causing EPSPs or IPSPs. In contrast, neuromodulators alter neuronal activity slowly, by biochemical means.
The effects of neuromodulators appear to be mediated by substances within the postsynaptic neuron called sec-ond messengers (Breedlove et al. 2007). These secsec-ond messengers (e.g., calcium and the cyclic nucleotides cAMP and cGMP couple the membrane receptors of the postsynaptic cell with the movements of ions through one or more enzymatic steps. Neuromodulators may, for exam-ple, upon reaching the receptor on the postsynaptic neu-ron, trigger the formation of the second messenger cAMP within the neuron, which in turn activates an enzyme that changes the shape of proteins in certain ion channels. Once the ion channels have been altered in this manner, the per-meability of the membrane to specific ions is also changed, thereby affecting the activity of the neuron. It is the rela-tively slow pace of the enzymatic activities that produces the typically prolonged effects of neuromodulators.
Functionally, neuromodulators appear to be inter-mediate to classic neurotransmitters and hormones.
Whereas neurotransmitters are released at specific synaptic clefts and hormones are broadcast throughout the body via the bloodstream, neuromodulators are released in the general vicinity of their target tissue. It is, however, difficult to establish the precise point at which a neurotransmitter becomes a neuromodulator, and a neuromodulator a hormone. In fact, the same chemical may have different functions in different places. Some chemicals, dopamine, for instance, act as neurotransmitters at some synapses and as neuromodu-lators at others. Similarly, a chemical may act locally in the nervous system as a neurotransmitter, whereas in other places in the body it is released into the blood-stream and acts at a distant site as a hormone does (see Chapter 7 for a discussion of hormones). Despite some fuzziness in definition, there is no question that neuro-modulators, through their actions on neurons, glands, and muscles, can produce profound effects on behavior.
Consider the behavior of the male blue crab (Callinectes sapidus) as an example of neuromodulation of rhythmic movements of the swimming legs. Just before a female blue crab matures, she releases a pheromone, a chemical used to communicate with other members of the species, in her urine. When a male blue crab senses the pheromone, he begins his courtship display. He spreads his claws apart in front, extends his walking legs, and raises his swimming legs in the rear. He then waves his paddle-shaped swimming legs from side to side above the carapace (Kamio et al. 2008). Besides courtship, two other distinct stereotyped behaviors, sideway swimming and backward swimming, involve the rhythmic move-ment of swimming legs. In each behavior, the swimming legs are waved in a slightly different way and the crab assumes a different posture. However, because these three behaviors are so similar, it is likely that they share common neural elements (Wood 1995a).
Neuromodulators, combined with the proper olfactory stimulation, affect whether the crab will per-form the courtship display instead of the two swimming behaviors. When the neuromodulators proctolin, dopamine, octopamine, serotonin, and norepinephrine are separately injected into blue crabs, each drug pro-duces a unique posture or combination of limb move-ments. The postures and limb movements are the same as those observed in freely moving, untreated crabs.
Injection of dopamine produces the posture of the courtship display, in which the male stands high on the tips of his walking legs; injection of proctolin produces the rhythmic leg movements characteristic of courtship that serve to fan chemicals in his urine (pheromones) toward a female to attract her (Wood 1995b).
Electrical stimulation of specific neurons under dif-ferent conditions has identified interneurons in the esophageal connectives (neural connections between the brain and ventral nerve cord) that trigger rhythmic wav-ing of the swimmwav-ing legs. Some of these interneurons trigger rhythmic leg waving when sex pheromone is applied to the antennule of the crab. Under these con-ditions, the leg waving is not distinctly characteristic of any of the three rhythmic behavior patterns. However, when proctolin is applied while these interneurons are being stimulated, the motor output changes to the rhyth-mic waving of the courtship display (Wood 1995b). The natural source of the proctolin that initiates courtship leg movements is thought to be a cluster of nerve cells in the subesophageal ganglia (Wood et al. 1996).
has been adjusted by natural selection so that peak sensitivity occurs at the most common wavelength of light in a given habitat (Bowmaker et al. 1994; Lythgoe et al. 1994). We will see more examples of sensory tun-ing when we explore the evolution of communication in Chapter 17.
