NDRB 4583 Neural Circuits: Barn Owl Auditory Prey Localization PDF

NDRB 4583: Neural Circuits 5. Barn owl auditory prey localization CHAPTER 5: Auditory localization Big question: how do barn owls locate prey using sound? Key Concepts Interaural level difference (ILD) vs Interaural time differen...

NDRB 4583: Neural Circuits 5. Barn owl auditory prey localization CHAPTER 5: Auditory localization Big question: how do barn owls locate prey using sound? Key Concepts Interaural level difference (ILD) vs Interaural time difference (ITD) Barn owl morphological adaptations Head rotation experiments Bird ILD/ITD pathways Adolphs & Jeffress models for ILD/ITD computation Spatial map formation and receptive fields Effects of lateral inhibition Visual displacement plasticity  NDRB 4583: Neural Circuits 5. Barn owl auditory prey localization 5.0 Overview: Auditory scene analysis The temporal and harmonical interplay between multiple instruments, for instance, in a jazz tune, results in a complex composite waveform. When impinging on the ears, this waveform generates a one- dimensional movement of the eardrums. The auditory system is able to extract all relevant physical cues to identify and distinguish the various sound sources, i.e., the instruments, from this one-dimensional movement of the eardrums. A fundamental problem in auditory sensing is sound localization. Where in space is the sound coming from? Imagine that you are blindfolded and surrounded by a group of people. Someone shouts “I’m here”. Just by sound, your brain can calculate which direction the sound came from. How does it do this basic computation? 5.1 Barn owl The barn owl (Tyto alba) is a nocturnal hunter that can find and track its prey in the darkness solely relying on acoustic cues. The owl hears rustling noise created by a small terrestrial animal and quickly locates the source of the sound using binaural acoustic information. The hearing range of barn owls covers frequencies from 0.2 to 12 kHz. This is rather narrow compared with mammals but broad in comparison with other birds. The lowest thresholds are found between 4 and 8 kHz. Overall, owl sound sensitivity is greater than that for humans (but about the same as a cat).  NDRB 4583: Neural Circuits 5. Barn owl auditory prey localization 5.2 Interaural time- and level-difference Sound reaching the ears can be compared based on differences in the level/amplitude and timing of the crests of sound waves reaching one ear compared with the other, referred to as interaural level difference (ILD) and interaural time difference (ITD), respectively. Sound reaching a closer ear generally has a greater amplitude than sound reaching the other (unless the subject is directly facing the source of sound). Similarly, sound waves reach a closer ear sooner than they reach the other. We will see how both modalities are used to calculate the location where the sound originated. Azimuth describes locations along the horizontal plane, while elevation describes locations along the vertical plane. In humans and other animals, elevation is determined by differences in the spectral waveform; sounds from one direction in elevation reaching the ear are filtered compared with sounds from another. This is why our ears (pinna) look funny! We will see that barn owls use ILD. We will see that azimuth is determined by ITD.  NDRB 4583: Neural Circuits 5. Barn owl auditory prey localization 5.3 Barn owl morphological adaptations The outstanding auditory capabilities of barn owls are due to morphological as well as neuronal specializations. The concavity of the facial disc forms a circular paraboloid that collects sound waves and directs those waves towards the owl's ears. The facial ruff functions as a sound collector and amplifier guiding the incoming sound to the ear openings. The facial ruff also enhances the directionality of the ears. Also note the asymmetry of the ear flaps (preaural flaps). The feathers making up this disc can be adjusted by the bird to alter the focal length of this sound collector, enabling the bird to focus at different distances and allowing it to locate prey by sound alone under snow, grass, and plant cover. The ruff consists of auricular and reflector feathers. While the auricular feathers are sound transparent and have mainly a protective function, the reflector feathers that line up at the border of the ruff reflect the sound towards the ear openings. The right ear is more sensitive above the horizontal plane, while the left ear is more sensitive below the horizontal plane.  NDRB 4583: Neural Circuits 5. Barn owl auditory prey localization 5.4 Head rotation experiments Owls are able to rotate their head in a full 260 degrees, while they have limited oculory mobility. Their head will move in the direction of a perceived sound. In the laboratory, we can measure owl head rotation in response to a sound stimulus. A detection coil is placed on the head of the owl. The owl is placed on a platform surrounded by an induction coil with a current passing through it. As the owl’s head turns, a current is generated in the detection coil and is relative to the position of the head. A sound that is of interest to the bird can be generated using a speaker positioned at various elevations (how high up) and azimuths (left to right). A second speaker can be used as a reference point. The animals are trained to move their head toward the direction of a sound We can then measure where the owl attends its gaze with respect to elevation and azimuth in response to the sound. 