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20 Evolution of Sound Localization in Mammals

S J Sterbing-DAngelo, Vanderbilt University, Nashville, TN, USA
2007 Elsevier Inc. All rights reserved.

3.20.1 Introduction 3.20.2 Cues for Sound Localization 3.20.3 Brain Structures for Sound Localization Brainstem Midbrain Isocortex 3.20.4 Behavioral Measures of Sound Localization

253 253 254 254 255 256 257

binaural contralateral exteroceptive fossorial inferior colliculus interaural isocortex lemniscal pathway marsupials With both ears. On the opposite side. Perception of external objects. Adapted to digging and underground life. Midbrain nucleus of the ascending primary auditory pathway. Between both ears. Top layer of the cerebral hemispheres in mammals ( neocortex). Pathway that involves the lateral lemniscus in the brainstem. Mammals in which the female typically has a pouch (marsupium), in which it rears its young through early infancy. Located in the midbrain. With one ear. Egg-laying mammals. Mammals that rear young through early infancy with a placenta. Birds and reptiles. Taxonomic unit, a grouping of organisms.

mesencephalic monaural monotremes Placentalia sauropsids taxon (plural taxa)

adds unique abilities arising from the development of the external ear and from the development of the isocortex (neocortex). The evolution of sound localization in mammals is not characterized by a straightforward sequence of changes in the underlying brain structures concomitant with an improvement in ability but rather is more related to the ecological niche of each species. Different habitats and different behavioral strategies for survival require different solutions for sound localization. Many species from a variety of taxa have developed a remarkable acuity for localizing sounds, which comes close to or matches human localization acuity. However, while acuity may be similar, for example, across echolocating bats (microchiroptera), homologous brain structures involved in sound localization can be anatomically or functionally different.

3.20.2 Cues for Sound Localization

The cues for sound localization comprise interaural cues, which are based on the information derived from both ears, and monaural cues, which are caused by the filtering of each external ear, the pinna (for overview see Blauert, 1997). The interaural cues are used for lateralization, that is, the left/right discrimination of sound. The monaural cues give additional information on the elevation of a source and allow front/back discrimination. All vertebrates that have bilateral hearing use binaural cues to some extent (e.g., frogs, reptiles, and birds). For low-frequency sounds from the side, the time of arrival of the sound waves differs between the two ears. This is the interaural time difference (ITD). If the sound source direction is located along the mid-line axis, for example, front, rear, or directly above, the ITD would have the value zero, because the sound wave reaches both

3.20.1 Introduction
The ability to localize sound sources in a complex environment is of paramount importance for orientation in a biological habitat, and intraspecies as well as interspecies communication. The accurate localization of an approaching predator or competitor can be a matter of life or death. This topical essay discusses the major features of the evolution of sound localization in mammals in terms of the physical cues for sound localization, the major brain structures involved, and behavioral measures of localization acuity across taxa. Sound localization in mammals builds upon similar systems shared by lower vertebrates that utilize bilateral hearing, and

254 Evolution of Sound Localization in Mammals

ears at the same time. For lateral incidence angles, the sound travels around the head and the body of the animal on various paths to reach the far ear, that is, the ear opposed to the sound event. The physiologically relevant ITD range depends on head size, head geometry, and pinna shape. A common measure to estimate the physiological range of ITDs in a species has been to simply measure the distance between the ear canal openings. However, depending on the angle of incidence and the shape or body position of an animal, sound has to travel on complicated paths around the animal. The ITDs in the fine structure of a sound can be detected up to ,2.5 kHz in many mammalian species. For both low and high frequencies, the ITDs in the envelope of a sound, for example, the onset slope or amplitude modulations, can also be utilized (Joris, 2003). For highfrequency sounds the head shadow attenuates the sounds at the far ear. This interaural cue is called the interaural intensity difference (IID). The IID for low frequencies is relatively small (a few dB), but for high frequencies it can be as large as 2030 dB for certain directions, depending on the head size. In contrast to amphibians, reptiles, and birds, most nonaquatic and nonsubterranean mammals possess a pinna of varying complexity in shape and mobility. The resulting pinna cue is what distinguishes the localization ability of the mammals. The angle of sound incidence upon the ridges and folds of the pinna causes certain frequencies to be amplified while others are attenuated. Therefore, the pinna cues provide information about the location of sound in space. Many mammals can move the pinna. Others, for example some primates, cannot. It is of paramount importance to emphasize that ITD, IID, and the monaural spectrum always vary together in a natural acoustic environment. Because of the influence of the pinna, the magnitudes of the IID and the ITD can vary nonmonotonically with frequency and direction, especially for high frequencies. For natural broadband sounds delivered in an ecologically valid environment, the left and right ear will have a spectral transfer function at each azimuth and elevation, and the differences between the ears lead to an interaural difference spectrum (for review see Blauert, 1997). The implication is that the advanced localization system of mammals can make use of the combined cues to achieve the highest possible acuity in all spatial dimensions. However, many fossorial species, for example the pocket gopher, show little ability to localize sounds, which is explainable by the lack of spatial cues in their subterranean habitat (Heffner and Heffner, 1990).

