Most bats and marine mammals orient themselves by emitting orientation sounds that are adapted for the purpose of locating objects at a distance by hearing their echoes (Griffin, 1958; Vincent, 1967; Airapet'yants andKonstantinov, 1970). They maintain normal orientation when vision is impossible, but become disoriented if deprived of hearing or if prevented from emitting orientation sounds. As far as we know echolocation is a sort of "solipsistic communication" between an animal and its environment. While the source of echoes may be the body of another animal, only passive physical reradiation of sound waves is involved rather than active reply by the second animal. Hence, echolocation does not properly fall within any reasonable definition of communication behavior, andits discussion in the present volume is justified only by its indirect relevance to the physiological and behavioral phenomena that may be important both in echolocation and in communication.
The echolocation of animals escaped notice until electronic technology permitted translation of the orientation sounds of batsfrom the ultrasonic range (20 to 150 kHz) into the frequency range of human hearing (Griffin and Galambos, 1941). The discovery of echolocation in whales and porpoises required conversion of underwater sounds into sounds conducted through air (Schevill and Lawrence, 1949, 1956; Kellogg et al., 1953; Kellogg, 1961; Norris, 1966;Airapet'yants and Konstantinov, 1970). While bats of the suborder Microchiroptera and marinemammals of the order Cetacea are the two groupsin which echolocation is well developed and well studied, there are isolated cases in cave-dwelling birds (Griffin, 1958; Novick, 1959; Medway, 1967; Griffin and Suthers, 1970), and it occurs in a rudimentary form in terrestrial shrews(Gould et al., 1964; Buchler, 1972) and rodents(Rosenzweig and Riley, 1955). Even human beingsare capable of a limited form of echolocation, although it is not known to be important exceptto the blind. For blind men, however, it is of the utmost importance (Supa, Cotzin, and Dallenbach, 1944; Griffin, 1958; Rice, 1967); I shall return below to further discussion of human echolocation.
Reliance on echolocation for rapid mobility under difficult conditions places severe demands not only on the auditory receptors but also, more importantly, on the analyzing capabilities of the animal's brain. Many bats fly in totally dark caves where irregular rocky obstacles are numerous and unpredictable. They also fly with equal skill in forested areas, avoiding branches, leaves, twigs, vines, and other small objects of considerable complexity. Some cetaceans swim in dark or highly turbid waters where vision is of little if any use. Often there are rocks or other underwater obstructions to be avoided, and some of the smaller porpoises live in muddy rivers and lakes where they must swim close to submerged vegetation, fallen trees, and roots. Two examples are especially impressive in the case of bats: landing on some suitable object and drinking water on the wing. The first maneuver involves flying close to the landing place, slowing, then rapidly turning the body upside down, and finally reaching for a toehold with the hind claws. Errors of a few millimeters produce either an unpleasantly hard collision or a fall and the need to repeat the whole procedure. Bats commonly fly low over the surface of water and dip the lower jaw or tongue just sufficiently to drink. An error of a few millimeters would result in either failure to reach the water or in a splashing submersion. Smooth floors often elicit this type of drinking behavior in captive bats, indicating that the specular reflection of orientation sounds from a horizontal surface is interpreted as a sign of water available for drinking.
The echolocation of stationary obstacles for many years appeared so incredible that no one even suggested that the same mechanism might also be used to locate small moving targets. Nevertheless convincing evidence hasshown that at least under some conditions both bats and porpoises pursue insects and fish, respectively, largely by echolocation (Griffin, 1953, 1958; Griffin et al., 1960; Norris et al., 1961). Despite the sensitivity and acuity of echolocation, some insects are located by passivehearing of their flight sounds or sounds resulting from their movements on the ground or in vegetation (Kolb, 1961; Airapet'yants and Konstantinov, 1970). The accuracy and precision of echolocation implies that the auditory nervous system responds selectively to faint echoes from significant objects, despite a variety of other sounds competing for the animal's attention. Animals thus endowed might find the analytical requirements of an advanced communication system already at their disposal. While scarcely any solid evidence is available, it may be of interest to discuss the speculative possibility that both echolocation and communication share certain physiological and behavioral mechanisms.