5.4.1 Detecting elevation: ILD Here we will examine how increasing or decreasing sound level arriving in the left or right ear affects the owl’s attention. To do this, we place an ear plug that will reduce sound entering one or the other ear. A soft plug minimally reduces sound levels, while a hard plug provides greater sound reduction. We can compare the position of the owl’s head relative to the actual location of the sound.  NDRB 4583: Neural Circuits 5. Barn owl auditory prey localization In the results shown to the right, we see that when the left ear is plugged the perceived sound appears to the owl to come more from the right, but significantly more elevated. Conversely, when the right ear is plugged sound is perceived to come from the left, but also from below. From this experiment it was concluded that interaural level difference (ILD) contributes most to localizing elevation. We will see later that azimuth is determined by interaural time difference (ITD). Localizing elevation is frequency dependent. For low frequencies the left ear is slightly more sensitive, sound is not efficiently reflected, and there is horizontal alignment between the left and right ears (i.e. no difference in elevation). At high frequencies both ears are equally sensitive, sound is reflected by the facial ruff. But note the vertical alignment between the left and right ears. 5.4.2 Detecting azimuth: ITD Something to think about: As we said earlier, the crests of sound waves reach the closer of the two ears. Since sound moves through air around 340 m/second and the distance between the ears of a barn owl is about 0.1 meters, then we might expect that the maximum difference in  NDRB 4583: Neural Circuits 5. Barn owl auditory prey localization arrival time for a particular wave would be 2.9x10-4 seconds or 290 microseconds! And if we consider ongoing temporal disparity (discussed more below), for a frequency within the range of detection for the owl (let’s say ~3 kHz), we’re talking about detecting that time difference every 0.3 milliseconds. There are two ways that difference in time can be detected binaurally (i.e. with both ears). First, from the onset or offset time disparities between the two ears. The advantage of this signal is that it is less likely to be confused with echos. Second, from the ongoing disparity of sound waves between the two ears. This has the advantage that precision can be achieved by repeated measurements. We can experimentally vary ongoing temporal disparity by adjusting the phase of sound reaching either of the ears. As shown in the figure to the right, varying tens of microsecond differences in the phase of incoming sound causes the owl to move its left or right. 5.4.3 ILD + ITD = location  NDRB 4583: Neural Circuits 5. Barn owl auditory prey localization It should now be obvious that the combination of both ILD and ITD provide a spatial map of both azimuth and elevation. In the figure to the right, we see a barn owl detecting sound from a mouse on the ground (a). The brief pulse of sound has both level disparity (left ear detects greater amplitude than the right) and time disparity (left ear detects the sound waves before the right). Therefore, the mouse is positioned to the left and below the orientation of the bird’s face. The globes (b & c) represent space around the head relative to the line of sight (remember that the eyes of a barn owl are nearly stationary). (b) For ITD values, purple indicates left ear leading and pink indicates right ear leading, while for ILD values (c) green indicates left ear greater and blue indicates right ear greater amplitudes. 5.3 Bird Brain Auditory Circuitry The inferior colliculus (IC) is a central processing unit through which almost all auditory information must pass before it can reach the more central nuclei in both mammals and birds. The correct anatomical term for the avian homolog of the IC is mesencephalicus lateralis dorsolis (MLd). We shall use the term IC. Much more is known about the mammalian IC than the avian IC. On the other hand, the barn owl IC shows some specializations that make it interesting for comparative studies on the anatomy and function of the auditory system. There are similarities between the auditory circuit of the mammalian and avian brains, but also differences. We’ll focus on the avian brain here.  NDRB 4583: Neural Circuits 5. Barn owl auditory prey localization In a simplified view of the avian circuit, as shown above, auditory information from the cochlea arrives via the 8th cranial nerve to both the nucleus magnocellularis (NM) and the angular nucleus (NA). From these two nuclei, two pathways lead to the IC in the midbrain: the ILD and ITD pathway. Note that both pathways are bilateral, there is communication between each side of the brain, and both IC project (and converge) in premotor cortex (and other locations). 