3.20.3 Brain Structures for Sound Localization

The brain receives acoustic information via only one row of inner hair cells located in the cochlea of the inner ear. Unlike the retina, which is a twodimensional structure, no spatial information is inherent in the pattern of activation of the receptors. Hence, the spatial position of a sound source has to be computed by the auditory structures of the brain. Solving this complex computation has resulted in a variety of evolutionary adaptations. I will restrict the discussion of the role of brain structures for the evolution of sound localization to a couple of nuclei in the superior olivary complex, the auditory midbrain (inferior colliculus), and the auditory cortex, although other brain structures are also involved in sound localization. To describe them all would exceed the scope of this topical essay (see Encephalization: Comparative Studies of Brain Size and Structure Volume in Mammals, The Effects of Domestication on Brain Size, Cetacean Brain Evolution). Brainstem

The superior olivary complex (SOC) is a group of auditory nuclei in the brainstem of amphibians, reptiles, and mammals. One major function of the SOC is to encode the cues that contribute to sound lateralization on the basis of convergent binaural ascending inputs arising from both ventral cochlear nuclei. The SOC consists of several nuclei. Of major interest for sound localization are the lateral superior olivary nucleus (LSO) and the medial superior olivary nucleus (MSO). The LSO is involved in the coding of IIDs (Boudreau and Tsuchitani, 1968) and envelope ITDs (Joris and Yin, 1995). The MSO processes ITDs in the fine structure of predominantly low-frequency sounds (Yin and Chan, 1990). The range of the interaural disparity cues increases with head size. A large head is especially advantageous for the use of fine structure ITDs. Hence, it is not surprising that mammalian species with large heads have a pronounced MSO and often a smaller LSO, while species with small heads have a relatively smaller MSO and a large LSO. However, a large-sized LSO does not necessarily indicate superior IID coding. For example, some hoofed species like the horse, are apparently not able to use IIDs to localize high-frequency tones, although they possess a well-developed LSO (Heffner and Heffner, 1986). The basic neuronal properties of the LSO appear to be similar across taxa (Tollin, 2003, review): most LSO neurons are excited by the ipsilateral ear and inhibited by the contralateral ear. In contrast, MSO neurons are excited by both ears in

Evolution of Sound Localization in Mammals


the cat and many other mammals. Individual MSO neurons are tuned to a certain range of ITDs (Yin and Chan, 1990). There is some weak evidence that the neurons of the mammalian MSO are spatially arranged in a manner that is consistent with a delay line, the anatomical basis of a coincidence detector (cross-correlation) model of ITD processing (Yin and Chan, 1990) as proposed by Jeffress (1948). Although, in the barn owl, the delay line in the nucleus that corresponds to the mammalian MSO (nucleus laminaris, NL) appears to be more clearly developed than in mammals (Kubke et al., 2002; Carr and Konishi, 1988), the function shows strong similarities. Neurons of both the NL and the MSO time-lock to monaural and binaural stimuli, and respond maximally when time-locked spikes from each side arrive simultaneously, that is, when the difference in the spike conduction delays compensates for the ITD (Goldberg and Brown, 1969; Carr and Konishi, 1988; Yin and Chan, 1990). The homology between the mammalian MSO and the nucleus laminaris was accepted for decades but has recently been questioned (Carr and Soares, 2002, review). However, it is clear that the mammalian MSO appears to be a less ideal cross-correlator than the owls NL (Batra and Yin, 2004), and additional mechanisms of ITD processing via inhibitory processes within the MSO have been proposed (Brand et al., 2002). These inhibitory mechanisms could actually improve the cross-correlator, and might therefore be an evolutionary step. Until recently, the fossil finds of early, mesozoic mammaliformes and mammals included only small, shrew to rat-size species, for example, Morganucodon, whose head was only about 20 mm long. The average small size of these fossils suggested that those early mammals were nocturnal insectivores, and possibly specialized to hear predominantly high frequencies like extant small insectivores and many rodents. The finding that some insectivores, for example some bat species, have a predominantly monaural MSO (Covey et al., 1991) prompted the theory that the mammalian MSO was initially a monaural structure which became binaural when the early nocturnal insectivorous mammals explored more ecological niches and evolved into larger species after the decline of the dinosaurs (Grothe, 2000, review). However, other bat species possess a binaural or mixed binaural/monaural MSO (Harnischfeger et al., 1985), or a binaural MSO that resembles the MSO of nonecholocating mammals (Grothe and Park, 1998). This diverse functional organization, and especially monaural characteristic might reflect an adaptation for certain echolocation strategies in the