Properties of Orientation Sounds
In all known cases the orientation sounds used for echolocation are quite brief—each one lasting only a small fraction of a second, in bats and cetaceans only one or a few milliseconds with the exceptions discussed below. It is convenient to refer to these sounds as pulses, since those of bats are not clicks with either simple or chaotic wave forms but orderly trains ofabout ten to several hundred sound waves. The ultrasonic orientation sounds of bats also have relatively faint audible components that can beheard under favorable conditions once one knows what to listen for (Galambos and Griffin, 1942; Dijkgraaf, 1943). Bats orient themselves in air with acoustic probes traveling at approximately 34 cm/msec, and porpoises use more rapidly traveling sound waves under water with velocities of about 155 cm/msec. Under some conditions echoes may return during the latter part of an emitted orientation sound, but many echolocating animals avoid this by adjusting the duration of emitted sounds in relation to the distance between themselves and the objects that are of immediate concern. This avoidance of overlap is almost universal in the best-studied bats of the family Vespertilionidae (Webster, 1966; Cahlander et al., 1964).
Two distantly related groups of bats, the family Rhinolophidae of the Old World and Pteronotus parnellii of the neotropical family Mormoopidae, have specialized orientation sounds containing relatively long constant-frequency portions in addition to frequency sweeps (Möhres, 1953; Griffin and Novick, 1955; Griffin, 1962). These constant frequencies are used to detect Doppler shifts due to relative motion of the bat and the target returningechoes (Schnitzler, 1968, 1970, 1973; Simmons, 1974; Simmons, Howell, and Suga, 1975). On the other hand the best-studied bats (the families Vespertilionidae, Molossidae, Natalidae, and Noctilionidae, which are all highly specialized for echolocation) employ a rapid downward sweep. This is also a very widespread, if not universal, component in the families Emballonuridae, Phyllostomatidae, and Desmodontidae (Simmons, Howell, and Suga, 1975).
The problems of accurate measurement of frequency patterns are complicated by the tendency of bats primarily concerned withlarge and motionless objects to use orientationsounds of relatively low intensity. Those species that are active predators, pursuing small moving insects or fish, use very considerably louder orientation sounds (Griffin and Novick, 1955; Griffin, 1962; Pye, 1967; Suthers, 1955). The advantage to the bat of the rapid frequency sweep is not entirely certain, but perhaps the most plausible explanation is that it enables a wide range of wavelengths to be reflected from small targets. With small objects approximatingthe wavelengths of the orientation sounds, the relative intensities of the various frequenciesmay well provide qualitative information about the nature of the reflecting object. This echo spectrum may be used to achieve discrimination between closely similar objects (Griffin et al., 1965; Griffin, 1967; Bradbury, 1970; Simmons,1973). Another possible advantage is discussedin the next section.
Cetaceans, when concerned with difficult problems of orientation with respect to objects at short distances, also use very short-duration orientation sounds (Kellogg, 1961; Vincent, 1967; Norris et al., 1961; Norris, 1974). Individually, these are clicks of such short duration that their frequency spectrum is extremely broad. In the best-known cases both bats and porpoises shorten the duration of theirorientation sounds to less than one millisecond when they are making close approaches to important objects such as morsels of food or, in the case of bats, landing places.
Orientation sounds also vary widely in other acoustic properties. The frequencies are generally high, or at least include wavelengths of a few millimeters or centimeters.This is presumably related to the greater magnitude of echoes from objects that are somewhat larger than the wavelengths of the sounds impinging on them. Another possible advantage is the rapid attenuation of high-frequency sound in air (Griffin, 1971; Evans and Bass, 1972). While restricting the range at which objects can be echolocated, this also limits the reverberations and "clutter" that would otherwise tend to interfere with the important echoes from objects at a close range.
Another important property ofthe orientation sounds used by both bats and cetaceans is the universal tendency for the rate at which they are repeated to increase sharply whenever the animal is faced with a difficult orientation problem—whether it be a bat landing on a crevice in the ceiling of a cave, a porpoise picking up a piece of fish floating close infront of the cement wall of a large tank, or either animal pursuing elusive moving prey. The pulse repetition rates rise from a very few isolated orientation sounds per second to brief bursts, in which they are repeated at rates up to 250 per second in bats and even higher in porpoises. When translated into audible clicks, this crescendo of orientation pulses becomes a buzz.