5.3.1 ILD pathway (elevation) What follows is an extremely simplified view of the ILD pathway. It is based on a model proposed by Adolphs (1993). Sound intensity information is reported by the firing rates of NA neurons that project to the posterior portion of the dorsal nucleus of the lateral lemniscus (LLDp), and then onto the central or core inferior colliculus (IC). In addition, there is reciprocal inhibition between both LLDp regions. Firing of cells in the left LLDp inhibit cells in the right LLDp, and vice versa. However, the amount of inhibition onto a particular cell varies due to the properties of each inhibitory synapse. As shown in the figure above (A), input on one side excites a set of LLDp neurons, each with roughly the same strengths. The amount of reciprocal inhibition, however, systematically varies between cells. As a result, the net firing of these neurons will also vary and the number of cells that fire will depend on the relative intensity of the contralateral sound input (i.e. louder contralateral input, few neurons will fire).  NDRB 4583: Neural Circuits 5. Barn owl auditory prey localization For sound right in front of the owl, intensity should be about equal on both sides (panel B, above), we see that on the left side three of the five cells fire (green, a-c), and three cells on the right side also fire (c’-e’). If neurons c and c’ project to the same neuron in IC, that midbrain neuron will respond when intensity is equal to both sides. If the sound is coming from the right side, the left side receives less intense sound and maybe only 2 of the 5 cells fire (a & b), while on the contralateral side 4 of the 5 fire (b’-e’). If neurons b and b’ project to the same neuron in IC, that midbrain neuron codes for sound coming slightly from the right side of the owl’s head. There are thousands of neurons in the LLDp and we expect a continuous function of different firing rates that follows a sigmoid relationship (C, above). Given that the contralateral side should also be the opposite sigmoid function, we would predict that the product of the two (convergence in the IC) would be Gaussian-like. Indeed, neurons in the IC respond to specific ILDs. 5.3.2 ITD pathway (azimuth) As we saw above, sound information from the 8th nerve also innervates the nucleus magnocellularis (NM), which projects to the nucleus laminaris (NL) along the ITD pathway. This pathway carries information relating to sound timing between the two ears. Jeffress Model Lloyd Jeffress (1948) proposed a time-delay neural network model that receives two sets of stimulus-locked spike train signals from the left and right auditory pathways and uses a set of delay lines and coincidence detectors to compute a temporal cross- correlation function.  NDRB 4583: Neural Circuits 5. Barn owl auditory prey localization The model suggests a systematic spatial arrangement of delay lines and coincidence detectors. This allows the network to convert an interaural temporal disparity into a maximum place of neural excitation. Sensory information from the hair cells of the ears travels to the ipsilateral nucleus magnocellularis (NM). From here, the signals project ipsilaterally and contralaterally to two nucleus laminari (NL). Each nucleus laminaris contains coincidence detectors that receive auditory input from the left and the right ear. Since the ipsilateral axons enter the nucleus laminaris dorsally while the contralateral axons enter ventrally, sounds from various positions along the azimuth correspond directly to stimulation of different depths of the nucleus laminaris. From this information, a neural map of auditory space is formed.  NDRB 4583: Neural Circuits 5. Barn owl auditory prey localization Evidence that neurons in the nucleus laminaris form a neural map is supported by the following experiment: an electrode is systematically guided through the nucleus laminaris. At varying distances along the dorsal- ventral axis, the firing rate of neurons is measured as a function of ITD. The dorsal neurons are tuned towards ITD fire at greater rate with sounds from the left, while those in the most ventral fire more with sounds from the right. The population of neurons sensitive to a particular ITD will be Gaussian due to variations in delay line lengths and the threshold for coincidence detection. The Jeffress model was computationally tested and there was a problem. The contralateral pathway is significantly longer than the ipsilateral pathway; spikes will not ever arrive at the same time assuming that the properties of the axons are the same. However, if a) the ipsilateral pathway is slower (i.e. thinner diameter or smaller internodal distance) and b) the contralateral pathway is faster (larger diameter fibers, greater internodal distance, spikes can arrive at the same time. Therefore, there must be developmental control of ITD tuning! Phase-locked responses  NDRB 4583: Neural Circuits 5. Barn owl auditory prey localization Another issue with the Jeffress model is how auditory neurons respond to high frequency input. If the frequency of a sound is operating at 5 kHz (about the mid-range for the owl), then the period of the signal is going to be 0.2 milliseconds. Individual auditory neurons cannot follow that high frequency. Phase or time-locking is where a neuron fires in synchrony with the phase of a stimulus, but not necessarily with the peak of every cycle. If there are more than one neuron phase-locked to a signal, then it is possible for a population of neurons to encode periodic information. 