different bat species rather than a primitive feature. More research in primitive nonecholocating insectivores is needed to evaluate this theory. The first true mammals were probably represented by Hadrocodium, Repenomamus, and Gobiconodon species, which would fill an intermediate position between the reptile-like Morganucodon and the earliest therian (therians marsupial and placental mammals), Triconodon, a species whose cranial endocast morphology places it at the time of origin of the mammalian isocortex (Rowe, 1996). Triconodon was quite large, and was about the size of a Virginia opossum. However, recent fossil finds indicate that some of the early mammalian Repenomamus species were considerably larger, for example Repenomamus giganticus, which had estimated bodyweight of 1214 kg, a skull length of 160 mm, and overall body length of more than 1 m. It has been proposed that R. giganticus was a carnivore (Hu et al., 2005). The apparently larger diversity in body size of those early mammals provokes the question whether some bigger species were sensitive to lower sound frequencies, and used the ITDs provided by their larger heads, and whether they possibly had a binaural MSO. A definite answer to this question cannot be provided by the fossils, because soft tissues are not preserved. In many primitive mammals, like monotremes and some insectivores the middle ear cavities are not bony, but in part covered by cartilage and connective tissue. What these species have in common is that their low-frequency hearing is poor independent of head size (Masterton et al., 1969; Aitkin and Johnstone, 1972; Gates et al., 1974). Hence, the evolution of the MSO and ITD coding in the brainstem remains an open question. Midbrain

The central nucleus of the inferior colliculus (IC) is an obligatory station of the primary ascending auditory pathway. The neuronal sensitivity to ITDs was first described by Rose et al. (1966) for the ICC of the cat, and further examined by Goldberg and Brown (1969) for the beagle. In the mammal IC the processing of combined interaural and spectral cues requires convergence of monaural and binaural inputs and across-frequency integration. The neuroanatomical aspects of this convergence in the IC have been studied using simultaneous tracer injections in different monaural and binaural lower brainstem nuclei (Oliver, 1987; Oliver and Shneiderman, 1991; Oliver et al., 1997; Loftus et al., 2004). Further anatomical evidence for across-frequency interaction within the ICC was provided by

256 Evolution of Sound Localization in Mammals

Malmierca et al., (1995). They found that distant isofrequency layers are interconnected in the ICC of the guinea pig. Some neurophysiological aspects of this convergence have been revealed for the ICC of the rabbit by combining the ITD with monaural amplitude modulation (DAngelo et al., 2003). It became evident that most neurons integrate ITD and monaural information to a varying degree. Chase and Young, (2005) as well as Sterbing et al. (2003) found evidence for the integration of different localization cues in the ICC of the cat and the guinea pig, respectively. Therefore, the mammalian ICC is a potential source of substantial monaural and binaural integration in the lemniscal pathway of a variety of mammals, which exceeds the function of the auditory midbrain in lower vertebrates. Isocortex