Besides detecting stimuli critical to survival, animals must be able to pick out that stimulus from a back-ground of “noise” in the same sensory modality. For example, recall that the cockroach runs when exposed to a gust of wind from a predator. Yet, it ignores non-threatening or irrelevant sources of wind, such as the wind that it creates itself while walking. How is such selectivity possible? In the laboratory, cockroaches run when exposed to wind with a peak velocity of only 12 mm per second, the approximate velocity of wind cre-ated by the lunge of a predator such as a toad.
Cockroaches, however, do not respond to the 100-mm-per-second wind that they create by normal walking.
How is it that cockroaches manage not to respond to the relatively strong wind created by walking and yet run when exposed to much softer wind signals? It turns out that it is not the velocity of the wind that is the critical factor but the acceleration (rate of change of wind speed), and a strike by a predator delivers wind with greater acceleration than the wind produced by the step-ping legs of a cockroach. In fact, when cockroaches were tested with wind puffs that had the same peak velocity but differed in acceleration, they ran more frequently when exposed to winds of higher acceleration (Plummer and Camhi 1981). Winds with low acceleration typically produced no response. Thus, cockroaches appear to pay particular attention to the acceleration of the wind stim-ulus, and this allows them to ignore irrelevant wind sig-nals and to focus on important information in their environment.
PROCESSING OF SENSORY INFORMATION FOR SOUND LOCALIZATION
We will consider the mechanisms of sound localization as an example of stimulus processing of biologically important stimuli. It is often important for an organ-ism to locate the source of sound. For example, a potential mate may be producing the sound. A male mosquito finds a female by the sound of her beating wings. It would do a male little good to know that a female was present and be unable to locate her.
Similarly, many predators determine their prey’s posi-tion by localizing sounds generated by the prey.
Locating the source of a sound has obvious importance to prey animals as well—the crunching sound of brush under a leopard’s foot has fixed its position for many a wary baboon.
What properties of sound enable its source to be located? Actually, part of the answer is remarkably sim-ple: Sounds can be localized by how loud they are, that is, by their intensity. A simple rule might be that sound seems louder when the receptor is closer to the sound.
If only one ear is involved in locating the sound source, however, the rule may not hold (Camhi 1984). Let’s say that the left ear hears a soft sound; was the sound soft because it was produced by a weak source on the left side or by a strong source on the right side? To eliminate such confusion, both ears must be used in the sound local-ization process—this is called binaural comparison.
Some animals use binaural comparison of sound inten-sity to locate the source of sound.
Timing is also important in locating the source of a sound. Two differences in timing could be of poten-tial use, and both rely on binaural comparison. The first occurs at the onset of sound—sound begins and ends sooner in the ear that is closest to the source. The second difference in timing occurs during an ongoing sound. During a continuing sound, there are differ-ences in the phase (the point in the wave of compres-sion or rarefaction) of the sound wave reaching each ear. The extent of the phase difference will depend both on the wavelength of the sound and on the dis-tance between the ears. When the wavelength of the sound is twice the width of the head, the peak of a sound wave arrives at one ear and the trough arrives at the other. Under these conditions, the sound is eas-ily localized. In contrast, when the wavelength of the sound equals the head width, the phase of the sound wave is the same in each ear, and the sound is difficult to localize (Figure 6.9).
Wavelength = two times head width
Wavelength = head width
Wavelength = less than two times head width Most useful for
phase information
No phase difference
Confusion
FIGURE6.9 Binaural comparison of phase. When the sound is prolonged, differences in the phase of the sound wave at each ear may indicate the direction of the source. The usefulness of this cue depends on the wavelength and the distance between the ears.
PREDATORS AND PREY:
THE NEUROETHOLOGY
OF LIFE-AND-DEATH STRUGGLES Now let’s consider how nervous systems gather and process information about the source of sounds to pro-duce adaptive behaviors—escape behavior by prey and prey localization by a predator. We will first consider how sound information is processed by the relatively simple nervous system of a night-flying (noctuid) moth, allowing it to escape from an echolocating bat. Then we will consider how a barn owl obtains and processes sound information to locate its prey.