5.4 Spatial Maps Electrodes can be implanted into the IC of the barn owl, while head direction is simultaneously monitored. Single sound- sensitive neurons exhibit a specific spatial range.  NDRB 4583: Neural Circuits 5. Barn owl auditory prey localization In the figure above we see the responses (i.e. firing rates) of a single neuron along the horizontal (azimuth) plane and along elevation. The neuron fires greatest when a sound is presented at 10 degrees to the right in the azimuth plane, but also when the sound is positioned at 0 degrees in elevation. The spatial region where the neuron fires above noise, also called a receptive field, occupies an area noted by the grey oval. After recording from many neurons, we see that there is a map across the IC; optimum firing rates systematically vary with location. Along the sagittal plane, elevation is mapped, whereas along the  NDRB 4583: Neural Circuits 5. Barn owl auditory prey localization horizontal plane relative ipsilateral/contralateral azimuth direction is reported. An interesting aspect of these receptive fields is that they are surrounded by inhibitory space. Sound outside of the receptive field actually reduces ambient neuronal firing. This results from 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. The example on the right uses a receptive field from the skin to demonstrate the effect of lateral inhibition Why is the receptive field ovoid in shape?  NDRB 4583: Neural Circuits 5. Barn owl auditory prey localization Remember that the response of an individual cell in the IC to varying ITDs and ILDs is roughly Gaussian. Assuming that ITD- sensitive neurons from the nucleus laminaris and ILD sensitive neurons (most likely from the nucleus angularis) converge in the IC, then spatio-temporal summation would lead to an oval relationship for firing rates along elevation and azimuth. 5.5 Visual Displacement Plasticity The IC also projects to the external IC (ICX), which is then linked to the optic tectum (OT --- in fish, reptiles, and birds the OT is the main visual processor in the brain). There is a strong relationship between visual localization and sound localization. This was demonstrated in a classic experiment where barn owl chicks were given 23 degree prisms, that offset visual input, to wear during early development. After one day with the prisms, the barn owl chick moves its head 23 degrees offset in response to a visual cue, while its auditory response isn’t affected. However, after more than a month with the goggles, the auditory response is offset the same distance as the visual response, even though there has been nothing done directly  NDRB 4583: Neural Circuits 5. Barn owl auditory prey localization to the auditory system! After the prisms have been removed, the barn owl can correctly attend to the visual stimulation pretty quickly, but the auditory response remains offset. It was hypothesized that there is plasticity in the auditory connections from the ICX to the optic tectum. Horizontal shifts in the visual field of OT neurons is accompanied by a shift in ITD tuning. In panel D, we see the shift in the projection of information from the ICC to the ICX (black and red arrows) that results from early prism experience. Left normal responses, right after several weeks of prism experience. Note that units that normally respond to 0 ITD (receptive field at 0° azimuth, i.e., vertical  NDRB 4583: Neural Circuits 5. Barn owl auditory prey localization meridian), following prism experience are tuned to 50 μs ITD (corresponding to 20° from the vertical meridian). Labeled axons in ICX after focal injections of a tracer (biocytin) in the ICC. A normal juvenile is shown on the left, prism-reared owl with a rostrally shifted map of ITD in the ICX is on the right. The quantitative shift in axonal sprouting after adaptation is shown in the figure to the right.  NDRB 4583: Neural Circuits 5. Barn owl auditory prey localization Normal After Prism Experience Learned responses depend, at least in part, on the formation of new synapses. When an instructive signal (visual cues) are paired with auditory cues, synaptogenesis or insertion of AMPA receptors is triggered. The new synapses initially are dominated by NMDA- receptor currents, suggesting that they were originally “silent”, and required the coincident instructive signal to induce AMPA receptor insertion. Also, GABAergic inhibition preserves the established network. With learning, inhibition can limit or block the normal response and promote the learned response.  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).