PERSPECTIVE What the bat’s voice tells the bat’s brain Nachum Ulanovsky*† and Cynthia F. Moss†‡ *Department of Neurobiology, Weizmann Institute of Science, Rehovot 76100, Israel; and ‡Department of Psychology and Institute for Systems Research, Program in Neuroscience and Cognitive Science, University of Maryland, College Park, MD 20742 Edited by Jeremy Nathans, Johns Hopkins University School of Medicine, Baltimore, MD, and approved May 7, 2008 (received for review May 15, 2007) For over half a century, the echolocating bat has served as a valuable model in neuroscience to elucidate mechanisms of auditory processing and adaptive behavior in biological sonar. Our article emphasizes the importance of the bat’s vocal-motor system to spa- tial orientation by sonar, and we present this view in the context of three problems that the echolocating bat must solve: (i) audi- tory scene analysis, (ii) sensorimotor transformations, and (iii) spatial memory and navigation. We summarize our research findings from behavioral studies of echolocating bats engaged in natural tasks and from neurophysiological studies of the bat superior col- liculus and hippocampus, brain structures implicated in sensorimotor integration, orientation, and spatial memory. Our perspective is that studies of neural activity in freely vocalizing bats engaged in natural behaviors will prove essential to advancing a deeper un- derstanding of the mechanisms underlying perception and memory in mammals. active sensing ͉ behavioral neurobiology ͉ echolocation ͉ spatial cognition ͉ navigation n their seminal 1959 paper, ‘‘What plete understanding of the neurobiology positions of targets from differences in the frog’s eye tells the frog’s brain’’ of spatial orientation by echolocation. the perceived arrival time, intensity, (1), Lettvin et al. articulated a key We will start with a brief overview of and spectrum of echoes at the two ears point in neuroscience: Neurobio- classic studies of bat echolocation and (19), relying on the same acoustic cues I as any ‘‘standard mammalian auditory logical experiments should consider the then focus on three topics that, until natural context in which biologically rel- recently, have received comparatively system’’ (19, 20). The bat estimates tar- evant sensory information is acquired little attention in the study of echolocat- get range from the time delay between and behavior is executed. This view, ing bats: (i) auditory scene analysis, (ii) the outgoing vocalization and returning which later became a guiding principle sensorimotor transformations, and (iii) echo (21); some bat species show ex- in the field of neuroethology (2), implies spatial memory and navigation. We ar- traordinary spatial discrimination along that neural activity may change with the gue that echolocating bats show remark- the range axis, with thresholds for animal’s behavioral state. This implica- able performance and are among the range changes Ͻ0.1 mm (22, 23). Fur- tion has been supported, for example, by ‘‘champions’’ of mammals in these three thermore, the bat’s sonar system is findings from the bird song system, domains; furthermore, we provide evi- used for assessing the detailed proper- where dramatic differences exist be- dence that the bat’s active control over ties of the target: the bat perceives the tween auditory responses to acoustic its vocalizations plays a key role in its size of an object from the intensity of stimuli in anesthetized and awake ani- perception, action, and spatial memory. echoes (24), the target velocity from mals (3). Similarly, large effects of the the Doppler shift of the echoes (25), animal’s behavioral state are observed Bat Echolocation: From Behavior to Neuro- and the object’s shape from the spec- in the rodent barrel cortex, where neu- biology. Echolocating bats are small fly- trum of the echoes (26). In fact, bats ral activity in response to a whisker de- ing mammals (weighing typically Ͻ35 g) are able to use their sonar for high- flection depends strongly on whether that emit brief calls through either the level perceptual tasks such as object the animal is passive or is actively mov- mouth or the nostrils and use the re- recognition and classification (26–29) ing its whiskers (4). turning echoes to orient in the environ- and even for texture discrimination, Further, numerous studies (e.g., refs ment and forage for food at night or e.g., the roughness of surfaces (30, 31). 