The origin of the mammalian isocortex, in which the auditory cortex is located, has been subject of contradicting studies (for review, see Aboitiz et al., 2002). In the past it was regarded as a homologue to a structure named the dorsal ventricular ridge in reptiles, which receives thalamic auditory and visual inputs. However, recent studies suggest that the mammalian isocortex arose from the dorsal pallium, which is predominantly visual and somatosensory in reptiles. This suggestion is supported by molecular and developmental evidence (for a review on the evolution of the isocortex, see Aboitiz et al., 2002). As a result, the mammalian isocortex would be a new evolutionary target for auditory thalamic projections. The development of the isocortex is accompanied by a gradual expansion of the brain, which is evident from fossil skull endocasts of early mammals, for example, Hadrocodium and Morganucodon. While the mesencephalic sensory pathways are the main processors of topographically organized exteroceptive information in sauropsids, and the lemniscal and collicular pathways are largely separated in sauropsids, this is not the case in mammals. In the mammalian isocortex both pathways are integrated, and might therefore implement more ascending information. The enlargement of the isocortex has been associated with the development of a modern middle ear, which makes the transmission of sound more effective. However, while most early mammals with an enlarged isocortex have a fully evolved middle ear, the reverse is not true. Not every mammal with a modern middle ear has an enlarged isocortex. This makes a theory that the enlargement of the isocortex occurred to process sounds inconclusive.

While there is consensus from lesion studies that at least parts of the auditory cortex (AC) are necessary for sound localization, it is unclear whether different fields of the AC contribute differently to or are specialized exclusively for sound localization. Unilateral lesions of the AC in carnivores and monkeys result in deficits of localization of exclusively contralateral sounds (Jenkins and Masterton, 1982; Jenkins and Merzenich, 1984). The only exception from this finding is the human, which might be caused by our hemispheric specialization (Zatorre and Penhune, 2001). If the inactivation is confined to certain fields of the auditory cortex of the cat, either a contralateral deficit or no deficit occurs (Malhotra et al., 2004). A deficit occurs for the tonotopically organized fields A1 (primary auditory cortex), PAF (posterior auditory field), as well as, for the nontonotopic multisensory field AES (anterior ectosylvian sulcus), but no deficit was found following inactivation of the tonotopical field AAF (anterior auditory field), nontonotopic A2 and other multisensory fields. These lesion studies prompted the question whether different fields of the auditory cortex contribute differently to sound localization in different species. As described above, monaural and binaural information converge in the ICC, where the majority of neurons are spatially tuned. One could assume that the actual processing of auditory space is complete at this level, and that the role of AC is to distribute this preprocessed information to higherorder areas (Schnupp et al., 2001; Kowalski et al., 1995). However, the auditory cortex offers new substrates for further processing. The first would be the connection between the cortical hemispheres (corpus callosum) in higher mammals (Placentalia) (for review, see Aboitiz and Montiel, 2003). Since monotremes and marsupials lack the corpus callosum, the placental mammals have the evolutionary advantage of an additional layer for the processing of spatial information. Unfortunately, the possible role of transcallosal projections for sound localization especially under evolutionary aspects is not understood yet. The second new substrate would be additional thalamic inputs that bypass the primary auditory cortex, but target certain secondary areas. In primates, for example, the secondary caudo-medial area (CM), which is known to be in part serially activated by A1 (Rauschecker et al., 1997), receives in contrast to A1 additional lemniscal and extralemniscal projections from other parts of the auditory thalamus than the ventral medial geniculate body (MGv). These derive, for example, from the dorsal and medial part of the MG (for review, see Jones, 2003). These additional inputs might indicate a specialization of this area for the processing of

Evolution of Sound Localization in Mammals


certain sound attributes. Based on anatomical studies on the topography in the connections of the lateral belt and parabelt (Romanski et al., 1999; Hackett et al., 1998a, 1998b, 1999a, 1999b), and preliminary electrophysiological studies, it has been proposed that area CM is specialized to code for sound location (Tian et al., 2001; Recanzone et al., 2000). From these findings, a model for two, separate what and where streams of cortical auditory processing was introduced by Romanski et al. (1999) in analogy to the processing streams in the visual system (Mishkin and Ungerleider, 1982). However, despite the fact that the architecture and connections of the different auditory cortical fields have been well described in the macaque (Hackett et al., 1998a, 1998b, 1999a, 1999b), their functional specialization for sound localization remains largely unknown. Even if many areas were coding for sound location, there might be differences in the processing of spatial information. For the cat, the work of Middlebrooks and co-workers on field PAF suggests that in this area, in contrast to A1, the acoustic space is coded in the form of response latency and patterns of trains of action potentials, rather than the rate of action potentials (Furukawa et al., 2000; Furukawa and Middlebrooks, 2002; Stecker et al., 2003). To summarize, the relative contribution of different fields of the AC has not been studied in enough species to clearly reveal an evolutionary trend of specialization of certain fields/areas for sound localization. However, all mammalian species studied so far (carnivores, rodents, bats, and primates) have in common that the AC can be divided in a core of 23 and a belt of additional areas. This seems to be the basic organization retained from a common ancestor. Because of the remarkable differences in the number of fields, their relative location, their connections, and different physiological properties in different species, it is likely that the complex cortical processing system has developed in a quite independent fashion across mammalian taxa, and is therefore an example for niche evolution.

