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Duration selective neurons in the inferior colliculus of the rat: topographic distribution and relation of duration sensitivity to other response properties.

Many animals use duration to help them identify the source and meaning of a sound. Duration-sensitive neurons have been found in the auditory midbrain of mammals and amphibians, where their selectivity seems to correspond to the lengths of species-specific vocalizations. In this study, single neurons in the rat inferior colliculus (IC) were tested for sensitivity to sound duration. About one-half (54%) of the units sampled showed some form of duration selectivity. The majority of these (76%) were long-pass neurons that responded to sounds exceeding some duration threshold (range: 5-60 ms). Band-pass neurons, which only responded to a restricted range of durations, made up 13% of duration-sensitive neurons (best durations: 15-120 ms). Other units displayed short-pass (2%) or mixed (9%) response patterns. The majority of duration-sensitive neurons were localized outside the central nucleus of the IC, especially in the dorsal cortex, where more than one-half of the neurons sampled had long-pass selectivity for duration. Band-pass duration tuned neurons were only found outside the central nucleus. Characteristics of duration-sensitive neurons in the rat support the idea that this filtering arises through an interaction of excitatory and inhibitory inputs that converge in the IC. Band-pass neurons typically responded at sound offset, suggesting that their tuning is created through the same mechanisms that have been described in echolocating bats. The finding that the first-spike latencies of all long-pass neurons were longer than the shortest duration to which they responded supports the idea that they receive transient inhibition before, or simultaneously with, a sustained excitatory input. The ranges of selectivity in rat IC neurons are within the range of durations of rat vocalizations. These data suggest that a population of neurons in the rat IC have evolved to transmit information about behaviorally relevant sound durations using mechanisms that are common to all mammals, with an emphasis on long-pass tuning characteristics.

Acoustic Stimulation↗

Neuronal encoding of ultrasonic sound by a fish.

Many species of odontocete cetaceans (toothed whales) use high-frequency clicks (60-170 kHz) to identify objects in their environment, including potential prey. Behavioral studies have shown that American shad, Alosa sapidissima, can detect ultrasonic signals similar to those of odontocetes that are potentially their predators. American shad also show strong escape behavior in response to ultrasonic pulses between 70 and 110 kHz and can determine the location of the sound source at least in the horizontal plane. The present study examines physiological aspects of ultrasound detection by American shad and provides the first insights into the neural encoding of ultrasound signals in any nonmammalian vertebrate. The recordings were obtained by penetration through the cerebellar surface. All but two units responded exclusively to ultrasound. Ultrasound-sensitive units did not phase-couple to any stimulus frequency. Some units resembled the response of constant latency neurons found in the ventral nucleus of the lateral lemniscus of bats. We suggest that ultrasonic and sonic signals are processed along different pathways in Alosa. The ultrasonic pathway in Alosa appears to be a feature detector that is likely to be adapted (e.g., frequency, intensity) to odontocete echolocation signals.

Acoustic Stimulation↗

Response selectivity for species-specific calls in the inferior colliculus of Mexican free-tailed bats is generated by inhibition.

Here we show that inhibition shapes diverse responses to species-specific calls in the inferior colliculus (IC) of Mexican free-tailed bats. We presented 10 calls to each neuron of which 8 were social communication and 2 were echolocation calls. We also measured excitatory response regions: the range of tone burst frequencies that evoked discharges at a fixed intensity. The calls evoked highly selective responses in that IC neurons responded to some calls but not others even though those calls swept through their excitatory response regions. By convolving activity in the response regions with the spectrogram of each call, we evaluated whether responses to tone bursts could predict discharge patterns evoked by species-specific calls. The convolutions often predicted responses to calls that evoked no responses and thus were inaccurate. Blocking inhibition at the IC reduced or eliminated selectivity and greatly improved the predictive accuracy of the convolutions. By comparing the responses evoked by two calls with similar spectra, we show that each call evoked a unique spatiotemporal pattern of activity distributed across and within isofrequency contours and that the disparity in the population response was greatly reduced by blocking inhibition. Thus the inhibition evoked by each call can shape a unique pattern of activity in the IC population and that pattern may be important for both the identification of a particular call and for discriminating it from other calls and other signals.