Escape Responses of Noctuid Moths
Noctuid moths are a favorite prey of certain bats. Indeed, moths typically make up more than half of a bat’s diet.
The bats capture their prey on the wing, locating these flying insects by echolocation—that is, by emitting high-frequency sounds that bounce back to the bat from any structure in the environment. Here we will focus on how moths escape predation.
Kenneth Roeder (1967) has provided a fascinating account of how the relatively simple auditory apparatus of the moth is used to detect an approaching bat and how the moth then takes evasive action. When the bat’s ultra-sonic echolocation pulses are soft, indicating that the bat is still at a distance, the moth turns and flies directly away. However, loud ultrasonic pulses mean that the bat is very close, and emergency actions are needed—erratic, unpredictable looping and wingfolding to produce a free fall. Moths that hear a bat’s approach and take evasive action are about 40% less likely to be eaten.
Roeder found that these moths have two ears, one on either side of the thorax (the insect’s midsection), and that each ear has only two auditory receptor cells (Roeder and Treat 1957). The receptors are tuned to the frequencies of the echolocation calls of species of bats living in their vicinity, which is generally between 20 and 50 kHz. One receptor, called the A1 cell, is about ten times more sensitive than the other cell, the A2 cell. The A1 cell begins to respond when the sound is soft, indi-cating that the bat is still at a distance. The sensitivity of this cell is important because it will determine how much time the moth will have to take appropriate evasive action. The A2 cell responds only to loud sounds (Pérez and Coro 1984; Roeder and Payne 1966), as would come from a nearby bat.
The moth responds to bat sounds long before the bat can detect the moth (Roeder and Payne 1966). North American moths can detect a hunting big brown bat (Eptescicus fuscus) from a distance of nearly 100 ft, whereas the bat must be within about 15 ft to detect a moth-size target (Fenton 1992). The A1 cell, then, warns the moth that there is a hunting bat in the vicinity, in much the
same way that your car’s radar detector alerts you of a police radar trap.
How does the moth’s nervous system analyze the available information and direct effective evasive maneuvers? The sensitive A1 cell responds to the sounds of a distant bat, and its input reveals the direc-tion and distance of the bat (Figure 6.10). If the bat, for example, is on the left side, the left A1 cell is exposed to louder sounds because the A1 cell on the right is somewhat shielded by the moth’s body. Therefore, the left receptor fires sooner and more frequently upon receiving each sound of the bat. When the bat is directly behind or in front of the moth, both neurons will fire simultaneously. A slight turn of the moth’s body will then result in differences in the right and left receptors, which will reveal whether the bat is approaching from the front or rear. What about its altitude? If the bat is above the moth, the bat’s sounds are louder during the upward beat of the moth’s wings when the moth’s ears are uncovered than when the moth’s wings are down, covering the ears and muffling the bat’s cries. However, if the bat is beneath the moth, the bat’s echolocation cries will reach the moth’s ears unimpeded regardless of the position of the moth’s wings. Therefore, the moth’s wingbeats will have no effect on the pattern of neural firing. The moth, then, is able to decode the incoming data, so that it detects both the presence and precise location of the bat.
How is this information processed to produce an appropriate escape pattern? If the bat is passing some distance away, the A1 cell begins to fire. Its firing rate will increase as the bat gets closer and its cries become louder. Up to a certain firing rate of the A1 cell, the dis-tance between predator and prey is too great for the bat to detect the moth. Therefore, the most adaptive response of the moth would be to turn and fly directly away, thus decreasing the likelihood of detection by increasing the intervening distance and by exposing less surface area to the bat. This escape pattern results when the moth turns its body until the A1 firing from each ear is equalized. When the bat changes direction, so does the moth (Roeder and Treat 1961).
Bats fly faster than moths, though, and if the bat gets too close, then the moth’s evasive maneuver switches to an erratic flight pattern. The moth’s wings begin to beat in either peculiar, irregular patterns or not at all. The insect itself probably has no way of knowing where it is going as it begins a series of loops, rolls, and dives. But it is also very difficult for the bat to pilot a course to intercept the moth. If the moth crashes into the ground, so much the better. It is safe here because the earth will mask its echoes.