While the orientation sounds of most bats are above the frequency range of human hearing several species use the octave from 10 to 20 kHz and are audible even under natural conditions. In the tropics some insectivorous bats use frequencies that sweep as low as 4 or 5 kHz (Griffin, 1971). In dark caves two species of cave-dwelling birds (Steatornis and Collocalia) and the genus Rousettus among the Megachiroptera (Old World fruit bats with large eyes, which rely on vision under most circumstances) echolocate quite successfully with clearly audible clicks. These clickscontain frequencies from roughly 3 to 8 kHz (Griffin, 1958), but despite these relatively low frequencies Rousettus and some species of Collocalia can detect cylindrical obstacles with diameters as small as 1 to 3 mm (Griffin, Novick, and Kornfield, 1958; Griffin and Suthers, 1970; Fenton, 1975). Thus echolocation of small objects is biologically possible with frequencies audible to human ears.
Problem of Interference
In many situations the echo of an orientation sound, when it returns to the ears of an echolocating animal, will consist of sound waves reflected from different parts of a large objectlying at sufficiently different distances so that interference between sound waves occurs. Except for very small objects or perfectly smooth surfaces such as calm water, such interference must occur even in the echoes of orientation sounds having very short durations. When single frequencies are employed, such destructive and constructive interference produces echoes that vary greatly in amplitude with small changes in the animal's relative distance from various parts of an echoing surface. These interference phenomena are similar in some ways to the familiar phenomenon of standing waves when a continuous tone is measured or listened to in a closed room. The principal difference is that interference patterns of echoes from different parts of a large object change rapidly with time. It seems likely that the variability of such echoes from short tones of constant frequency would make echolocation difficult, and this may help explain why so many echolocating animals use FM pulses as orientation sounds. This problem could theoretically be avoided by using other types of signals, such as bursts of random noise, but no animal highly specialized for echolocation has been found to use noise bursts. Some evidence suggests, however, that small terrestrial mammals use sounds of rather indefinite frequency in a marginal form of echolocation (Buchler, 1972). But these sounds are of such low intensitythat it has been difficult to measure their acoustic properties accurately enough to throw much light on this question.
It is misleading to think of echolocation as merely the hearing of isolated echoes. In actual practice under natural conditions, echolocating animals must discriminate certain faint echoes from many other sounds of similar properties occurring at nearly the same time. These include sounds of outside origin andechoes of objects other than the target of immediate concern. Consider, for example, the problems faced by an insectivorous bat relying for its food supply entirely upon echoes from insects measuring only a fraction of the wavelengths of its orientation sounds. These are encountered at unpredictable times and places but, very often, close to other small objects such as leaves or twigs. Any one orientation pulse returns to the bat's ears echoes from a large number ofobjects at different distances and direction. Only one part of this complex of echoes is relevant. All other information must be ignored or used merely for the avoidance of stationary obstacles. Since most of the unimportant targets are larger than the critically important morsel of food, the interfering echoes will very often be more intense than those important to the animal. Yet, despite these difficulties, small insectivorous bats such as Myotis lucifugus capture insects measuring only a few millimeters in wingspread at rates of several per minuteduring their routine feeding behavior—often under conditions where there is extensive interference from echoes of other larger objects (Gould, 1955, 1959; Griffin et al., 1960; Webster, 1963).
The neurophysiological mechanisms employed by bats in such discriminative auditory orientation have been studied rather extensively in recent years by Grinnell (1963), Grinnell and Grinnell (1965), Suga (1964, 1965, 1973), Suga et al. (1975), Harrison (1965), and Henson (1965, 1970). There are some specializations for auditory sensitivity in the ultrasonicfrequency range, apparently shared by other small mammals (Ralls, 1967; Sales and Pye, 1974). Auditory areas of bat brains are enlarged relative to those of other mammals, but this hypertrophy is present only posterior to the diencephalon. The medullary, midbrain, and, in particular, the collicular auditory areas are relatively enormous, whereas the auditory thalamus and cortex are only slightly enlarged in comparison to those of shrews and rodents.