Acoustic Stimulation↗

Quantitative observations on the nasal epithelia and olfactory innervation in bats. Suggested design mechanisms for the olfactory bulb.

The nasal epithelia of two species of bats were quantified with respect to relative surface areas and olfactory epithelial volumes. In the macrosmatic Aribeus jamaicensis 55.9% of the nasal cavity surface was covered by olfactory epithelium (232.4 mm2), in contrast to only 28.9% in the microsmatic Myotis lucifugus (36.4 mm2). The roles of the various nasal epithelia have been discussed as they may relate to olfaction, respiration and echolocation. In the olfactory bulbs of both species, the estimated concentration of mitral cells approximated at 2,500/mm2 compared to an olfactory nerve concentration of 5/mm2. In Artibeus, calculated total volume of olfactory epithelium was on the order of 16 times greater than in Myotis, and Artibeus' olfactory bulb diameter was twice as great. These findings, together with previously published surface, volume and physiological relationships, suggest a developmental design mechanism for an olfactory bulb in which the number of olfactory receptors increases some 450-fold above an initially established ratio of 2:1 between receptors and mitral cells. Key governing factors could be requisite mechanical rigidity of the cribriform plate of the ethmoid bone and response thresholds of higher brain centers.

Animals↗

Distribution of carboxylic esterases in the telencephalon and diencephalon of a microchiropteran bat (Taphozous melanopogon Temminck).

The contribution deals with the histoenzymological makeup of telencephalon and diencephalon of a microchiropteran bat which is considered to have a primitive type of brain. Three esterases, namely acetylcholinesterase (AChE), butyrylcholinesterase (BChE) and nonspecific esterase (NSE), have been studied. In comparison with other mammalian brains the telencephalon and diencephalon of the bat demonstrate a high concentration of enzyme, especially in the nucleus caudatus and putamen, stria medullaris and the nuclei of the thalamus. AChE concentration is higher in neurons, while BChE is seen in almost all fibrous areas of the telencephalon and diencephalon. NSE activity is prominent in neurons and neuropil of neocortex, thalamus and hypothalamus. All the above data indicate that the brain of echolocating microchiropteran bats is metabolically much more active than that of other mammals. This is specifically true of the auditory system which is considerably specialized in these animals; this is also confirmed by the present histoenzymological study.

Acetylcholinesterase↗

Textbook cricket goes to the field: the ecological scene of the neuroethological play.

Sensory ecology has recently emerged as a new focus in the study of how organisms acquire and respond to information from and about their environment. Many sensory scientists now routinely explore the physiological basis of sensing, such as vision, chemoreception or echolocation, in an ecological context. By contrast, research on one of the most performing sensors in the animal kingdom, the wind-sensitive escape system of crickets and cockroaches, has failed so far to encompass ecological and evolutionary considerations. We report survival and behavioural experiments in which wood crickets interacted freely with natural predators in the field. Our results illustrate how the lack of knowledge about the ecology of these insects may entail our understanding of the biological relevance of their wind sensors. We found that predation pressure was most important on early stage crickets. Because laboratory studies have focused exclusively on adults' sensory systems, it is crucial that physical, physiological and neurobiological studies now turn to juveniles. Another common assumption challenged by our results is the nature of the air flow to which crickets are sensitive. Our results identify wolf spiders as the major predatory risk for wood crickets. Air movement stimuli produced by hunting spiders are likely to be strikingly different from air flows produced by flying insects. Yet, our theoretical understanding of air motion sensing is currently drawn from oscillatory flows of flying predators only.

Air Movements↗

Ultrasound-triggered, flight-gated evasive maneuvers in the praying mantis Parasphendale agrionina. I. Free flight.

