Bat Echolocation: Neural Circuits - PDF

NDRB 4583: Neural Circuits 4. Bat Echolocation CHAPTER 4: Bat Echolocation Big question: how do bats calculate distance and speed of their prey? Key Concepts Physics of sound Information a bat needs to calculate...

NDRB 4583: Neural Circuits 4. Bat Echolocation CHAPTER 4: Bat Echolocation Big question: how do bats calculate distance and speed of their prey? Key Concepts Physics of sound Information a bat needs to calculate the location of a moving moth FM vs CF bats The mammalian auditory system Neuronal calculation of range and velocity  NDRB 4583: Neural Circuits 4. Bat Echolocation 4.0 Overview If you ask a baseball coach what makes the game of baseball so difficult, you might hear the response “You’re trying to hit a round object moving with high velocity with another rounded object also moving at high velocity”. A batter uses visual sensory input to compute the speed and direction of the incoming ball. The brain and motor system then makes calculations governing the motor system so that the bat is swung and makes appropriate contact with the ball. We can’t study the circuitry of a human baseball player. But there is an animal model that comes close. The main prey of most bats are small, quick-moving insects. In the figure below, a bat is capturing a meal worm (MW) projected into the air. The task of hunting is made even more difficult for bats because they are only active at night, dusk and dawn. To help them find their prey in the dark, most bat species have developed a remarkable navigation system called echolocation or biosonar. Bats use of sound waves and echoes to determine where objects are in space. 4.1 Sound Sounds is the perception of pressure waves of air, the alternating density of gas molecules. Waves of changing pressure propagate across distance. Someone’s vocal chords or a loudspeaker generates variations in air pressure. When they propagate to you, differences in air pressure make the tympanic membrane in your inner ear vibrate.  NDRB 4583: Neural Circuits 4. Bat Echolocation Sound waves are characterized by their amplitude and frequency (pitch). The amplitude of a sound is the amount of change in air density. The greater the change, the greater the amplitude. Period is the time between the compressed air peaks. Frequency is the inverse of period (1/period) and is measured in cycles per second or Hertz (Hz). A complex sound is the result of the combination of multiple sine waves of different amplitudes, frequencies, and phases (time delays between peaks). Information can be encoded in sound in a variety of ways. Three of the simplest are constant frequency (CF), amplitude modulated (AM), and frequency modulated (FM) signalling. CF signalling is the generation of a constant tone a specific frequency and harmonics. Harmonics are waves with a frequency that is a positive integer multiple of the frequency of the original wave, known as the fundamental frequency. An AM signal carries information by variations in amplitude as a function of time. In contrast, FM signals are conveyed by changes in frequency as a function of time.  NDRB 4583: Neural Circuits 4. Bat Echolocation 4.2 Bat calls during hunting Bats use CF, FM, or both CF and FM signaling. The Big Brown Bat (Eptesicus) primarily uses FM calls for echolocation, while the Horseshoe Bat (Rhinolophus) uses a combination of FM and CF calls. The fruit bat Rousettus uses a very fast FM call, which is more of a “click”. Note that Eptesicus and Rhinolophus calls have harmonics! Harmonics result from the resonant properties of strings (i.e. vocal chords), as well as resonant properties of the bat’s head. While hunting the interval between calls increases as the bat approaches the prey, then tracks the prey, and finally captures the play (Terminal). The figures above are called sonograms; the ordinate is frequency and the abscissa is time. As before, as the bat approaches and tracks its prey, the interval between calls increases. First, note the the harmonics produced by Eptesicus, but not Rhinolophus, are  NDRB 4583: Neural Circuits 4. Bat Echolocation shown in this figure. But also note that the characteristics of the FM (Eptesicus) or CF-FM (Rhinolophus) signals changes as well. 4.3 Pulse-echo sensitivity? We can place a hungry bat on a perch in front of two platforms that are sound-reflective and train it to seek prey. Using a microphone and loudspeaker system, a simulated or phantom target can be generated by controlling which speaker is activate, as