Grinnell (1963) was the first to study the neurophysiological basis of discrimination against interference, and some of hisexperiments were directed toward explaining thdemonstrated resistance of bats to jamming by broad-band interfering noise (Griffin et al., 1963). Evoked potentials from the posterior colliculus in response to short tone bursts similarto orientation sounds could be masked by simultaneous noise from a second high-frequency loudspeaker. In one typical experiment (Grinnell, 1963), the masking noise raised the threshold fora detectable evoked potential by 43 dB, provided the noise arrived from almost the same direction as the signal. When the noise-generating loudspeaker was moved 60°, however, the thresholdfell by about 25 dB. Most of this effect was due to the directional differences in auditory sensitivity, but there was also evidence of neurophysiological interaction within the brain between the nerve impulses from the two ears, whichserved under some conditions to improve furtherthe animal's ability to detect faint signals despite a masking noise. Implications of some recent neurophysiological experiments by Suga are discussed in the next section.
When flying bats were pressedto the limits of their abilities to detect finewires in a severe jamming noise, they performedbetter than could be accounted for by signal detection theory if only a single communication channel was assumed to be operating between the wire obstacle and the bat's brain. The flight maneuvers of these bats showed a strong tendencyto approach wires obliquely when the jamming noise became truly difficult, and this doubtless served to separate the faint echoes from the jamming noise by taking advantage of their differing angles of incidence (Griffin, McCue, and Grinnell, 1963). Neurophysiologically, the addition of information arriving via the second ear expanded the discriminative capabilities of the bat's information-processing system sufficiently to bring its performance well within the theoretical boundary conditions of signal-detection theory.
Simmons has recently developed a powerful new method for studying the capabilities of echolocation in bats. This method employs a modification of the Lashley jumping stand into a "Simmons flying stand," in which a batis trained to fly from a starting platform to one of two other platforms. Blinded bats reinforced with food learned to choose the correct platform on the basis of echolocation. With this method Simmons (1973) has been able to demonstrate an ability to discriminate targets on the basis of their size, shape, angular position, anddistance. These experiments and many of their ramifications are well reviewed by Simmons, Howell, and Suga (1975). Distance discrimination proved most illuminating. Differential distance thresholds prove to be only a few centimeters, considerably less than the lengths of the orientation sounds as they travel through the air. These results could be accounted for only by assuming that the auditory system of the bat made use of virtually all the information physically present in the echoes. Thus these experiments confirmed and greatly improved upon those of Griffin, McCue, and Grinnell with flying bats.
Simmons and his colleagues have gone on to experiment with the effects of interfering noise on distance discrimination, andthe results, while too complex to discuss here, clearly support the conclusion that the auditory brains of bats approach very closely the theoretical limits set by signal-detection theory for an "ideal detector" (Simmons, Howell, and Suga, 1975). Another important conclusion that has resulted from Simmons's experiments has been the rigorous demonstration that bats determine distance by differences in the time required for an echo to return. This was established by substituting electronic delay lines for physical separation between the bat and its target. The two landing platforms were in fact equidistant, but when the echo from one was delayed by a small fraction of a millisecond the bat treated itas a more distant target.
Human Echolocation and Its Possible Relationship to Speech
This brief review of what is known about the capabilities for discriminative echolocation achieved by less than one gram of bat brain suggests that echolocating animals possess powers of auditory discrimination and information processing that are more than adequate for complex types of communication. But the extent to whichbats actually utilize these capabilities for communication remains for future investigation todiscover. Bats and cetaceans certainly do communicate by sound, as discussed elsewhere in this book. The communicative sounds of bats are mostly at frequencies lower than those of their orientation sounds (Gould, 1971; Bradbury, 1972); presumably the better carrying power of lower frequencies makes them superior for communication.
The search for other applications that might justify including a chapter on echolocation in this book has called to minda puzzling aspect of human echolocation as it is practiced by the blind. A basic challenge is posed by the simple question: Why is it that blind men cannot echolocate as well as bats or dolphins? As more and more has been learned about the echolocating abilities of 7-gram bats, with brains weighing approximately 1 gram, the disparity has increased —to the embarrassing disadvantage of our 1,500-gram brains. Simple arithmetic of wavelengths suggests that a factor of five, or at the most ten, should separate the minimum sizes of objects discriminated because man is limited to lower frequencies of sound. But where bats catch fruit flies at rates of several per minute, blind men cannot safely drive automobiles, let alone fly airplanes to catch birds—which performance, of course, would be directly analogous.
