Neural Attenuation of Responses to Emitted Sounds in Echolocating Bats

Suga, Nobuo; Schlegel, P.

doi:10.1126/science.177.4043.82

Cited by 167 publications

(80 citation statements)

References 9 publications

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“…Consequently, the shifts in amplitude and frequency that we found have to be implemented within the neuronal network involved in vocal motor control to avoid such reflectory compensation. Several multimodal structures have been identified within the brainstem of bats and other mammals that may serve as candidates for audiovocal integration (42), such as the ventrolateral reticular formation (43,44), the parabrachial region (45), the ventral nucleus of the lateral lemniscus (46,47), the paralemniscal area (48,49), and the external nucleus of the inferior colliculus (50). Further studies will tackle the questions of if and how these structures are involved in the neural adjustments governing the Lombard effect and the associated frequency changes.…”

Section: Discussionmentioning

confidence: 99%

Ambient noise induces independent shifts in call frequency and amplitude within the Lombard effect in echolocating bats

Hage

Jiang

Berquist

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

126

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The Lombard effect, an involuntary rise in call amplitude in response to masking ambient noise, represents one of the most efficient mechanisms to optimize signal-to-noise ratio. The Lombard effect occurs in birds and mammals, including humans, and is often associated with several other vocal changes, such as call frequency and duration. Most studies, however, have focused on noisedependent changes in call amplitude. It is therefore still largely unknown how the adaptive changes in call amplitude relate to associated vocal changes such as frequency shifts, how the underlying mechanisms are linked, and if auditory feedback from the changing vocal output is needed. Here, we examined the Lombard effect and the associated changes in call frequency in a highly vocal mammal, echolocating horseshoe bats. We analyzed how bandpassfiltered noise (BFN; bandwidth 20 kHz) affected their echolocation behavior when BFN was centered on different frequencies within their hearing range. Call amplitudes increased only when BFN was centered on the dominant frequency component of the bats' calls. In contrast, call frequencies increased for all but one BFN center frequency tested. Both amplitude and frequency rises were extremely fast and occurred in the first call uttered after noise onset, suggesting that no auditory feedback was required. The different effects that varying the BFN center frequency had on amplitude and frequency rises indicate different neural circuits and/or mechanisms underlying these changes.A ny transmission of signals between sender and receiver faces the challenge of being subjected to masking by noise. For acoustic signals, for example, animals have evolved several strategies that aid in increasing the signal-to-noise ratio, thus facilitating signal transmission. One of the most efficient mechanisms is the socalled Lombard effect, i.e., the involuntary rise in call amplitude in response to masking ambient noise (1). This effect was first described in human communication a century ago (2) and has since been found in several species of birds (3-11) and various mammals (12-17), including bats (18). In human speech, several vocal changes, such as a rise in fundamental frequency (19) or lengthening in word duration (20), are often accompanied with the Lombard effect; combined, these changes are referred to as Lombard speech (21). Vocal changes associated with the Lombard effect have rarely been analyzed in animal species. So far, noisedependent changes in call frequency have been observed in birds (8,11,22), and changes in call duration in birds and monkeys (8,12).Most animal studies, however, have focused on noise-dependent changes in call amplitude and do not examine other possible vocal changes (2-5, 7, 9, 10, 15-17). It is therefore still largely unknown how the adaptive changes in call amplitude relate to frequency shifts or call elongation and how the underlying mechanisms are linked. It is also unknown if auditory feedback from the changing vocal output is needed to drive the Lombard effect in general.Over...

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Section: Discussionmentioning

confidence: 99%

Ambient noise induces independent shifts in call frequency and amplitude within the Lombard effect in echolocating bats

Hage

Jiang

Berquist

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

126

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“…In contrast to the auditory processing of passive sounds, the neuronal processing of echoes is coupled to, and influenced by, the vocalisation pattern (Suga and Schlegel, 1972;Schuller, 1979), for example by opening temporal processing windows (Roverud and Grinnell, 1985). Based on neurophysiological data, it was suggested for the gleaning bat Antrozous pallidus that it processes passively heard prey sounds and actively acquired echoes in two different, parallel auditory pathways (Fuzessery, 1994;Razak and Fuzessery, 2002), which converge later in the auditory cortex (Razak et al, 1999).…”

Section: Experiments 2: Spectral Processing During Echolocationmentioning

confidence: 99%

“…The neuronal processing of auditory information is different in passive hearing and active echolocation and is closely coupled to and directly influenced by the vocalizations during echolocation (Suga and Schlegel, 1972;Schuller, 1979). The behavioural responses to auditory stimuli may thus differ in the same experimental task between passive and active hearing.…”

Section: Introductionmentioning

confidence: 99%

Comparing passive and active hearing: spectral analysis of transient sounds in bats

