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PubMed2001

Corticofugal modulation of duration-tuned neurons in the midbrain auditory nucleus in bats.

Animal sounds, as well as human speech sounds, are characterized by multiple parameters such as frequency, intensity, duration, etc. The central auditory system produces neurons tuned to particular durations and frequencies of sounds emitted by a species. In bats, "duration-tuned" neurons are mostly sensitive to short durations and high frequencies of sounds used for echolocation. They are scattered in the frequency maps of the inferior colliculus and auditory cortex. We found that electric stimulation of cortical duration-tuned neurons modulates collicular duration-tuned neurons in both duration and frequency tuning only when collicular and cortical neurons paired for studies are within +/-4 ms in best duration and within +/-6 kHz in best frequency. There are four types of modulations: sharpening or broadening of duration tuning, and lengthening or shortening of best duration. Sharpening is observed in "matched" collicular neurons whose best durations are the same as those of stimulated cortical neurons, and it is accompanied by augmentation of the auditory responses at their best durations. The other three types of modulations are observed in "unmatched" collicular neurons whose best durations are different from those of stimulated cortical neurons. Lengthening or shortening of best duration is linearly related to the amount of the difference in best duration between collicular and cortical neurons. Corticofugal modulation is specific and systematic according to relationships in both duration and frequency between stimulated cortical and recorded collicular neurons.

Animals↗
PubMed1995

Basilar membrane resonance in the cochlea of the mustached bat.

The mustached bat (Pteronotus parnellii) detects the wing beats of prey insects by resolving small frequency modulations in the return echoes to the constant frequency component of its echolocation call at about 61 kHz. The fine frequency discrimination required for this task is due largely to the mechanical properties of the cochlea, as indicated indirectly by the presence of large otoacoustic emissions at 61 kHz. A laser diode interferometer was used to measure basilar membrane displacements in the basal turn of the cochlea at a location that is 4-6 mm basal to the 61-kHz place on the basilar membrane. The region of the basilar membrane from which the measurements were made was tuned not only to those characteristic of this location (88-98 kHz) but also very sharply tuned to 61 kHz. The 61-kHz tuning was labile and could be modeled as a simple resonance. The resonance is not restricted to the 61-kHz place but involves more basal regions. We also provide direct evidence to show that otoacoustic emissions from the ear propagate along the basilar membrane.

Acoustic Stimulation↗
PubMed1998

Echo-delay resolution in sonar images of the big brown bat, Eptesicus fuscus.

Echolocating big brown bats (Eptesicus fuscus) broadcast ultrasonic frequency-modulated (FM) biosonar sounds (20-100 kHz frequencies; 10-50 microseconds periods) and perceive target range from echo delay. Knowing the acuity for delay resolution is essential to understand how bats process echoes because they perceive target shape and texture from the delay separation of multiple reflections. Bats can separately perceive the delays of two concurrent electronically generated echoes arriving as little as 2 microseconds apart, thus resolving reflecting points as close together as 0.3 mm in range (two-point threshold). This two-point resolution is roughly five times smaller than the shortest periods in the bat's sounds. Because the bat's broadcasts are 2,000-4,500 microseconds long, the echoes themselves overlap and interfere with each other, to merge together into a single sound whose spectrum is shaped by their mutual interference depending on the size of the time separation. To separately perceive the delays of overlapping echoes, the bat has to recover information about their very small delay separation that was transferred into the spectrum when the two echoes interfered with each other, thus explicitly reconstructing the range profile of targets from the echo spectrum. However, the bat's 2-microseconds resolution limit is so short that the available spectral cues are extremely limited. Resolution of delay seems overly sharp just for interception of flying insects, which suggests that the bat's biosonar images are of higher quality to suit a wider variety of orientation tasks, and that biosonar echo processing is correspondingly more sophisticated than has been suspected.

Animals↗
PubMed2000

On cortical coding of vocal communication sounds in primates.

Understanding how the brain processes vocal communication sounds is one of the most challenging problems in neuroscience. Our understanding of how the cortex accomplishes this unique task should greatly facilitate our understanding of cortical mechanisms in general. Perception of species-specific communication sounds is an important aspect of the auditory behavior of many animal species and is crucial for their social interactions, reproductive success, and survival. The principles of neural representations of these behaviorally important sounds in the cerebral cortex have direct implications for the neural mechanisms underlying human speech perception. Our progress in this area has been relatively slow, compared with our understanding of other auditory functions such as echolocation and sound localization. This article discusses previous and current studies in this field, with emphasis on nonhuman primates, and proposes a conceptual platform to further our exploration of this frontier. It is argued that the prerequisite condition for understanding cortical mechanisms underlying communication sound perception and production is an appropriate animal model. Three issues are central to this work: (i) neural encoding of statistical structure of communication sounds, (ii) the role of behavioral relevance in shaping cortical representations, and (iii) sensory-motor interactions between vocal production and perception systems.