Free-flying male praying mantises Parasphendale agrionina (Gerst.) perform evasive maneuvers when stimulated by ultrasound and when attacked by hunting, echolocating bats. They do not, however, respond in any way when standing on a substratum. The maneuvers are graded in intensity with distance from the sound source: far from the source they are simple turns, whereas close to the source they are steep diving turns or spirals. The maneuvers are made under power, and the male's velocity doubles to almost 4 m s-1 by the end of a steep dive. The mantis does not show any directional preference. The behavioral threshold of 64 dB SPL and minimum latency to course change of 125 ms indicate that these mantises should have adequate time to evade bats using calls of greater than 85-90 dB SPL (at 10 cm). In field experiments with wild, hunting bats, P. agrionina successfully evaded capture in all five attacks to which they responded with evasive maneuvers. Out of three attacks on P. aeruginosa and three on a normally non-responding mantis, Miomantis paykullii Stål, in which there were no evasive maneuvers, the mantis was captured in five cases.

Animals↗

Ultrasonic vocalizations of flying bats monitored by radiotelemetry.

Ultrasonic vocalizations of flying bats were effectively monitored with radiotelemetry. We describe a device light enough to be carried by an 11 g bat for periods of up to 1 h. It transmitted signals adequate for fine frequency analysis within a range of approximately 3 m. Telemetry permitted the recording of constant-frequency pulses free from flight-induced Doppler shifts and without time delays. The difference in frequency between telemetered signals and the same signals detected by a remote microphone was used to calculate velocity and Doppler shifts. Pulse emission behavior of Pteronotus parnellii in flight was compared with simulated flight on a pendulum. The data showed significant differences in echo bandwidths, constant-frequency pulse durations and interpulse intervals. In flight, pulses and interpulse intervals tended to be shorter and bats maintained echo frequencies within a significantly narrower band. Phases of echolocation that characterized the approach to a target were clearly evident in flight, but not during pendulum swings. Differences in pulse durations and interpulse intervals may be correlated with the integration of wingbeat, respiration and vocalization. The absence of wing motion in simulated flight changes this integration.

Animals↗

Respiratory muscle activity in relation to vocalization in flying bats.

The structure of the thoracic and abdominal walls of Pteronotus parnellii (Microchiroptera: Mormoopidae) was described with respect to their function in respiration and vocalization. We monitored electromyographic activity of respiratory and flight muscles in relation to echolocative vocalization. In flight, signals were telemetered with a small FM transmitter modified to summate the low-frequency myopotentials with biosonar signals from a ceramic-crystal microphone. Recordings were also made from the same bats confined to a small cage. Vocalizations were used as the parameter by which all muscle activities were correlated. A discrete burst of activity in the lateral abdominal wall muscles accompanied each vocalization. Diaphragmatic myopotentials occurred between groups of calls and did not coincide with activity of the abdominal wall or with vocalizations. Flight muscles were not active in resting bats. During flight, vocalizations and the abdominal muscle activity that accompanied them coincided with myopotentials of the pectoralis and serratus ventralis muscles. We propose that contractions of the lateral abdominal wall provide the primary power for the production of intense biosonar vocalization in flying and in stationary bats. In flight, synchronization of vocalization with activity of the pectoralis and serratus ventralis jointly contribute to the pressurization of the thoraco-abdominal cavity. This utilization of pressure that is normally generated in flight facilitates respiration and allows for the production of intense vocalizations with little additional energetic expenditure.

Abdominal Muscles↗

Ultrasound acoustic startle response in scarab beetles.

We discovered an auditory sense in a night-flying scarab beetle, Euetheola humilis, the first scarab to be shown to hear airborne sounds. In the field, beetles were captured beneath speakers broadcasting ultrasound that simulated bat echolocation pulses. Apparently, the beetles took evasive action from a potential bat predator and flew into the traps. Using another behavioral assay in laboratory studies, the beetles were sensitive to frequencies ranging from 20 to 70 kHz at levels between 60 and 70 dB SPL. One component of the behavioral response, a head roll, was graded with stimulus intensity, and the number of potentials in electromyographic recordings from muscles involved in the roll increased as stimulus intensity increased. The response latency was about 40 ms at threshold, decreasing to about 30 ms at 20 dB above threshold. The beetle's short response latency is ideally suited for predator avoidance behavior and the frequency tuning of the response suggests that it could function in evasion from insectivorous bats. The beetle's acoustic sensitivity is remarkably similar to that of other night-flying insects showing ultrasound-induced startle and it should provide these scarab beetles with a similar advance warning of predation risk.