well as the amplitude and timing of the echo can be controlled. If the bat is given the choice between two phantom targets and the time delay between the two is very small (zero jitter), the bat will choose either of the targets roughly 50% of the time. But if one echo arrives sooner, the bat will pick the earlier echo. The bat can sense a difference of as little as a 20 nanosecond difference in timing, corresponding to a detection resolution 0.1 mm! 4.4 How to catch a moth Distance (range)  NDRB 4583: Neural Circuits 4. Bat Echolocation Calculated from the difference in time between the call and the echo. Target Range (distance) = speed of sound x Pulse-echo delay / 2 Azimuth and Elevation Azimuth is calculated from binaural cues, including interaural time difference (ITD) and interaural level difference (ILD). Elevation is determined by a) moving ears and comparing positions and b) the influence of the pinnae on sound patterns. Prey size The size of the prey can be calculated from the amplitude of the echo and delay. At a given distance, size should be related to the amplitude. Small amplitude echo, small moth. But what if the moth was farther away? Then the amplitude of the echo should be even smaller. A large amplitude echo and a long delay would indicate that the prey is huge!  NDRB 4583: Neural Circuits 4. Bat Echolocation Prey Velocity and distinguishing prey from clutter The concept of the Doppler effect or shift is central to understanding how bats determine which direction the prey is flying. The Doppler effect is observed whenever the source of waves is moving with respect to an observer. The Doppler effect can be described as the effect produced by a moving source of waves in which there is an apparent upward shift in frequency for observers towards whom the source is approaching and an apparent downward shift in frequency for observers from whom the source is receding. The echo returning off of an insect flying toward a bat will be shifted to higher frequencies, while an insect flying away will shift the echo to a lower frequency. For a stationary object, there should be no change in frequency. Doppler Shift: fe = fc (1 + 2 x flight speed / speed of sound) (fe = frequency of the echo; fc = frequency of the call)  NDRB 4583: Neural Circuits 4. Bat Echolocation As an added bonus, the flutter of the insect will also affect the frequency returning to the bat, further identifying the object as prey. In general, bats that emit FM/Click sounds live in open areas, free of foliage and clutter. In contrast, CF/FM bats generally live in environments with heavy vegetation. FM/Click calls are good for determining range. Different targets reflect sounds preferentially at certain frequencies. CF calls are good for velocity and flutter; the bat can detect differences in the frequency of the return signal. This can’t be done with FM or click. Additionally, depending on the environment, one of the harmonics may provide a stronger return than the fundamental frequency of the call. The bat also hears its own first harmonic, which may be weak to other bats!  NDRB 4583: Neural Circuits 4. Bat Echolocation The combination of CF and FM, such as in mustached bats solves the “clutter problem”; how does that bat tell the difference between its prey and the surrounding vegetation? Different harmonics may also provide more information for the bat. For distant prey, the bat may attend to lower harmonics that are generally stronger in amplitude, have less attenuation. For close prey, the higher harmonics may be stronger providing finer detail. Flutter of the prey can be used by the bat to discriminate between different insect species. When the wings are directly opposed toward the angle of the sound, the amplitude of the echo will be  NDRB 4583: Neural Circuits 4. Bat Echolocation greater than when they are facing away. The difference in this amplitude further contributes to identifying the return signal as prey. The key to understanding how bats discriminate prey from “clutter” is the phenomenon of Doppler shift compensation (discussed further below). In an experiment where a moth was placed on a pendulum swing, moving toward and away from the bat, the bat varied its call to maintain what is called an acoustic fovea. Varying the call frequency makes the “reference” frequency of the echo stay constant! The bat adjusts the frequency of the call. We will see later that this results in an extremely efficient mechanism for calculating velocity using biosonar.  