This disparity of skill at echolocation can scarcely be due entirely to the hesitant recognition that "facial vision" or "obstacle sense" in the blind is largely, if not entirely, echolocation. Many direct investigations of human echolocation have been carried out, along with applied research attempting to improve the usefulness of echolocation to the blind (Zahl, 1950; Clark, 1963). Human echolocationhas been studied surprisingly little in the thirty years since its existence and importance were conclusively demonstrated by Supa, Cotzin, and Dallenbach (1944), despite the obvious human importance of any improvements that might be achieved by understanding it better (Griffin, 1958). Rice, Schuster- man, and Feinstein (1965) measured threshold diameters of disks that could be detected by blind human subjects at distances of 61 to 275 cm. Optimal conditions were provided; all targets were oriented so as to return maximum echoes, the room was quiet, and no other echo- generating surfaces were close to the test targets. The thresholds approximated a subtended angle of 4.6°, and size and distance discrimination were also quite good.
In later experiments, Rice (1971) found that especially proficient individual subjects could do considerably better. One blind man could detect 4 and 5 cm disks almost perfectly at 92 cm (subtended angle about 2.3°), and a young woman who had been blind from infancy could detect long cylindrical rods down to a diameter of about 6 mm (Rice, pers. comm.). In these experiments by Rice and his colleagues the subjects were allowed to make any sort of vocal sound they wished. All did make orientation sounds of some sort, but some used clicks, others longer-duration wide-band hisses, and still others repeated various words or syllables. Their performance did not differ significantly, indicating that the human auditory system can detect echoes almost equally well regardless of frequency pattern within the audible frequency range.
Except for Rice's careful, well-controlled experiments under optimal conditions, human echolocation has not been studied with appreciable success. Instead much effort has gone into the development and testing of guidance devices, small instruments for echolocation by means of high-frequency sound or light beams, which deliver signals to the user that are designed to warn him of approaching obstacles. In most devices these signals are delivered through earphones, and one of the best is binaural (Kay, 1966). In some instruments tactile presentation of the warning signals has been employed. Most of these devices work quite well in the laboratory, and in field tests under reasonably normal conditions they seem useful for blind persons. But I have been waiting in vain for many years to hear of a device so successful that the blind subjects were reluctant to give it back to the experimenter. A truly effective guidance device would so greatly improve a blind person's life that I can easily imagine him hiding it away to prevent its being taken from him. This would surely lead to urgent pleas for mass production, black markets, and so forth. Alas, nothing of the kind has been reported (Dufton, 1966).
One reason often suggested for the ineffectiveness of these devices is that the audible warning signals interfere with the normal use of ambient sounds that carry information about the environment. In theory the tactile presentation should avoid this difficulty, but here too the criteria of true success suggested above have yet to be reported. In this connection it should be borne in mind that echoes of sounds emitted by a blind person are only one class of ambient sounds that are doubtless useful for spatial orientation; sounds originating from other sources and their echoes from various objects all contribute to the audible sound fields through which we move. In one recent study newly blinded people learned to move about on city sidewalks and to cross streets more rapidly than usual when trained with tape recordings of the ambient sounds they were likely to hear (De l'Aune, Scheel, Needham, and Kevorkian, 1974). We almost certainly fail to pay attention to a variety of auditory information available to us because vision tells us what we need to know about most of our immediate surroundings.
It may well be that attempts to transfer responsibility for echolocation to the artificial guidance devices have deflected efforts away from the more tedious, but perhaps ultimately more rewarding, attempt to learn how a man could operate like a bat or a dolphin within the human range of hearing and with airborne sounds. But whatever deficiencies there may have been in research efforts on this front, thousands of intelligent and able-bodied blind people have been experimentingempirically along these lines for centuries. If it were easy some would have learned how to employ echolocation as skillfully as echolocating animals do. Yet efforts to improve acoustic orientation by the blind should certainly continue and should include both ambient sounds and echolocation.