5–11) demonstrate that a comparative dusk (13–16). There are Ͼ800 species of Thus, echolocation is an exquisite sen- approach to neuroscience yields insights echolocating bats that occupy a broad sory system that can provide the bat that cannot be obtained by study of a range of habitats, and adaptations to with very detailed information about single species. In this article, we con- habitat and food sources are reflected in the environment. sider the behavior and neurobiology of their sonar call designs (15). The diver- The structure of an individual echolo- a mammal long studied from a compar- sity of bat behavior presents a rich op- cation call, or ‘‘pulse,’’ follows one ative standpoint, the echolocating portunity to understand the adaptive of three basic designs. (i) Frequency- bat (12–16), and here we stress the evolution of bats and sonar call design modulated (FM) calls, with durations of additional importance of performing (for comprehensive reviews, we direct 0.5–20 ms, often containing harmonics experiments in freely behaving animals. the reader to refs. 12 and 16). For this (Fig. 1A Left). Bats that use these calls Researchers of bat echolocation have Perspective, we draw from studies of are known as ‘‘FM bats,’’ and they con- long been inspired by observations of several species and distinguish between species-specific natural behaviors, but specializations and general mechanisms Author contributions: N.U. and C.F.M. wrote the paper. we note that past experimental studies to the extent that data are available. of the bat nervous system have rarely Most bat species use ultrasonic echo- The authors declare no conflict of interest. engaged the echolocating bat in these location calls, but a few species emit This article is a PNAS Direct Submission. natural behaviors. However, recent re- sonar calls with components that are †To whom correspondence may be addressed. E-mail: [email protected] or [email protected]. search that has explicitly studied neural audible to humans (17, 18). Bats com- edu. activity in freely behaving bats has un- pute the 3D location of objects from This article contains supporting information online at covered some surprising discoveries, as acoustic information carried by echoes www.pnas.org/cgi/content/full/0703550105/DCSupple- detailed below, and we believe future of their sonar vocalizations. The bat mental. work along these lines is key to a com- computes the horizontal and vertical © 2008 by The National Academy of Sciences of the USA www.pnas.org͞cgi͞doi͞10.1073͞pnas.0703550105 PNAS ͉ June 24, 2008 ͉ vol. 105 ͉ no. 25 ͉ 8491–8498 Downloaded by guest on September 28, 2021 produced also increases, allowing the animal to more accurately and rapidly sample the position and features of a so- nar target (32, 41). Similar adaptive changes in echolocation calls occur also in CF-FM and click-producing bats (15, 34) and have been used by researchers to delineate three ‘‘phases’’ of insect pursuit: the ‘‘search mode,’’ ‘‘approach ϫ Fig. 1. Biosonar behavior of echolocating bats. (A) Spectrogram representation (frequency time) of mode,’’ and ‘‘terminal phase’’ (attack echolocation calls of three bat species: big brown bat (E. fuscus), which produces FM echolocation calls; lesser horseshoe bat (Rhinolophus hipposideros), which produces CF-FM calls; and Egyptian fruit bat mode) (15, 41). Notably, during search (Rousettus aegyptiacus), which uses clicks for echolocation. Red color indicates maximal intensity. Arrows mode, the silent intervals between echo- point to the dominant harmonic: first harmonic in Eptesicus and second harmonic in Rhinolophus. The last location calls in FM bats can be quite two calls were recorded in Israel, courtesy of B. Fenton (University of Western Ontario, London, ON, long, often lasting several hundred milli- Canada) and A. Tsoar (Hebrew University of Jerusalem, Jerusalem). (B) Spectrogram of a sequence of FM seconds (17, 42) (e.g., Fig. 1B); thus, calls produced by a European free-tailed bat as it chased an insect. Gray bars denote the three echolocation the FM bat’s calls and echoes are similar 3 3 phases of insect-pursuit: search approach terminal phase (attack) (recorded in Israel by N.U. and B. to the discrete light flashes of a strobo- Fenton). scope. Despite the bat’s stroboscopic- like ensonification of the environment, stitute the majority of echolocating bat rized also by their foraging habitat, such its agile and smooth flight suggests the species. FM calls can be further subdi- as foraging in open space (far from bat may experience a stable and contin- vided based on finer acoustic properties echo-returning objects) or near edges of uous perceptual world, constructed from of their calls and on the signal’s adapta- forests or hunting inside vegetation (15). the discontinuous arrival of sonar echoes. tions to natural habitats (12). (ii) Con- In fact, the signal structure of each bat From an experimental standpoint, the stant-frequency (CF) calls are produced species is often suited remarkably well stroboscopic nature of echolocation pre- by a number of microchiropteran bat to the bat’s foraging habitat. Moreover, sents the opportunity for researchers to species in the Old World (Rhinolophid as discussed in detail below, the bat’s noninvasively record the timing of sen- and Hipposiderid bats) and the New signals may change rapidly and adap- sory inputs in freely moving animals, a World (Pteronotus parnellii). CF calls tively according to the task at hand, in powerful tool in neuroscience research, can last several tens of milliseconds, and a manner that can often be well under- as elaborated below.