Acoustic Stimulation↗

The peripheral auditory characteristics of noctuid moths: information encoding and endogenous noise

The ability of the noctuid A1 cell acoustic receptor to encode biologically relevant information from bat echolocation calls is examined. Short-duration stimuli (less than approximately 6 ms) reduce the dynamic resolution of the receptor, making intensity, and hence range, estimates of foraging bats unreliable. This low dynamic range is further reduced by inaccurate encoding of stimulus intensity, reducing the real dynamic range of the A1 cell to 1 bit at stimulus durations below 3.1 ms. Interspike interval is also an unreliable measure of stimulus intensity at low stimulus levels and/or for short-duration stimuli. The quantity of information encoded per stimulus is reduced as the presentation rate of stimuli is increased. The spontaneous generation of A1 cell action potentials may reduce the ability of the moth to discriminate bat from non-bat signals. Even with a recognition criterion of three A1 cell spikes per call, the moth would regularly make wrong decisions about a bat being present in the immediate environment. Removing this noise would necessitate a considerable loss of information through filtering at the interneurone level. It is proposed that, for bats using short-duration calls, the moth would only be able to recognise an approaching bat from the repetitious nature of the incoming signal.

Journal Article↗

Forewing asymmetries during auditory avoidance in flying locusts

Flying locusts orient to sounds in their environment. Sounds similar to those produced by echolocating bats cause a flying locust to change its flight path. We used high-speed cinematography and videography to study changes in body posture and wing kinematics of tethered locusts in response to stimulation with bat-like sounds. Locusts showed both negative and positive phonotaxis to this stimulus. Within a few wingbeats of stimulus onset (between 126 and 226ms), locusts deflected their abdomens to one side, and the angle of the left and right forewings with respect to the dorsal­ventral body axis became asymmetrical during the downstroke. This forewing asymmetry, in which the forewing on the inside of the turn became more depressed, ranged from 20 to 45° (37±9.7°, mean ± s.d.) and was correlated with the direction and magnitude of abdomen deflection, a measure of steering in tethered, flying locusts. Hindwing stroke angle asymmetries were minimal or non-existent after stimulation. Coincident with changes in forewing asymmetry and abdomen deflection was a decrease in stroke amplitude (19±6.5°) of the forewing on the inside of the attempted turn. Motor patterns from forewing first basalar (M97) muscles showed an asymmetry in the timing of left and right depressor activation that ranged from 10.4 to 1.6ms (4.23±2.85ms). The number of spikes per depressor burst increased to a maximum of three spikes in the muscle on the inside of the attempted turn, and depressor frequency (wingbeat frequency) increased by approximately 2Hz (2.17±0.26Hz). We suggest that the asymmetry in forewing first basalar activity is causally related to the asymmetry in the timing of the initiation of the downstroke, resulting in an asymmetry in the ranges of the stroke angles of the forewings, which would impart a roll torque to the locust. This would augment the steering torques generated by concurrent changes in the angle of attack of the fore- and hindwings and changes in abdomen position to effect rapid avoidance manoeuvres.

Journal Article↗

Behavioral response to ultrasound by the tiger beetle Cicindela marutha dow combines aerodynamic changes and sound production.