Goerlitz

Hübner

Wiegrebe

2008

Journal of Experimental Biology

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SUMMARYIn vision, colour constancy allows the evaluation of the colour of objects independent of the spectral composition of a light source. In the auditory system, comparable mechanisms have been described that allows the evaluation of the spectral shape of sounds independent of the spectral composition of ambient background sounds. For echolocating bats, the evaluation of spectral shape is vitally important both for the analysis of external sounds and the analysis of the echoes of self-generated sonar emissions. Here, we investigated how the echolocating bat Phyllostomus discolor evaluates the spectral shape of transient sounds both in passive hearing and in echolocation as a specialized mode of active hearing. Bats were trained to classify transients of different spectral shape as low-or highpass. We then assessed how the spectral shape of an ambient background noise influenced the spontaneous classification of the transients. In the passive-hearing condition, the bats spontaneously changed their classification boundary depending on the spectral shape of the background. In the echo-acoustic condition, the classification boundary did not change although the background-and spectral-shape manipulations were identical in the two conditions. These data show that auditory processing differs between passive and active hearing: echolocation represents an independent mode of active hearing with its own rules of auditory spectral analysis.

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“…Echolocation works best when the loud outgoing vocalizations do not mask or reduce the listener's sensitivity to the weaker returning echoes (Jen and Suga, 1976;Suga and Schlegel, 1972;Fenton et al, 1995). Most echolocators avoid forward masking effects by separating pulse and echo in time; however, ~160 species of bats in the families Rhinolophidae and Hipposideridae and the mormoopid Pteronotus parnellii separate pulse and echo information in frequency.…”

Section: Introductionmentioning

confidence: 99%

Evolution of high duty cycle echolocation in bats

Fenton

Faure

Ratcliffe

2012

Journal of Experimental Biology

112

129

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SummaryDuty cycle describes the relative ʻon timeʼ of a periodic signal. In bats, we argue that high duty cycle (HDC) echolocation was selected for and evolved from low duty cycle (LDC) echolocation because increasing call duty cycle enhanced the ability of echolocating bats to detect, lock onto and track fluttering insects. Most echolocators (most bats and all birds and odontocete cetaceans) use LDC echolocation, separating pulse and echo in time to avoid forward masking. They emit short duration, broadband, downward frequency modulated (FM) signals separated by relatively long periods of silence. In contrast, bats using HDC echolocation emit long duration, narrowband calls dominated by a single constant frequency (CF) separated by relatively short periods of silence. HDC bats separate pulse and echo in frequency by exploiting information contained in Doppler-shifted echoes arising from their movements relative to background objects and their prey. HDC echolocators are particularly sensitive to amplitude and frequency glints generated by the wings of fluttering insects. We hypothesize that narrowband/CF calls produced at high duty cycle, and combined with neurobiological specializations for processing Doppler-shifted echoes, were essential to the evolution of HDC echolocation because they allowed bats to detect, lock onto and track fluttering targets. This advantage was especially important in habitats with dense vegetation that produce overlapping, time-smeared echoes (i.e. background acoustic clutter). We make four specific, testable predictions arising from this hypothesis.Key words: Chiroptera, calling behaviour, signal design, Yinpterochiroptera, Yangochiroptera, flutter detection, Doppler shift compensation. Fig.1A-C). For the purpose of this paper, we define LDC bats as those producing signals with a duration <25% of their signal period during the search phase of echolocation. Most LDC bats produce echolocation calls with their larynx, although a handful of species in the family Pteropodidae use tongue clicks (Griffin et al., 1958;Yovel et al., 2010).HDC bats avoid auditory masking by separating pulse and echo in frequency, allowing them to broadcast calls and receive echoes at the same time (Schuller, 1974;Schuller, 1977). HDC bats take advantage of information contained in Doppler-shifted echoes generated by the relative movements of bat and target, including acoustic glints generated by the wingbeats of fluttering insects. Echolocation calls of HDC bats consist of a long CF component followed by a brief, downward FM sweep. In some species, the initial portion of the call also contains a short, upward FM sweep (Henson et al., 1987; Jones and Rayner, 1989). Narrowband calls of HDC bats are typically multi-harmonic with the highest signal energy in the second acoustic element (Pye and Roberts, 1970;Schnitzler and Denzinger, 2011). HDC bats emit long duration calls (e.g. 10 to >50ms) relative to their call period ( Fig.1D-F). We operationally define HDC bats as those whose signal durations are ≥25% of...

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Neural Attenuation of Responses to Emitted Sounds in Echolocating Bats

Cited by 167 publications

References 9 publications

Ambient noise induces independent shifts in call frequency and amplitude within the Lombard effect in echolocating bats

Ambient noise induces independent shifts in call frequency and amplitude within the Lombard effect in echolocating bats

Comparing passive and active hearing: spectral analysis of transient sounds in bats

Evolution of high duty cycle echolocation in bats

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