A Mechanism for Vocal-Respiratory Coupling in the Mammalian Parabrachial Nucleus

Smotherman, Michael; Kobayasi, Kohta I.; Ma, Jie; Zhang, Shuyi; Metzner, Walter

doi:10.1523/jneurosci.4607-05.2006

Cited by 61 publications

(50 citation statements)

References 48 publications

(85 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Echo playbacks (echo mimics) were generated as described previously (30,31,45). Briefly, echolocation pulses were captured by a calibrated 1/4-inch microphone (4939 with preamplifier 2633; Brüel and Kjaer) placed 15 cm ahead of the bat's head.…”

Section: Methodsmentioning

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.

125

View full text Add to dashboard Cite

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...

show abstract

Section: Methodsmentioning

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.

125

View full text Add to dashboard Cite

show abstract

“…The major descending input to n.IX-X arises from the pretrigeminal nucleus of the dorsal tegmental area of the medulla (DTAM) in the rostral hindbrain (Wetzel et al, 1985;Brahic and Kelley, 2003;Zornik and Kelley, 2007). Based on its location and projections, DTAM is a potential homolog of the mammalian parabrachial nucleus (PB), also known to participate in vocal behavior (Jürgens, 2002;Smotherman et al, 2006). A major neuronal population in DTAM (DTAM IX-X neurons) projects to motor neurons throughout n.IX-X.…”

Section: Introductionmentioning

confidence: 99%

Regulation of Respiratory and Vocal Motor Pools in the Isolated Brain ofXenopus laevis

Zornik¹,

Kelley²

2008

J. Neurosci.

View full text Add to dashboard Cite

The aquatic frog Xenopus laevis uses a complex vocal repertoire during mating and male-male interactions. Calls are produced without breathing, allowing the frogs to vocalize for long periods underwater. The Xenopus vocal organ, the larynx, is innervated by neurons in cranial motor nucleus (n.) IX-X, which contains both vocal (laryngeal) and respiratory (glottal) motor neurons. The primary descending input to n.IX-X comes from the pretrigeminal nucleus of the dorsal tegmental area of the medulla (DTAM), located in the rostral hindbrain. We wanted to characterize premotor inputs to respiratory and vocal motor neurons and to determine what mechanisms might be involved in regulating two temporally distinct rhythmic behaviors: breathing and calling. Using isolated brain and larynx preparations, we recorded extracellular activity from the laryngeal nerve and muscles and intracellular activity in laryngeal and glottal motor neurons. Spontaneous nerve activities mimicking respiratory and vocal patterns were observed. DTAM projection neurons (DTAM IX-X neurons) provide direct input to glottal and laryngeal motor neurons. Electrical stimulation produced short-latency coordinated activity in the laryngeal nerve. DTAM IX-X neurons provide excitatory monosynaptic inputs to laryngeal motor neurons and mixed excitatory and inhibitory inputs to glottal motor neurons. DTAM stimulation also produced a delayed burst of glottal motor neuron activity. Together, our data suggest that neurons in DTAM produce vocal motor output by directly activating laryngeal motor neurons and that DTAM may coordinate vocal and respiratory motor activity.

show abstract

“…From these experiments we were unable to establish whether the inhibitory inputs to the PB that delayed inspiration during extended vocal sequences came from either descending motor commands or ascending afferent feedback, or a combination of both. However, the ventrolateral PB is known to be a central relay site mediating the reflexive coordination of respiratory rhythms with locomotor activity [8,100]: this general phenomenon known as locomotor-respiratory coupling is mediated by somatic afferent feedback to the same region of the PB in which we were able to manipulate vocal-respiratory coupling in horseshoe bats, which led us to hypothesize that vocal-respiratory coupling in mammals may rely upon somatosensory feedback from the larynx [137] …”

Section: Vocal-respiratory Coordination In Horseshoe Batsmentioning

confidence: 99%

“…Collectively these results led to the hypothesis that one of the principle roles of the PB in vocalizing may be to adapt respiratory rhythms to vocal motor commands by causing the appropriate phase shifts. This hypothesis was tested by pharmacologically inactivating the ventrolateral PB in awake, spontaneously vocalizing horseshoe bats [137].…”

Section: Laryngeal and Pulmonary Sources Of Feedbackmentioning

confidence: 99%

See 1 more Smart Citation

Sensory feedback control of mammalian vocalizations

Smotherman

2007

Behavioural Brain Research

View full text Add to dashboard Cite

Somatosensory and auditory feedback mechanisms are dynamic components of the vocal motor pattern generator in mammals. This review explores how sensory cues arising from central auditory and somatosensory pathways actively guide the production of both simple sounds and complex phrases in mammals. While human speech is a uniquely sophisticated example of mammalian vocal behavior, other mammals can serve as examples of how sensory feedback guides complex vocal patterns. Echolocating bats in particular are unique in their absolute dependence on voice control for survival: these animals must constantly adjust the acoustic and temporal patterns of their orientation sounds to efficiently navigate and forage for insects at high speeds under the cover of darkness. Many species of bats also utter a broad repertoire of communication sounds. The functional neuroanatomy of the bat vocal motor pathway is basically identical to other mammals, but the acute significance of sensory feedback in echolocation has made this a profitable model system for studying general principles of sensorimotor integration with regard to vocalizing. Bats and humans are similar in that they both maintain precise control of many different voice parameters, both exhibit a similar suite of responses to altered auditory feedback, and for both the efficacy of sensory feedback depends upon behavioral context. By comparing similarities and differences in the ways sensory feedback influences voice in humans and bats, we may shed light on the basic architecture of the mammalian vocal motor system and perhaps be able to better distinguish those features of human vocal control that evolved uniquely in support of speech and language.

show abstract

A Mechanism for Vocal-Respiratory Coupling in the Mammalian Parabrachial Nucleus

Cited by 61 publications

References 48 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

Regulation of Respiratory and Vocal Motor Pools in the Isolated Brain ofXenopus laevis

Sensory feedback control of mammalian vocalizations

Contact Info

Product

Resources

About