Tethered flying tiger beetles, Cicindela marutha, respond to trains of bat-like ultrasonic pulses with a short-latency, multi-component behavior. The head rolls to one side, the metathoracic legs kick to the opposite side, the elytra swing backwards towards the hindwings and pronate, the hindwings increase their stroke excursion and frequency, and the plane of the hindwing motion tilts forward. In addition, the beetles produce trains of ultrasonic clicks typically containing 100-200 clicks in response to a 1 s stimulus. The clicks average 85-90 dB SPL at 2 cm. The latencies for hindwing changes and elytra swing in response to stimuli more than 10 dB over threshold are 90-110 ms; the latency to clicking is 120-150 ms. Neither the head roll nor the leg kick appears to be directional relative to the sound source. The behavioral response is broadly tuned with greatest sensitivity at 30-60 kHz and mean behavioral thresholds of 75-80 dB SPL. Physiological audiograms from the auditory afferents show substantially greater sensitivity and sharper tuning than the behavioral response, which suggests that tiger beetles may use their hearing in other contexts as well as during flight. The combination of aerodynamic components and arctiid-month-like clicking may provide these insects with a powerful defense against attack by echolocating bats.

Animals↗

Representation of behaviorally relevant sound frequencies by auditory receptors in the cricket teleogryllus oceanicus

Teleogryllus oceanicus is particularly sensitive to two ranges of sound frequency, one corresponding to intraspecific acoustical signals (4-5 kHz) and the other to the echolocation cries of bats (25-50 kHz). We recorded summed responses of the auditory nerve to stimuli in these two ranges. Nerve responses consist of trains of compound action potentials (CAPs), each produced by the summed activity of a number of receptor neurons. The amplitude of the CAP is up to four times larger for stimuli at 4.5 kHz than for stimuli at 30 kHz, suggesting either that the extracellular spikes produced by receptors that respond to 4.5 kHz are larger than those that respond to 30 kHz, or that receptors fire more synchronously in response to stimulation at 4.5 kHz, or that more receptors respond to stimulation at 4.5 kHz. Neither unit spike amplitude nor conduction velocity (which is expected to vary with spike amplitude) differs for the two frequencies, and the responses to 4.5 kHz are not produced by more tightly synchronized receptor populations, as judged by CAP breadth. We conclude that more receptors respond to 4. 5 kHz than to 30 kHz.

Journal Article↗

'Un chant d'appel amoureux': acoustic communication in moths

Tympanal sound receptors in moths evolved in response to selective pressures provided by echolocating insectivorous bats. The presence of these ultrasound detectors also set the stage for the later evolution of ultrasonic courtship signals in the tympanate moth families. Male moths have repeatedly exploited the bat-detection mechanisms in females for the purpose of finding, identifying and obtaining mates. Ultrasonic courtship has been described in several members of the moth families Arctiidae, Noctuidae and Pyralidae, and ultrasound is predicted to play a significant role in the courtship of other tympanate moths including the Sphingidae, Lymantriidae, Notodontidae and Geometridae. Ultrasonic signals are involved in species recognition, in male-male competition for mates and in female mate-choice systems. Pre-existing motor systems, including those involved in bat defence, have also been exploited for the purpose of generating high-frequency courtship signals. Sound production mechanisms in moths include thoracic tymbals, tegular tymbals, alar castanets and genital stridulatory organs. Thus, in both their sensory and motor aspects, the weapons of bat/moth warfare have frequently evolved into components of courtship systems.

Journal Article↗

Experience-dependent modification of ultrasound auditory processing in a cricket escape response.

The ultrasound acoustic startle response (ASR) of crickets (Teleogryllus oceanicus) is a defense against echolocating bats. The ASR to a test pulse can be habituated by a train of ultrasound prepulses. We found that this conditioning paradigm modified both the gain and the lateral direction of the startle response. Habituation reduced the slope of the intensity/response relationship but did not alter stimulus threshold, so habituation extended the dynamic range of the ASR to higher stimulus intensities. Prepulses from the side (90 degrees or 270 degrees azimuth) had a priming effect upon the lateral direction of the ASR, increasing the likelihood that test pulses from the front (between -22 degrees and +22 degrees ) would evoke responses towards the same side as prepulse-induced responses. The plasticity revealed by these experiments could alter the efficacy of the ASR as an escape response and might indicate experience-dependent modification of auditory perception. We also examined stimulus control of habituation by prepulse intensity or direction. Only suprathreshold prepulses induced habituation. Prepulses from one side habituated the responses to test pulses from either the ipsilateral or contralateral side, but habituation was strongest for the prepulse-ipsilateral side. We suggest that habituation of the ASR occurs in the brain, after the point in the pathway where the threshold is mediated, and that directional priming results from a second process of plasticity distinct from that underlying habituation. These inferences bring us a step closer to identifying the neural substrates of plasticity in the ASR pathway.