Animal Communication↗
PubMed1982

The causes of whale strandings.

Strandings of cetaceans (whales and dolphins) is probably the result of a sequence of events rather than a simple cause-and-effect relationship. Strandings of solitary animals are more common than massed and generally thought to be due to severe disease. Mass strandings (three to several hundred individuals) are less common, but very spectacular. Mass strandings are considered to be due to a complex of factors in which behavioural factors are probably important, severe disease making an unimportant, or negligible contribution. There may be interaction of physical conditions (weather, tides, currents, coastline) and biological conditions (predators, feeding, disturbance of echolocation and disease) which result in stranding. One postulated reason for stranding is that it is dependent on instinctive behaviour, deeply located in subcortical areas of the brain, which provokes cetaceans to seek refuge ashore when under stress.

Journal Article↗
PubMed1962

The sarcoplasmic reticulum of the bat cricothroid muscle.

The bat cricothyroid muscle is believed to participate in the production of the short bursts of frequency modulated ultrasound which these animals use as an echolocation device. The evidence seems to indicate that this muscle must be extremely fast acting. It possesses a very well developed sarcoplasmic reticulum, consisting of intercommunicating longitudinal and transverse tubular elements. The transverse elements, situated at the level of the junction between the A and the I bands, are tripartite complexes of tubules called triads, and these are sometimes replaced by more complex structures, the pentads. The intermediate element of the triad appears as a slender continuous tubule, which can be shown to come into close contact with the sarcolemma and also to share with it certain common staining properties. The longitudinal components of the reticulum consist of very numerous tubules which link successive triads to each other and anastomose to form multiple layers of close-meshed reticula in the interfibrillar sarcoplasm. Both the longitudinal and the transverse elements of the sarcoplasmic reticulum form a continuous network across the muscle fiber. It is suggested that the extraordinary development of the sarcoplasmic reticulum in the bat cricothyroid is related to the unusual physiological properties of this muscle.

Animals↗
PubMed1994

Phylogeny of all major groups of cetaceans based on DNA sequences from three mitochondrial genes.

Traditionally, living cetaceans (order Cetacea) are classified into two highly distinct suborders: the echolocating toothed whales, Odontoceti, and the filter-feeding baleen whales, Mysticeti. A molecular phylogeny based on 1,352 base pairs of two mitochondrial ribosomal gene segments and the mitochondrial cytochrome b gene for all major groups of cetaceans contradicts this long-accepted taxonomic subdivision. One group of toothed whales, the sperm whales, is more closely related to the morphologically highly divergent baleen whales than to other odontocetes. This finding suggests that the suborder Odontoceti constitutes an unnatural grouping and challenges the conventional scenario of a long, independent evolutionary history of odontocetes and mysticetes. The superfamily Delphinoidea (dolphins, porpoises, and white whales) appears to be monophyletic; the Amazon River dolphin, Inia geoffrensis, is its sister species. This river dolphin is genetically more divergent from the morphologically similar marine dolphins than the sperm whales are from the morphologically dissimilar baleen whales. The phylogenetic relationships among the three families of Delphinoidea remain uncertain, and we suggest that the two cladogenetic events that generated these three clades occurred within a very short period of time. Among the baleen whales, the bowhead is basal, and the gray whale is the sister species to the rorquals (family Balaenopteridae). The phylogenetic position of beaked whales (Ziphioidea) remains weakly supported by molecular data. Based on molecular clock assumptions, the mitochondrial-DNA data suggest a more recent origin of baleen whales (approximately 25 mya) than has been previously assumed (> 40 mya). This revised phylogeny has important implications for the rate and mode of evolution of morphological and physiological innovations in cetaceans.

Animals↗
PubMed1996

Facilitative responses to species-specific calls in cortical FM-FM neurons of the mustached bat.

FM-FM neurons in the auditory cortex of the mustached bat are highly specialized for echolocation, responding facilitatively to the combination of frequency modulated (FM) components of biosonar pulse and its echo. Here we propose they are also specialized for processing bat communication calls. FM-FM neurons respond facilitatively to natural call syllable pairs, and exhibit inter-syllable interval tuning to the natural range of intervals. Our results support a role for 'combination-sensitive' neurons in communication, and suggest that cortical neurons can possess multiple distinct specialized modes of response.