NDRB 4583: Neural Circuits 4. Bat Echolocation 4.5 The mammalian auditory system Tympanic auditory systems have appeared three times during evolution: in amphibians, reptiles and avian ancestors, and mammals. In the mammalian auditory system, sound waves enter the outer ear and travel through a narrow passageway called the ear canal, which leads to the eardrum. The eardrum vibrates from the incoming sound waves and sends these vibrations to three tiny bones in the middle ear. These bones are called the malleus, incus, and stapes. The bones in the middle ear amplify, or increase, the sound vibrations and send them to the cochlea, a snail- shaped structure filled with fluid, in the inner ear. An elastic partition runs from the beginning to the end of the cochlea, splitting it into an upper and lower part. This partition is called the basilar membrane because it serves as the base, or ground floor, on which key hearing structures sit. Once the vibrations cause the fluid inside the cochlea to ripple, a traveling wave forms along the basilar membrane. Hair cells—sensory cells sitting on top of the basilar membrane— ride the wave. Hair cells near the wide end of the snail-shaped cochlea detect higher-pitched sounds. Those closer to the center detect lower-pitched sounds. Bat sound sensitivity ranges from 100 kHz to 10 kHz. As the hair cells move up and down, microscopic hair-like projections (known as stereocilia) that perch on top of the hair cells bump against an overlying structure and bend. Bending causes pore-like channels, which are at the tips of the stereocilia, to open  NDRB 4583: Neural Circuits 4. Bat Echolocation up. When that happens, chemicals rush into the cells, creating an electrical signal. Hair cells trigger spikes in specific auditory neurons that project to the cochlear nucleus. From their, neurons project ultimately to the auditory cortex. 4.6 Tonotopic mapping of frequency If you record from auditory neurons of the mustached bat or the horseshoe bat, you will find that they tend to fire more in response to specific frequencies. These both are CF-FM bats. In contrast, the Little Brown bat only emits FM calls and its auditory neurons are not “tuned” to specific frequencies. The figure to the right are tuning curves from 12 different neurons from the mustached bat. Note the very steep curves for 5 neurons around 61 kHz. 4.7 Auditory Circuit Computations Below is a diagram simplifying the auditory circuit in the mammalian brain.  NDRB 4583: Neural Circuits 4. Bat Echolocation 4.7.1 Range Neurons projecting from the basilar membrane to the cochlear nucleus are tonotopically mapped. So-called “FM neurons” projecting from the cochlea to the cochlear nucleus synapse onto neurons that project to the inferior colliculus. Two sets of neurons project to the medial geniculate body (MGB). One set, FM1 neurons (the call or pulse), project, with a delay, while FM2-FM4 (echo) are tuned neurons that project to the MGB with little delay. The key to calculating range is the difference in time for FM1 and the other FM signals to reach the MGB.  NDRB 4583: Neural Circuits 4. Bat Echolocation Delay-tuned neurons. Pulse echo delay sensitive neurons found in MGB. They only fire when there is a specific delay between pulse FM1 and echo FMx. As mentioned above, two groups of cells in IC project to the MGB. In turn, MGB neurons project to FM/FM area of auditory cortex (AC). Remember spatiotemporal summation? Delay-tuned neurons in the MGB and AC only fire with specific pulse-echo intervals. Differential inhibition has also been proposed as a mechanism to delay sensitivity. If the time course of inhibition varies between neurons, some slow and some fast, then only those neurons stimulated by the echo and in which inhibition has ceased will fire.  NDRB 4583: Neural Circuits 4. Bat Echolocation Finally, MGB neurons project (again, tonotopically) to the auditory cortex. There, one can find neurons that fire in response to specific delays between FM1 and FMx. 4.8.2 Velocity Velocity is calculated based on the Doppler shift. To do this, the bat must compare between two CF frequencies. For the case of the mustached bat, we will consider three channels of sound that are analyzed in parallel (CF1, CF2, and CF3). The CF2 channel pulse and echo have the largest amplitude. Neurons in the medial geniculate body do not respond to CF1, CF2, or CF3 alone. They do fire strongly when CF1 occurs at the same time as CF2 or CF3. The neurons are tuned to fire at precise frequency differences within the CF-CF area of auditory cortex, where there are two types of CF-CF neurons; CF1-CF2 and CF1-CF3.  