Is there something qualitatively different about bat brains that allows discrimination of echoes imperceptible to much larger and more complex human brains? Extensive investigations by Grinnell and Suga (up to about 1970) failed to reveal any neurophysiological differences of a truly basic nature, although in bats and cetaceans a larger proportion of the auditory brain appears to be devoted to cells that recover sensitivity very rapidly after the end of a relatively loud sound. Bullock, Ridgway, and Suga (1971) and Bullock and Ridgway (1972) demonstrated this type of difference in marine mammals by comparing porpoises with sea lions, which have only a very limited capacity for echolocation, if any. In another type of neurophysiological investigation Henson (1965) has demonstrated that Hartridge (1945) was correct when he suggested that the relatively large middle-ear muscles of bats serve to reduce auditory sensitivity during the emission of each pulse of orientation sound. These muscles also relax rapidly enough that good sensitivity is regained in time to listen for echoes arriving after a few milliseconds. Human middle- ear muscles do not seem to operate with as short a latency, and probably they do not achieve as great a reduction insensitivity as Henson reports for bats (Wever and Lawrence, 1954). Our complete lack of any information about activities of the intra-aural muscles during human echolocation inhibits further speculation along these lines.
Suga and Shimozawa (1974) have recently demonstrated that in bats, along with the action of the middle-ear muscles, purely neural mechanisms attenuate the response to echoes in comparison to the response that would occur if the same sound were to arrive independently from an outside source rather than following a few milliseconds after the emission of an orientation sound. No comparable experiments have yet been carried out on other mammals, still less on men. Hence we cannot yet say whether this type of neural attenuation is an important factor that limits human echolocation in comparison to the superbly effective analysis of information contained in echoes that is achieved by the brains of bats, but the question clearly calls for further investigation.
Another approach to this question is stimulated by the subjective reduction in loudness of echoes of any sounds following closely after a much louder sound. This phenomenon can be demonstrated by making a tape recording of a loud sharp click that lasts only a few milliseconds. If the recording is made in any ordinary indoor situation, the click will be followed by a gradually decreasing series of echoes from the walls, floor, and other objects within a few feet of the recording microphone. When played back in normal fashion, these succeeding echoes will not be noticeable any more than they were with the original click, except for a slight dulling of its quality. But if the tape is played in reverse, so that the echoes precede the sharp click, their gradual buildup over several milliseconds is clearly audible as a hissing sound of growing loudness leading into the click itself. "Click" becomes "shhhick." Would a procedure as simple as time-inverted playback rescue the information so important to the blind?
It is not altogether clear how this reduction in subjective loudness of echoes is achieved in the human brain, or even at what neuroanatomical level it occurs. But the information of vital importance to echolocation is obviously contained in the same time span as that during which the suppression of echoes occurs. Perhaps this echo suppression is absent, or even reversed, in echolocating animals, as suggested by the recent experiments of Suga (1973). If so, this might explain their superior ability to react to echoes following within milliseconds after a loud orientation sound.
These compounded speculations can be useful only insofar as they stimulate new inquiry, preferably direct experimentation. But they lead to an inverse question: Why did human beings acquire the echo-suppression mechanism in the first place? Could it be helpful, if not essential, for the discrimination of speech, especially indoors or in situations where multiple echoes confuse the wave forms of impinging vocal signals that must be analyzed in order to extract meaningful information from messages of another member of the same species? Physicists have sometimes expressed surprise that we can understand speech at all when it arrives in such a jumble of interfering patterns that any direct oscillographic display makes sensible distinctions appear hopeless.
To be sure, the well-known emphasis of the auditory analyzing system upon Fourier analysis, and its almost total disregard of phase information, helps explain this discrepancy. Experiments by Batteau (1967, 1968), discussed by Freedman (1968), have shown that the human auditory system can respond differentially to clicks arriving at the external ear from different directions, and that this factor accounts in part for our ability to localize the direction of instant- ness of sounds even when only one ear is involved.
In Griffin (1968) I left to others to judge whether such conjectures could usefully be carried back into the evolutionary history of our remote ancestors at the stage when human speech first developed into a form that we would recognize as such. While I am not aware that my suggestion has yet led to any new experiments or new theoretical insights, I again suggest that the question remains significant for our understanding of human echolocation and perhaps also for theories about the evolution of human speech.
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