3.20.4 Behavioral Measures of Sound Localization

The variations of the organization of the auditory pathway involved in sound localization between mammalian species raises the question whether this variation is correlated with sound localization acuity. One might further assume that a bigger head, that is, a larger interaural distance, might improve the performance in localizing sounds. The

acuity of sound localization has been examined behaviorally in a wide variety of mammalian species. Most information is available on the minimum audible azimuth angle (MAAA) which is defined as the minimum angle for which the animal (or a human listener) perceives two separate sound sources instead of only one fused sound source. However, this measure does not represent a sound localization task, for which an animal would have to point to a perceived invisible/ unknown sound source, but a sound source discrimination task. The methods used to assess the MAAA varied, but in most cases some kind of operant conditioning was used. To allow comparison, only studies that used broadband signals in an operant conditioning setup in air (not under water) were included in the following analysis. The head width was plotted against the MAAA for 18 mammalian species (Figure 1). Surprisingly, the minimum audible angle does not clearly depend on the interaural distance of the animal (R 0.39). Very small species, for example, echolocating bats, can have quite small MAAAs despite their specialization for high frequencies, suggesting that ITDs do not play a major role for this sound-source discrimination task in these species. On the other hand, rodents with comparable headsize can have MAAAs ranging from 12 to 27 . For comparative behavioral measures of sound localization acuity Heffner and Heffner (1992) pointed out an important problem: parameters unrelated to the auditory system might affect sound source localization behavior. Mammals that have a visual streak, that is, a horizontally enlarged area of highest visual acuity, might only orient their head up to a position where the acoustic target reached the boundary of the visual streak, while animals with a small visual fovea, for example primates, would have to direct their gaze toward an acoustic target within a much smaller area of vision. The disparity between the localized and physical position of the sound source would naturally be expected to be greater for mammals with a visual streak than for mammals with a small fovea. The actual sound localization acuity on the basis of the physical sound localization cues, however, might very well be comparable, but hard to test in an experimental setup. In summary, it is compelling how many factors affect sound localization. It appears to be difficult if not impossible to correlate certain parameters, like head size, pinna shape, or middle ear volume with localization acuity. The evolution of sound localization in mammals is a multifaceted aspect that is driven by ecological needs independent of taxon and common ancestry.

258 Evolution of Sound Localization in Mammals

Marsupials Rodents Primates Pinnipeds Carnivores Herbivores Echolocating Bats

40 35 30 MAAA (deg) 25 20 15 10

Mu Dm OI Ma Ef Rn Mp Cl Ec

Aj Mexican fruit bat: Heffner et al. (2001) Cc dog: Heffner (1976) Cl chinchilla: Heffner et al. (1994) Dm kangaroo rat: Heffner and Masterton (1980) Dv opossum: Ravizza and Masterton (1972) Ec horse: Heffner and Heffner (1984) Ef big brown bat: Koay et al. (1998) Em elephant: Heffner and Heffner (1982) Fc cat: Casseday and Neff (1975) Hs human: Heffner and Heffner (1984) Ma hamster: Izraeli et al. (2002) Mm macaque: Heffner and Masterton (1978) Mp ferret: Kavanagh and Kelly (1987) Mu gerbil: Heffner and Heffner (1988b) OI grasshopper mouse: Heffner and Heffner (1988a) Pv harbor seal: Holt et al. (2004) Rn wild Norway rat: Heffner and Heffner (1985) Zc Californian sea lion: Holt et al. (2004)

A j Fc Cc 5 Dv 0 0 10

Mm S SIl Pv Hs 20 30 Head width (cm) 40 R = 0.39 50 60 Em

Figure 1 MAAA plotted against head width for 18 mammalian species. Only studies that used broadband signals in an operant conditioning setup in air (not under water) were included.

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Further Reading
Popper, A. N., Fay, R. R., and Webster, D. B. (eds.) 1992. The Evolutionary Biology of Hearing. Springer.