suggesting it is specifically linked to phonation. Our findings indicate that somatosensory feedback to expiratory muscles elicits compensatory adjustments that help stabilize, in real time, the subsyringeal pressure against fluctuations caused by changes in posture or physical activity.