Animal Communication↗
PubMed2000

Auditory responses from the frontal cortex in the mustached bat, Pteronotus parnellii.

Response properties of neurons in an auditory field in the frontal cortex of the mustached bat, Pteronotus parnellii, have not been studied before. We recorded neural responses to constant frequency (CF) stimuli from the frontal auditory field in awake animals. The majority (75%) of neurons in this area responded well and often exhibited low thresholds to CF stimuli. Most CF-responsive neurons exhibited sharp tuning with values of > 180 for Q10db, a quality factor expressing the sharpness of tuning at 10dB above threshold. Neurons at 13 recording sites exhibited combination sensitivity in that their responses were facilitated by presenting combinations of either CF1/CF2 and/or CF1/CF3 components of the mustached bat's echolocation signal. Unlike the typical on-responses to a 30 ms tone, observed in the mustached bat's auditory cortex and at subcortical levels, many frontal auditory neurons exhibited loosely time locked firing patterns that lasted for > 100 ms.

Animals↗
PubMed2001

Auditory sensitivity of Hawaiian moths (Lepidoptera: Noctuidae) and selective predation by the Hawaiian hoary bat (Chiroptera: Lasiurus cinereus semotus).

The islands of Hawai'i offer a unique opportunity for studying the auditory ecology of moths and bats since this habitat has a single species of bat, the Hawaiian hoary bat (Lasiurus cinereus semotus), which exerts the entire predatory selection pressure on the ears of sympatric moths. I compared the moth wings discarded by foraging bats with the number of surviving moths on the island of Kaua'i and concluded that the endemic noctuid Haliophyle euclidias is more heavily preyed upon than similar-sized endemic (e.g. Agrotis diplosticta) and adventive (Agrotis ipsilon and Pseudaletia unipuncta) species. Electrophysiological examinations indicated that, compared with species less preyed upon, H. euclidias has lower auditory sensitivities to the bat's social and echolocation calls, which will result in shorter detection distances of the bat. The poor ears of H. euclidias suggest that this moth coevolved with the bat using non-auditory defences that resulted in auditory degeneration. This moth now suffers higher predation because it is drawn away from its normal habitat by the man-made lights that are exploited by the bat.

Acoustic Stimulation↗
PubMed2005

Adaptation of brain regions to habitat complexity: a comparative analysis in bats (Chiroptera).

Vertebrate brains are organized in modules which process information from sensory inputs selectively. Therefore they are probably under different evolutionary pressures. We investigated the impact of environmental influences on specific brain centres in bats. We showed in a phylogenetically independent contrast analysis that the wing area of a species corrected for body size correlated with estimates of habitat complexity. We subsequently compared wing area, as an indirect measure of habitat complexity, with the size of regions associated with hearing, olfaction and spatial memory, while controlling for phylogeny and body mass. The inferior colliculi, the largest sub-cortical auditory centre, showed a strong positive correlation with wing area in echolocating bats. The size of the main olfactory bulb did not increase with wing area, suggesting that the need for olfaction may not increase during the localization of food and orientation in denser habitat. As expected, a larger wing area was linked to a larger hippocampus in all bats. Our results suggest that morphological adaptations related to flight and neuronal capabilities as reflected by the sizes of brain regions coevolved under similar ecological pressures. Thus, habitat complexity presumably influenced and shaped sensory abilities in this mammalian order independently of each other.

Adaptation, Physiological↗
PubMed2006

A bizarre new toothed mysticete (Cetacea) from Australia and the early evolution of baleen whales.

Extant baleen whales (Cetacea, Mysticeti) are all large filter-feeding marine mammals that lack teeth as adults, instead possessing baleen, and feed on small marine animals in bulk. The early evolution of these superlative mammals, and their unique feeding method, has hitherto remained enigmatic. Here, I report a new toothed mysticete from the Late Oligocene of Australia that is more archaic than any previously described. Unlike all other mysticetes, this new whale was small, had enormous eyes and lacked derived adaptations for bulk filter-feeding. Several morphological features suggest that this mysticete was a macrophagous predator, being convergent on some Mesozoic marine reptiles and the extant leopard seal (Hydrurga leptonyx). It thus refutes the notions that all stem mysticetes were filter-feeders, and that the origins and initial radiation of mysticetes was linked to the evolution of filter-feeding. Mysticetes evidently radiated into a variety of disparate forms and feeding ecologies before the evolution of baleen or filter-feeding. The phylogenetic context of the new whale indicates that basal mysticetes were macrophagous predators that did not employ filter-feeding or echolocation, and that the evolution of characters associated with bulk filter-feeding was gradual.

