A Role for the Superior Colliculus in the Control of Sonar Vocal Production in the Echolocating Bat, Eptesicus fuscus

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Date
2005-03-28
Authors
Sinha, Shiva
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Moss, Cynthia F
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Abstract
Microchiroptera have evolved a biological sonar system that enables aerial foraging in total darkness. These echolocating bat species emit sequences of ultrasonic vocalizations and use the returning echoes to create acoustic images of the environment. Bats orient their gaze in space by adjusting their sonar vocalizations, flight dynamics, and head aim in a coordinated manner when approaching targets. Insectivorous species of echolocating bats have been shown to actively modulate the features of sonar vocalizations with changing target distance. Therefore, variations in the time-frequency structure and temporal patterning of sonar calls produced by foraging bats reflect adaptive goal directed behaviors. The bat's heavy reliance on sound production and processing is reflected in neural specializations of auditory and motor structures. The experiments described in this dissertation probe the midbrain superior colliculus (SC), a vertebrate sensorimotor nucleus mediating orienting behaviors, and they specifically explore adaptations in the SC of the insectivorous bat, <i>Eptesicus fuscus</i>, for acoustic orienting. The anatomical experiments conducted demonstrate that the bat SC has projections to pre-vocal motor control regions in the brainstem: paralemniscal tegmentum area, cuneiform nucleus, and midbrain reticular formation. Further insights were gained by developing chronic neural recording techniques to study SC neuronal activity in actively echolocating bats. These are the first chronic recordings in unrestrained, freely behaving bats. The physiological experiments reveal two bouts of neural activity prior to each sonar vocalization, and suggest a relationship between the timing of pre-vocal activity and sonar call duration. Based on the anatomical findings and the functional pre-motor activity identified here, along with previous electrical and chemical microstimulation studies in the bat midbrain, a conceptual model is proposed for the SC of bats that suggests its role in orienting acoustic gaze along the range axis. This role of the bat SC is similar to that proposed for primate and feline SC in controlling the visual depth of focus via vergence eye movements. The parallel between the visuomotor and echolocation systems for orienting gaze to objects at different distances suggests that the computations performed by the SC serve common functions across modalities and effort organs.
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