Acoustic Stimulation↗

Neuroethology of the katydid T-cell. I. Tuning and responses to pure tones.

The tuning and pure-tone physiology of the T-cell prothoracic auditory interneuron were investigated in the nocturnal katydid Neoconocephalus ensiger. The T-cell is extremely sensitive and broadly tuned, particularly to high-frequency ultrasound (>20 kHz). Adult thresholds were lowest and showed their least variability for frequencies ranging from 25 to 80 kHz. The average best threshold of the T-cell in N. ensiger ranged from 28 to 38 dB SPL and the best frequency from 20 to 27 kHz. In females, the T-cell is slightly more sensitive to the range of frequencies encompassing the spectrum of male song. Tuning of the T-cell in non-volant nymphs was comparable with that of adults, and this precocious ultrasound sensitivity supports the view that it has a role in the detection of terrestrial sources of predaceous ultrasound. In adults, T-cell tuning is narrower than that of the whole auditory (tympanic) organ, but only at audio frequencies. Superthreshold physiological experiments revealed that T-cell responses were ultrasound-biased, with intensity/response functions steeper and spike latencies shorter at 20, 30 and 40 kHz than at 5, 10 and 15 kHz. The same was also true for T-cell stimulation at 90 degrees compared with stimulation at 0 degrees within a frequency, which supports early T-cell research showing that excitation of the contralateral ear inhibits ipsilateral T-cell responses. In a temporal summation experiment, the integration time of the T-cell at 40 kHz (integration time constant tau =6.1 ms) was less than half that measured at 15 kHz ( tau =15.0 ms). Moreover, T-cell spiking in response to short-duration pure-tone trains mimicking calling conspecifics (15 kHz) and bat echolocation hunting sequences (40 kHz) revealed that temporal pattern-copying was superior for ultrasonic stimulation. Apparently, T-cell responses are reduced or inhibited by stimulation with audio frequencies, which leads to the prediction that the T-cell will encode conspecific song less well than bat-like frequency-modulated sweeps during acoustic playback. The fact that the T-cell is one of the most sensitive ultrasound neurons in tympanate insects is most consistent with it serving an alarm, warning or escape function in both volant and non-volant katydids (nymphs and adults).

Acoustic Stimulation↗

Molecular phylogeny of Japanese Rhinolophidae based on variations in the complete sequence of the mitochondrial cytochrome b gene.

Microchiroptera have diversified into many species whose size and the shapes of the complicated ear and nose have been adapted to their echolocation abilities. Their speciation processes, and intra- and interspecies relationships are still under discussion. Here we report on the geographical variation of Japanese Rhinolophus ferrumequinum and R. cornutus using the complete sequence of the mitochondrial cytochrome b gene to clarify the phylogenetic positions of the 2 species as well as that of Rhinolophidae within the Microchiroptera. We have found that sequence divergence values within each of the 2 species are unexpectedly low (0.07%-0.94%). We have also found that there is no local specificity of their mtCytb alleles. On the other hand, the divergence values for Japanese Microchiroptera (12.7%-16.6%) are much higher than those for other mammalian genera. Similarly, the values among five genera of Vespertilionidae were 20.5%-27.3%. Phylogenetic analysis shows that the 2 species of family Rhinolophidae in the suborder Microchiroptera belong to the Megachiroptera cluster in the constructed maximum parsimony tree. These results suggest that the speciation of Rhinolophidae involved its divergence as an independent lineage from other Microchiroptera, and other microbats might be paraphyletic. In addition, the tree also shows that the order Chiroptera is monophylitic, and the closest group to Chiroptera is the ungulates.

Alleles↗