Spatially Selective Auditory Responses in the Superior Colliculus of the Echolocating Bat

Abstract

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...

Biosonar navigation above water II: exploiting mirror images

“…Because of the large spatial receptive fields of delay-tuned neurons, they do not seem to be suited to process directional information of echoes in the AC of the mustached bat (Suga et al 1990). In the midbrain superior colliculus of E. fuscus, however, Valentine and Moss (1997) found that responses of delay-tuned neurons depended not only on the temporal delay between pulse and echo, but also on the direction of stimulation. They could show that the best delay of all delay-tuned neurons changed with the azimuthal position of sound presentation.…”

“…Delay-tuned neurons, sensitive to certain pulse-echo delays, have been found in the midbrain (Dear and Suga 1995;Portfors and Wenstrup 1999;Valentine and Moss 1997), thalamus (Olsen and Suga 1991;Wenstrup 1999), and AC (Dear et al 1993;Feng et al 1978;Hagemann et al 2010;Suga et al 1990;Sullivan 1982) of different bat species. Because of the large spatial receptive fields of delay-tuned neurons, they do not seem to be suited to process directional information of echoes in the AC of the mustached bat (Suga et al 1990).…”

Flying in silence: Echolocating bats cease vocalizing to avoid sonar jamming

“…Two populations of neurons have been identified in the superior colliculus of the big brown bat (E. fuscus), one that responds selectively to acoustic stimulation at a particular azimuth and elevation (2D neurons) and one that responds selectively to acoustic stimulation over restricted azimuth, elevation, and distance (3D neurons) (38). The population of 2D neurons responds to single frequency-modulated (FM) signals and would be well suited for passive localization of sound sources but not for precise distance measurements required for prey capture.…”

Visually guided gradation of prey capture movements in larval zebrafish

“…In a variety of species there are topographic representations of sensations that also register appropriately with tectal motor maps. These include electroreception in weakly electric fishes (Bastian, 1982), thermosensation in rattlesnakes (Hartline et al, 1978), echolocation in bats (Valentine and Moss, 1997), audition in barn owls (Knudsen, 1982) and somatosensation in cats (Stein et al, 1976). While less is known about other sensory inputs to the zebrafish tectum, given the conserved nature of tectal organization it is likely a similar coregistration of different sensory modalities exists.…”