Animals↗
PubMed1998

Base-compositional biases and the bat problem. III. The questions of microchiropteran monophyly.

Using single-copy DNA hybridization, we carried out a whole genome study of 16 bats (from ten families) and five outgroups (two primates and one each dermopteran, scandentian, and marsupial). Three of the bat species represented as many families of Rhinolophoidea, and these always associated with the two representatives of Pteropodidae. All other microchiropterans, however, formed a monophyletic unit displaying interrelationships largely in accord with current opinion. Thus noctilionoids comprised one clade, while vespertilionids, emballonurids, and molossids comprised three others, successively more closely related in that sequence. The unexpected position of rhinolophoids may be due either to the high AT bias they share with pteropodids, or it may be phylogenetically authentic. Reanalysis of the data with varying combinations of the five outgroups does not indicate a rooting problem, and the inclusion of many bat lineages divided at varying levels similarly discounts long branch attraction as an explanation for the pteropodid-rhinolophoid association. If rhinolophoids are indeed specially related to pteropodids, many synapomorphies of Microchiroptera are called into question, not least the unitary evolution of echolocation (although this feature may simply have been lost in pteropodids). Further, a rhinolophoid-pteropodid relationship--if true--has serious implications for the classification of bats. Finally, among the outgroups, an apparent sister-group relation of Dermoptera and Primates suggests that flying lemurs do not represent the ancestors of some or all bats; yet, insofar as gliding of the type implemented in dermopterans is an appropriate model for the evolution of powered mammalian flying, the position of Cynocephalus in our tree indirectly strengthens the argument that true flight could have evolved more than once among bats.

Animals↗
PubMed2000

Hair cell heterogeneity and ultrasonic hearing: recent advances in understanding fish hearing.

The past decade has seen a wealth of new data on the auditory capabilities and mechanisms of fishes. We now have a significantly better appreciation of the structure and function of the auditory system in fishes with regard to their peripheral and central anatomy, physiology, behaviour, sound source localization and hearing capabilities. This paper deals with two of the newest of these findings, hair cell heterogeneity and the detection of ultrasound. As a result of this recent work, we now know that fishes have several different types of sensory hair cells in both the ear and lateral line and there is a growing body of evidence to suggest that these hair cell types arose very early in the evolution of the octavolateralis system. There is also some evidence to suggest that the differences in the hair cell types have functional implications for the way the ear and lateral line of fishes detect and process stimuli. Behavioural studies have shown that, whereas most fishes can only detect sound to 1-3 kHz, several species of the genus Alosa (Clupeiformes, i.e. herrings and their relatives) can detect sounds up to 180 kHz (or even higher). It is suggested that this capability evolved so that these fishes can detect one of their major predators, echolocating dolphins. The mechanism for ultrasound detection remains obscure, though it is hypothesized that the highly derived utricle of the inner ear in these species is involved.

Animal Communication↗
PubMed1991

Facilitation and Delay Sensitivity of Auditory Cortex Neurons in CF - FM Bats, Rhinolophus rouxi and Pteronotus p.parnellii.

Responses of auditory neurons to complex stimuli were recorded in the dorsal belt region of the auditory cortex of two taxonomically unrelated bat species, Rhinolophus rouxi and Pteronotus parnellii parnellii, both showing Doppler shift compensation behaviour. As in P.p.parnellii (Suga et al., J. Neurophysiol., 49, 1573 - 1626, 1983), cortical neurons of R.rouxi show facilitated responses to pairs of pure tones or frequency modulations. Best frequencies for the two components lie near the first and second harmonic of the echolocation call but are in most cases not harmonically related. Neurons facilitated by pairs of pure tones show little dependence on the delay between the stimuli, whereas pairs of frequency modulations evoke best facilitated responses at distinct best delays between 1 and 10 ms. Facilitated neurons are found in distinct portions of the dorsal cortical belt region, with a segregation of facilitated neurons responding to pure tones and to frequency modulations. Non-facilitated neurons are found throughout the field. Neurons are topographically aligned with increasing best delays along a rostrocaudal axis. The best delays between 2 and 4 ms are largely overrepresented numerically, and occupy approximately 56% of the cortical area containing facilitated neurons. A functional interpretation of the large overrepresentation of best delays approximately 3 ms is proposed. Facilitated neurons are located almost entirely within layer V of the dorsal field.

