Roderick A. Suthers - US grants

Flying bats use sonar (echolocation) to track and intercept moving prey. A particularly interesting problem is presented in the case of fish-eating bats because the prey can only be tracked by sonar when at the surface of the water; at other times it is "invisible" to sonar. This is a project in which the behavior of a fish-eating bat will be investigated as it tracks and intercepts a target that is under the control of the experimenter. The target's velocity, acceleration and path of movement will be varied, as will the amount of time it spends at the water surface. The experimenter will measure the flight path and head aim of the bat, where it dips its feet in attempting to capture prey that has disappeared beneath the surface, and its ability to resolve differences in velocity of targets moving across its path. The study will also address the role of learning in the bat's development of tracking behavior. The project is important for a number of reasons. The general issue of how animals use sonar for obtaining information and how they process that information to intercept moving and periodically disappearing targets is significant to understanding basic aspects of animal behavior, particularly of bats and marine mammals. It also offers the possibility of suggesting improvements in man-made sonar tracking devices.

This research focuses on basic problems in the sensorimotor control and development of complex vocal communication in songbirds. Songbirds provide an excellent model in which to study issues important both to students of animal communication and to those of human speech. Except for man, songbirds are the only animal in which learning plays an important role in the development of complex vocal signals. Songbirds were also the first animal model for central lateralization of vocal motor control analogous to cerebral dominance in human speech. Studies on the neuroethology of birdsong provide a way of experimentally evaluating a variety of concepts important to understanding human speech among which are included the possibility of special phonetic processing in the production and perception of vocal signals, the motor theory of speech perception and the function of central lateralization. These experiments utilize a new technique in which microbead thermistors are placed in each bronchus to record air movement associated with respiration and phonation. Respiratory pressure and the pattern of electrical activity of muscles comprising the vocal organ can also be measured. For the first time it is possible to directly monitor the sound produced and motor activity occurring on each side of the intact syrinx during song. Specific questions to be addressed include: What acoustic contribution does each side of the syrinx make to song? How is activity on the two sides coordinated? Can each side act independently of the other? Is song from a normal syrinx lateralized and if so does this originate centrally (analogous to cerebral dominance in human speech) or peripherally (thus being inappropriate as an animal analog of hemispheric dominance in speech)? What are the motor correlates responsible for specific vocal gestures or phonetic elements of song and how do they develop in the young bird? How are the sometimes conflicting, but interdependent, motor demands of respiratory ventilation integrated with song production? What differences with respect to the preceding questions are there between birds which retain a highly variable plastic song as adults verses those with a crystallized, more stereotyped song? The proposed experiments on adult birds thus address fundamental problems of broad interest. These include the peripheral control and execution of complex central motor patterns; the nature and function of lateralized motor control at both the central and peripheral levels; the motor correlates of specific vocal gestures including the possibility of a special phonetic processing for the production of vocal communication; the use of the same peripheral structure in different behaviors such as vocalization and respiration. Studies on young birds will in addition make a significant contribution toward a better understanding of ontogenetic aspects of sensorimotor development of vocalizations for communication; motor correlates of impressionable periods and the possible role of motor learning.

9411191 Suthers Vocal behaviors represent complex outputs of the nervous system with great behavioral and social significance. These behaviors, whether in primates or birds, demonstrate (a) a strong dependence on learning, and (b) complexities of neural control such as lateralization -- unequal control by the two sides of the nervous system. In the past, investigation of these phenomena in animal systems has relied very heavily on surgical disruption of the pathways controlling vocalization. In this proposal, a research team headed by Dr. R. Suthers will study the development of avian vocal behavior using new techniques that allow many fine details of vocal control to be analyzed without surgical disruption. These studies will enable Dr. Suther's team to uncover the normal controls on the development of coordination between the two sides of the song production organ, the syrinx. They will also allow new understanding of how the patterns of coordination are acquired by juveniles, and how complex aspects of tonality are produced. These studies will enhance our knowledge of the biology of communication systems, and are directly relevant to speech communication and linguistics. ***

DESCRIPTION (adapted from applicant's abstract) The research described in this proposal focuses upon the coordination of respiratory, vocal organ, and craniomandibular motor programs in producing the complex learned vocalizations of songbirds and parrots. Using neuroanatomical and physiological approaches, the research plan addresses five specific hypotheses: 1) that crystallized motor programs for both the respiratory and vocal organ muscle components of adult song can be modified by feedback from the periphery only if the vocalizations are learned; 2) that this sensory feedback arises from mechanoreceptive, proprioceptive, or thermal receptors in the vocal tract or respiratory system, and that auditory feedback is not necessary; 3) that compensatory motor responses after perturbations of respiratory pressure first appear during the plastic phase of song learning during the process of matching the output to a model syllable; 4) that respiratory and vocal organ motor neurons receive inputs from a common premotor source; 5) that, in achieving vocal complexity, parrots rely on increased plasticity in their respiratory and craniomandibular motor patterns to offset the limitations imposed by a simpler tracheal syrinx.

DESCRIPTION (provided by applicant): Songbirds are one of the few animal models for human speech in which it is possible to experimentally investigate basic physiological and acoustic challenges associated with producing complex, learned vocalizations. Parallels between the production of speech and birdsong have recently been strengthened by the discovery in birds of new song-related motor programs that modulate the dimensions of the supra glottal vocal tract, causing it to act as a variable resonance filter that tracks the fundamental frequency of sound generated in the vocal organ. The following research focuses on sensorimotor control of the oropharyngeal-esophageal cavity (OEC), which dominates the vocal tract filter. A long-term goal is to increase our understanding of how the nervous system controls complex behaviors. The first specific aim is to perform a detailed functional morphological analysis of the songbird head and neck, using micro dissection, MRI and CT scan. The data obtained will be combined with that from cineradiography of vocal tract movements during song. The resulting kinematic model will be elaborated by the addition of in vivo and in vitro measures of biophysical, physiological and biochemical factors determining the contractile performance of the relevant vocal tract muscles. The inclusion of these data in the model will make it possible to convert the kinematic model into a dynamic 3D biomechanical model of song-related vocal tract movements. The second specific aim investigates the role of sensory feedback in the OEC's ability to keep its resonance frequency tuned to the song's fundamental frequency, which is controlled by the syrinx. Cineradiography will be combined with manipulation of sensory feedback by deafening, pitch shifting vocal output or altering the fundamental frequency to determine the role of sensory feedback in controlling vocal tract filters so their resonance matches the fundamental frequency. The possible role of somatosensory feedback in tuning the vocal tract filter will also be investigated. The third specific aim will use neuroanatomical and neurophysiological techniques to map the premotor pathways of the cranial nerves in order to identify the neural pathways by which auditory information accesses the motoneurons to muscles of the upper vocal tract and to look for possible neural connections to the brain's song control nuclei, which controls the vocal organ. Songbirds provide a valuable model system in which to investigate some of the control mechanisms relevant to various speech pathologies that are important to public health.