NDRB 4583: Neural Circuits 4. Bat Echolocation The calculation is achieved simply by the summation of two inputs. A single pulse (CF1) or echo (CF3) alone can’t fire MGB neurons. Velocity-sensitive MGB neurons arise from integration of two CF inputs via spatial summation. Again, MGB neurons project tonotopically to the auditory cortex where neurons are specialized to detect either velocity (CF-CF area), or range (FM-FM area, described above).  NDRB 4583: Neural Circuits 4. Bat Echolocation Doppler Shift Compensation As mentioned earlier, FM bats typically forage in open spaces. CF/FM bats, however, hunt where there is dense foliage. Therefore, some CF/FM bats have evolved a mechanism to better distinguish prey from clutter. Part of the CF2 channel projects directly to the auditory cortex Doppler Shift CF processing area (DSCF). This region has frequency versus amplitude coordinates. It over-represents frequencies between the CF2 resting frequency (~61 Hz) and 1 kHz above it. The DCSF region contains neurons with extremely narrow frequency tuning, centered around the dominant harmonic of the bat call (CF2). The narrowest frequency tuning in any animal’s cortex. This is considered an acoustic fovea. CF bats’ auditory systems are finely tuned to the narrowband frequencies in the calls they produce. This results in a sharp acoustic fovea, as illustrated in the audiogram above. The sharp tuning curve arises because of lateral inhibition. lateral inhibition is the capacity of an excited neuron to reduce the activity of its neighbors. Lateral inhibition disables the spreading of action potentials from excited neurons to neighboring neurons in the lateral direction (i.e. surrounding frequencies). The basilar membrane in the cochlea has receptive fields similar to the receptive fields of the skin and eyes. Also, neighboring cells in the auditory cortex have similar specific frequencies that cause them to fire, creating a map of sound frequencies similar to that of the somatosensory cortex. Lateral inhibition in tonotopic channels can be found in the inferior colliculus and medial geniculate body, as well as higher levels of auditory processing in the brain.  NDRB 4583: Neural Circuits 4. Bat Echolocation Why doppler shift compensation? So Instead of having the animal be highly sensitive to every frequency and then compute the target properties from a wide range of echo frequencies, the animals control something that is relatively easy to modulate-the frequency of the emitted pulses. The resulting neural computation is much simpler to perform; the bat only needs to detect the feedback regulated changes that it actively makes to its pulses, and how this relates to target distance and target properties. Mustached bats live in areas with substantial vegetation, making it difficult to distinguish prey from flora. These bats are CF-FM bats; they produce calls that are a combination of CF and FM pulses. 4.9 Auditory cortex: a summary If we look at the auditory cortex altogether, we see five different subdivisions. First, The anterior and posterior divisions of primary auditory cortex (yellow) are tonotopically mapped and respond to a range of stimulus frequencies from 10 to 100 kHz. The DSCF region (pink) is over-represented at frequencies between 60 and 63 kHz (discussed further below). The, the dorsal-medial area (blue) has neurons that are sensitive to azimuth, as well as elevation. Their sensitivity is based on relative interaural time and level differences (to be discussed further in the Barn Owl chapter).  NDRB 4583: Neural Circuits 4. Bat Echolocation Range is calculated within the FM-FM area (green). Here, the pulse-echo difference, mapped tonotopically from 1-20 ms (direction of arrows), determines distance to the prey. The CF/CF area (orange) has neurons sensitive to differences in the primary call frequency (CF1) relative to the return echo of the harmonics (CF2 and CF3). Their relative tuning maps to differences in velocity (between the bat and the target). Finally, the large DSCF (pink) found in CF/FM bats represents an “acoustic fovea” allowing for high resolution analysis of Doppler shift. It drives motor systems that compensate as moving prey advances or retreats from the bat. This allows the bat to calculate doppler shift due to the flutter of the prey more precisely (in the CF/CF area), permitting identification of prey versus plants (i.e. clutter).