How does the moth determine whether the bat is gaining on it? One clue is that the sound of an approaching bat grows louder. Recall that the A2 cell is less sensitive than the A1 cell and doesn’t begin to fire
until the bat is close by. Based on these differences in threshold, Roeder suggested that the A1 cell functions as an “early warning” cell and the A2 cell as an “emer-gency” neuron that switches the moth’s evasive response to an erratic flight pattern. As reasonable as the hypoth-esis seems, it is not consistent with the data. One would predict, for instance, that if the activity of the A2 cell was the switch that changes the evasive response from flying directly away to erratic flight, then a moth with only one type of A cell would not switch to erratic flight
when the intensity of the bat’s call increased.
Notodontid moths have a single type of A cell, but they display both types of evasive behavior (Surlykke 1984).
Thus in noctuid moths, which have two auditory cells, the A2 cell does begin firing when the bat is nearby, but this activity may not be responsible for the change to erratic flight.
Another clue to the bat’s proximity is provided by the type of echolocation sounds the bat produces because these change during the hunt. While the bat is
a b c
Sound pulses
Sound pulses
Sound stimulus A1 cell firing
A1 cell firing
A1 cell firing A1 cell firing
A1 cell firing
Wings up Wings down
FIGURE6.10 The relationship of sound pulses from a hunting bat and an auditory neural firing in the hunted moth. (a) When a hunting bat, emitting its high-pitched sounds, approaches a noctuid moth from the side, the receptors on that side fire slightly sooner and more rapidly than those on the shielded side. (b) When the bat is behind the moth, the moth’s receptors on both sides fire with a simi-lar rapid pattern. (c) When the bat is above the moth, the moth’s auditory receptors fire when its wings are up but not when its wings cover the receptors on the down stroke. (Redrawn from Alcock 2001.)
searching for prey, its pulses are relatively long (about 10 ms) and are repeated slowly (about 10 per second).
When prey has been detected, the bat switches to the approach phase of the hunt. The sound pulses get shorter (about 5 ms) and are repeated more rapidly (about 20 per second). In the final approach, which begins when the bat is within a meter of its prey, the bat begins a feeding buzz, consisting of short pulses (0.5 to 2 ms) repeated rapidly (100 to 200 per second) (Boyan and Miller 1991).
The response of the A1 cell can follow the bat’s call rates at all phases of the hunt up to about 150 ms before the bat would capture the moth (Fullard et al. 2003).
Since the call rate changes as the bat gets closer to its prey, the output of the A1 cell provides information about the distance of the bat. The A1 cell sends this information directly to two interneurons, called 501 and 504. These interneurons respond differently to the same input from A1. The differences in interneuron responses somehow encode information about the distance of the bat and direct the appropriate escape response (Boyan and Fullard 1986; Boyan and Miller 1991).
Prey Localization by Barn Owls
Silently and suddenly, a barn owl (Tyto alba) sweeps from the sky to strike its prey with astonishing accuracy (Figure 6.11). How does it find its prey? Although in nature the barn owl’s keen night vision is important in locating prey, the sounds of a scurrying mouse are sufficient for the owl to strike with deadly precision.
Laboratory tests have revealed that birds such as the barn owl are able to locate the source of sounds within 1° or 2° in both the horizontal and vertical planes (1° is approximately the width of your little finger held at arm’s length). Because of its astounding ability to detect and
locate the source of sound, this nocturnal predator can pinpoint its prey by the rustlings the prey makes, and it can precisely determine not only the prey’s location along the ground but also its own angle of elevation above the prey.
How do we know that the hunting owl uses the prey’s sound? For one thing, we know that barn owls can catch a mouse in a completely darkened room (Payne 1962). In experiments, a barn owl was able to capture a skittering leaf pulled along the floor by a string in a dark room (indicating that sight and smell are not involved), and if unable to see, it will leap into the middle of an expensive loudspeaker from which mouse sounds emanate.
To locate its prey by using sound cues, the barn owl must place the source of the sound on a horizontal plane from left to right (i.e., its azimuth), as well as on a ver-tical plane (i.e., its elevation). We now know that a barn owl uses different cues for locating sound cues in hori-zontal and vertical planes.