Journal Article↗
PubMed1991

Auditory Pontine Grey: Connections and Response Properties in the Horseshoe Bat.

This study investigates the role of the pontine grey as a link between the auditory system and the cerebellum in the bat, Rhinolophus rouxi. We recorded response properties of single neurons in the pontine grey and, in the same preparation, injected wheat germ agglutinin - horseradish peroxidase (WGA - HRP) in areas responsive to sound. Thus the functional evidence was correlated with retrograde and anterograde transport. The main results are: (i) all auditory neurons in the pontine grey are tuned within one of two harmonically related frequency ranges of the echolocation call. The upper range corresponds to the constant frequency and frequency modulated components of the second harmonic, but the lower range corresponds only to the frequency modulated component of the first harmonic. There is no systematic tonotopic organization; (ii) discharge patterns are extremely variable, latencies cover a wide range, and about half of the neurons are binaurally responsive with excitation from both ears; (iii) most pontine auditory neurons respond preferentially to frequency modulated stimuli; (iv) there is massive input to the pontine grey from the central nucleus of the inferior colliculus; (v) cortical input to the pontine grey does not originate in tonotopically organized auditory cortex. The input is from a dorsal belt area that is specialized for processing combinations of sounds with specific frequency ratios and delays; (vi) projections from the auditory region of the pontine grey are widespread within the cerebellar cortex. The data suggest that the pontine grey transmits to the cerebellum information contained in specific components of the bat's biosonar signal.

Journal Article↗
PubMed1997

Significance of the paralemniscal tegmental area for audio-motor control in the moustached bat, Pteronotus p. parnellii: the afferent off efferent connections of the paralemniscal area.

The paralemniscal tegmental area has been determined in the brain of the New World moustached bat, Pteronotus p. parnellii, by electrical microstimulation eliciting echolocation calls and pinna movements. It is located in the dorsal tegmentum rostral and medial to the dorsal nucleus of the lateral lemniscus and is characterized by medium sized and large neurons. Tracer injections (WGA-HRP) showed that the most intense input to the paralemniscal tegmental area originates in the intermediate and deep layers of the homolateral superior colliculus. The strong projections from the ipsi- and contralateral nucleus praepositus hypoglossus most probably contributes vestibular information. Further inputs in descending order of intensity are from the substantia nigra, the contralateral paralemniscal tegmental area, the putamen, the ventral reticular formation in its lateral portions, the medial cerebellar nucleus and the dorsal reticular formation. Efferent projections of the paralemniscal tegmental area reach the putamen bilaterally, the nucleus accumbens and other parts of the basal ganglia, the pretectal area, the substantia nigra, the intermediate and deep layers of the superior colliculus bilaterally and the tegmental area ventral to it. Connections to the dorsal part of the periaqueductal grey, the cuneiform nucleus and the parabrachial region are important in the context of vocal control, whereas projections to the medial portion of the contralateral facial nucleus may interfere with the control of pinna movement. The findings suggest that the paralemniscal tegmental area is involved in audio-motor control of vocalization and pinna movements in bats; connectional and functional similarities and disparities to tegmental regions described in other mammals are discussed.

Afferent Pathways↗
PubMed2006

Effects of selective logging on bat communities in the southeastern Amazon.

Although extensive areas of tropical forest are selectively logged each year, the responses of bat communities to this form of disturbance have rarely been examined. Our objectives were to (1) compare bat abundance, species composition, and feeding guild structure between unlogged and low-intensity selectively logged (1-4 logged stems/ha) sampling grids in the southeastern Amazon and (2) examine correlations between logging-induced changes in bat communities and forest structure. We captured bats in understory and canopy mist nets set in five 1-ha study grids in both logged and unlogged forest. We captured 996 individuals, representing 5 families, 32 genera, and 49 species. Abundances of nectarivorous and frugivorous taxa (Glossophaginae, Lonchophyllinae, Stenodermatinae, and Carolliinae) were higher at logged sites, where canopy openness and understory foliage density were greatest. In contrast, insectivorous and omnivorous species (Emballonuridae, Mormoopidae, Phyllostominae, and Vespertilionidae) were more abundant in unlogged sites, where canopy foliage density and variability in the understory stratum were greatest. Multivariate analyses indicated that understory bat species composition differed strongly between logged and unlogged sites but provided little evidence of logging effects for the canopy fauna. Different responses among feeding guilds and taxonomic groups appeared to be related to foraging and echolocation strategies and to changes in canopy cover and understory foliage densities. Our results suggest that even low-intensity logging modifies habitat structure, leading to changes in bat species composition.

Animals↗