When a bat approaches a target, it continuously modifies its echolocation sounds and relies on incoming echo information to shape the characteristics of its subsequent sonar cries. In addition, acoustic information about the azimuth and elevation of a sonar target elicits orienting movements of the head and pinnae toward the sound source. This requires a common sensorimotor interface, where echo information is used to guide motor behaviors.Using single-unit neurophysiological methods and free-field auditory stimulation, we present data on biologically relevant specializations in the superior colliculus (SC) of the bat for orientation by sonar. In the bat's SC, two classes of spatially tuned neurons are distinguished by their sensitivity to echoes. One population shows facilitated, delay-tuned responses to pairs of sounds, simulating sonar emissions and echoes. Delay tuning, related to encoding target range, may play a role in guiding motor responses in echolocation, because the bat adjusts its emissions with changes in target distance. The delay-facilitated response depends on the direction of stimulation and on the temporal relationship between the simulated emission and echo in the sound pair, suggesting that this class of neurons represents the location of a target in three dimensions. A second population encodes the target in two dimensions, azimuth and elevation, and does not show a facilitated response to echoes delivered from any locus. Encoding of azimuth and elevation may be important for directing head aim, and this class may function in transforming auditory spatial information into signals used to guide acoustic orientation.
Key words: superior colliculus; echolocation; bats; acoustic orientation; spatial perception; sensorimotor integrationThe midbrain superior colliculus (SC; optic tectum) of vertebrates is thought to play a role in spatial perception and in the translation of multisensory signals into commands for the control of quick (saccadic) orienting responses. In individual species, the organization of the SC reflects the importance of a particular sensory modality to an animal's goal-directed behavioral responses. By analogy with the role of the SC in the saccadic eye-movement system of primates (Sparks, 1986), in gaze-control orientation behavior in cat and barn owl (Knudsen, 1982;Middlebrooks and Knudsen, 1984;Du Lac and Knudsen, 1990;Munoz et al., 1991), and in prey-catching behavior in pit viper and frog (Hartline et al., 1978;Grobstein, 1988), the SC of the echolocating bat may play a role in integrating sensory and motor signals that drive this animal's acoustic orientation by sonar.The bat guides its flight and forages in darkness by emitting ultrasonic vocal signals and listening to the echoes returning to its ears from objects in space (Griffin, 1958;Moss and Schnitzler, 1995). Binaural differences in arrival time, intensity, and spectrum of echoes encode the location of an object in azimuth and elevation (Lawrence and Simmons, 1982;Simmons et al., 1983;Pollak, 1988). The third dim...