Echolocation

Many kinds of bats have poor vision and yet fly well at night, avoiding obstacles and catching insects at rates as high as two per second. They orient by emitting ultrasonic pulses (i.e., sound at frequencies too high to be audible to humans) and detecting echoes reflected by objects around them. They are able to use the information in the auditory echoes to locate and discriminate prey insects, and catch them in the open and in wooded environments. Box Extension 14.1 describes how echolocating bats detect and catch insects.

The Italian naturalist Lazzaro Spallanzani (1729–1799) provided the first evidence that “bats see with their ears” in 1793. Spallanzani placed hoods over the heads of bats and found that they were disoriented, flying into walls. When the bats were blinded, however, they flew with normal orientation and were still able to catch insects. In an ingenious set of experiments, Spallanzani plugged the ears of bats with either hollow brass tubes or tubes filled with wax. The bats with wax-filled tubes were disoriented, but those with hollow tubes (through which sound could pass) flew normally. Spallanzani correctly concluded that the ears were necessary for oriented flight in the dark but that the eyes were not.

Although Spallanzani’s results were confirmed and extended by Charles Jurine (1751–1819) in 1794, they were disbelieved and became buried in obscurity. Why were Spallanzani’s elegant and surprisingly “modern” experiments given so little credence? We must realize that in the eighteenth century the wave nature of sound was not understood, and thus the concept of sound too high in frequency for humans to hear was inconceivable. In fact, there was no general understanding of the possibility that animals had sensory capabilities that humans lacked.

“Spallanzani’s bat problem” remained unexplained until 1938, when Donald Griffin, using newly developed ultrasound detectors, showed that bats emitted high-intensity ultrasound in the frequency range of 30–100 kilohertz (kHz). Griffin subsequently independently confirmed Spallanzani’s experiments and demonstrated that bats orient by detecting the echoes of their ultrasonic cries.

Even with our present, relatively good understanding of the phenomenon, bat echolocation is a mind-boggling display of sensitivity and precision. Most species of bats emit ultrasonic cries, typically as pulses of either constant frequency (CF bats) or of decreasing frequency within each pulse (frequency-modulating, or FM, bats). The little brown bat (Myotis lucifugus) is an example of an FM bat. A cruising Myotis emits pulses that sweep in frequency from 80 to 40 kHz. The sound energy of these pulses is an enormous 120 decibels, equivalent to a jet plane taking off 100 m away. Bat cries would be nearly deafening to humans if their sound energy were within the human auditory frequency range.

Despite the intensity of their cries, the echoes that bats detect are extremely faint. Echolocating bats must detect and orient to faint echoes that arrive within 20 milliseconds (ms) after emitting a potentially deafening cry. Several physiological and anatomical specializations contribute to this ability. The inner ear is mechanically isolated from the rest of the skull, decreasing bone conduction of the cry to the ear. Auditory sensitivity is effectively decreased during a cry by contraction of tensor tympani muscles (see page 379), and the recovery of sensitivity after the cry is extremely rapid. Some bats have a selective short-term enhancement of auditory sensitivity during a period 2–20 ms after calling—an appropriate time frame for detecting echoes returning from an object 34–340 cm away.

CF bats make use of the Doppler shift of sound frequency to enhance echo detection. The Doppler shift is a shift in sound frequency (and pitch) based on movement of the sound source relative to the observer. If the bat is approaching an object, the Doppler effect will shift the echoes returning from the object to a higher frequency—the same phenomenon that causes the familiar increase in sound frequency when a train or siren is approaching, and then the decrease in frequency when the source passes and begins to recede. The ears of CF bats are sharply tuned to a frequency several kilohertz higher than their cries. Thus their auditory sensitivity is much greater to Doppler-shifted echoes (from an object being approached) than to the cry itself.

How does a bat’s brain process the complex auditory information to catch prey or avoid objects? Neural auditory processing of echolocation signals has received considerable study in mustached bats (Pteronotus). Mustached bats are CF/FM bats: Their call has a relatively long CF tone with a short FM downsweep at the end (see figure).

Echolocation in a mustached bat The cry of a mustached bat has both constant-frequency (CF) and frequency-modulated (FM) portions. The graph is a sonogram of sound frequency as a function of time. Solid lines represent the cry; the width of the line indicates loudness. The fundamental frequency (CF₁) is weak, and the bat hears it by bone conduction. Several overtones (CF₂, CF₃, CF₄) are louder. Echoes (dashed lines) return with a time delay (indicating distance) and with a Doppler-shifted frequency (indicating the bat’s approach velocity). A large area of the bat’s cerebral cortex is devoted to processing auditory information for echolocation. Some areas process the time delay of the FM sweep to determine target distance, and other areas process the degree of Doppler shift to determine relative velocity.

The fundamental frequency of the tone is 30 kHz, with harmonics at 60, 90, and 120 kHz. The Doppler shift of the CF tone conveys information about approach velocity to the target; the delay of the echo’s FM sweep gives information about the target’s distance; and the strength of the echo indicates relative target size. A considerable area of the bat’s cerebral cortex is devoted to processing different aspects of this coded information.

Bats, of course, must not only detect echoes, but must also determine their direction with great accuracy. Several auditory specializations contribute to this localization. For example, contralateral inhibition is well developed in bat auditory centers. Many CNS auditory neurons are excited by sound stimulation of one ear and inhibited by sound stimulation of the other ear. Behavioral experiments indicate that these neurons must be sensitive to differences as small as 0.01 ms in time of stimulation of the two ears. Several other auditory mechanisms contributing to echolocation have been explored. No matter how much we learn about the mechanisms of bat echolocation, however, the performance itself remains amazing. Not only can bats catch two insects a second, but the insects can be as small as mosquitoes and fruit flies.

Echolocation is not confined to bats. Neotropical oilbirds orient through caves by echolocation, and dolphins employ sound pulses for echolocation, as well as for communication.

References

Moss, C. F., and S. R. Sinha. 2003. Neurobiology of echolocation in bats. Curr. Opin. Neurobiol. 6: 751–758.

Simmons, J. A., S. P. Dear, M. J. Ferragamo, T. Haresign, and J. Fritz. 1996. Representation of perceptual dimensions of insect prey during terminal pursuit by echolocating bats. Biol. Bull. 191: 109–121.

Suga, N. 1989. Principles of auditory information-processing derived from neuroethology. J. Exp. Biol. 146: 277–286.

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