The owl uses time differences in the arrival of sound in each ear to place it on a horizontal plane and differences in intensity between the two ears to deter-mine the elevation of the sound source (reviewed in Konishi 2003). Masakazu (Mark) Konishi (1993a, b) learned this by playing sound in a barn owl’s ear through small earphones. An owl turns its entire head to face the direction from which it perceives the sound source, because its eyes are fixed in their sockets. When the sound in one ear preceded that in the other, the owl turned its head in the direction of the leading ear. The longer the time difference, the further the owl turned its head.
The intensity differences in the two ears vary with the elevation of the sound source largely because of the arrangement of the ear canals and facial feathers (von Campenhausen and Wagner 2006). The two ear canals that channel the sound toward the inner ears are, oddly enough, situated asymmetrically, with the right one higher than the left. Because of this difference in ear placement, each ear responds differently to a sound at a given elevation. This helps the owl determine its own elevation above the sound source, information critical to an aerial predator. Also, the face of the barn owl is composed of rows of densely packed feathers, called the facial ruff, that act as a focusing apparatus for sound (Figure 6.12). Troughs in the facial ruff, like a hand cupped behind the ear, both amplify the sound and make the ear more sensitive to sound from certain directions.
The facial ruff assists the owl in localizing sounds by creating differences in intensity of the sound in both ears. Loudness is a cue to localizing the sound in both the horizontal and the vertical dimensions. Sound is gen-erally louder in the ear closer to the source. Because of the structure of the facial ruff, the left ear collects FIGURE6.11 A hunting barn owl. A barn owl can locate
its prey by using sound cues alone.
low-frequency sounds primarily from the left side, and the right ear collects low-frequency sounds from the right side. A comparison of the intensity of low-fre-quency sounds in each ear helps the owl determine from which side of the head the sound originates. However, the facial ruff channels high-frequency sound to each ear differently, depending on the elevation of the sound source. As a result, the right ear is more sensitive to high-frequency sounds that originate above the head, and the left ear is more sensitive to high-frequency sounds from below the head. The owl compares the loudness of high-frequency sounds in each ear to determine its position above or below the sound source. As a sound source moves upward from below the bird to a position above the owl’s head, the high-frequency sounds would first be loudest in the left ear and then gradually become louder in the right ear (Knudsen 1981).
Information on the timing and loudness of sounds in each ear is then sent to the owl’s central nervous system over the auditory nerve in a pattern of nerve impulses.
The information is first sent to the cochlear nuclei. Each side of the brain (cerebral hemisphere) has two cochlear nuclei: the magnocellular nucleus and the angular nucleus. Every axon in the auditory nerve sends a branch
to both of these nuclei. Whereas the branch of the audi-tory nerve that goes to the magnocellular nuclei conveys timing information, the branch to the angular nuclei transmits intensity information. Thus, the timing data that place the sound on a horizontal plane are processed separately from the intensity data that place the sound on a vertical plane. These different features of sound are processed in parallel along nearly independent pathways to higher processing stations, where a map of auditory space is eventually formed (Konishi 1993b).
The map of auditory space is formed in the exter-nal nucleus of the inferior colliculus of the midbrain.
Within the inferior colliculus are certain neurons that respond selectively to specific degrees of binaural dif-ferences in sound (Figure 6.13). For example, one neu-ron may respond maximally to differences that correspond to a sound originating 30° to the right of the owl. The sound would arrive a certain amount sooner and be a certain degree louder in the right ear than in
FIGURE6.12 The barn owl, a night hunter, has a facial disc of densely packed feathers that may gather sounds and aid in detecting their source.
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FIGURE6.13 Auditory neurons in the midbrain area (the inferior colliculus) of a barn owl. The top figure shows a hemisphere of space in front of the owl’s head. Neurons in the inferior colliculus respond to sounds that origi-nate at different points. The numbered rectangles indicate 14 areas to which specific inferior colliculus neurons are tuned. The lower figure indicates the manner in which the auditory space of the owl is represented in the inferior colliculus. A horizontal section of the inferior colliculus is shown with bars, indicating the position of specific neurons. The point in space to which that neuron responds is indicated.
Notice that the neurons in the inferior colliculus are spatially organized. (From Knudsen and Konishi 1978.)