Sensing in a noisy world: lessons from auditory specialists, echolocating bats

Corcoran, Aaron J.; Moss, Cynthia F.

doi:10.1242/jeb.163063

Cited by 69 publications

(46 citation statements)

References 146 publications

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“…All Doppler shifts that occur in bat biosonar can be classified as either prey-generated or self-generated. At present, preygenerated Doppler shifts are the only well-established solution to the problem of identifying prey in clutter with active biosonar (21). The importance of prey-generated Doppler shifts is evident from numerous, far-reaching adaptations in bats that range from pulse design to behavior and from the inner ear (22) to the auditory cortex (23,24).…”

Section: Discussionmentioning

confidence: 99%

Fast-moving bat ears create informative Doppler shifts

Yin

Müller

2019

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

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Many animals have evolved adept sensory systems that enable dexterous mobility in complex environments. Echolocating bats hunting in dense vegetation represent an extreme case of this, where all necessary information about the environment must pass through a parsimonious channel of pulsed, 1D echo signals. We have investigated whether certain bats (rhinolophids and hipposiderids) actively create Doppler shifts with their pinnae to encode additional sensory information. Our results show that the bats' active pinna motions are a source of Doppler shifts that have all attributes required for a functional relevance: (i) the Doppler shifts produced were several times larger than the reported perception threshold; (ii) the motions of the fastest moving pinna portions were oriented to maximize the Doppler shifts for echoes returning from the emission direction, indicating a possible evolutionary optimization; (iii) pinna motions coincided with echo reception; (iv) Doppler-shifted signals from the fast-moving pinna portion entered the ear canal of a biomimetic pinna model; and (v) the time-frequency Doppler shift signatures were found to encode target direction in an orderly fashion. These results indicate that instead of avoiding or suppressing all self-produced Doppler shifts, rhinolophid and hipposiderid bats actively create Doppler shifts with their own pinnae. These bats could hence make use of a previously unknown nonlinear mechanism for the encoding of sensory information, based on Doppler signatures. Such a mechanism could be a source for the discovery of sensing principles not only in sensory physiology but also in the engineering of sensory systems.biosonar | ear motions | Doppler shifts | time-frequency signatures | nonlinear sensing C onspicuous pinna motions (1-5) are an integral part of biosonar behaviors in horseshoe bats and Old World leafnosed bats [families Rhinolophidae and Hipposideridae (6, 7)]. These motions have been demonstrated to enhance sensing and navigation performance (8-10), but the functional role of these dynamic features and the underlying mechanisms have yet to be fully understood (7). In the acoustic domain, source or receiver motions can result in Doppler shifts, i.e., nonlinear scaling of signals in time and frequency. The possibility of pinna-induced Doppler shifts had been mentioned as an aside in early work by Pye and coworkers (2, 3, 11) but has not been considered further-let alone investigated in any depthin the literature since. This complete neglect is regrettable, because ear-generated Doppler shifts could constitute a previously unknown, nonlinear mechanism for the active encoding of sensory information. To test this hypothesis, we have carried out a quantitative experimental investigation of the hypothesis that pinna motions cause functionally relevant Doppler shifts in bats. For pinna-generated Doppler shifts to have a functional role, five necessary conditions must be met: (i) pinna surface speeds must be high enough to produce Doppler shifts that exceed the animal's per...

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Section: Discussionmentioning

confidence: 99%

Fast-moving bat ears create informative Doppler shifts

Yin

Müller

2019

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

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“…Interestingly, studies have suggested that intrinsic noise could enhance sensitivity to weak signals (Stein, Gossen, & Jones, ). The latter might be important for bats that have to cope with faint signals during navigation (i.e., echoes) often in noisy environments (Corcoran & Moss, ).…”

Section: Discussionmentioning

confidence: 99%

Modified synaptic dynamics predict neural activity patterns in an auditory field within the frontal cortex

López‐Jury

Mannel

García‐Rosales

et al. 2019

Eur J of Neuroscience

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Frontal areas of the mammalian cortex are thought to be important for cognitive control and complex behaviour. These areas have been studied mostly in humans, non‐human primates and rodents. In this article, we present a quantitative characterization of response properties of a frontal auditory area responsive to sound in the brain of Carollia perspicillata, the frontal auditory field (FAF). Bats are highly vocal animals, and they constitute an important experimental model for studying the auditory system. We combined electrophysiology experiments and computational simulations to compare the response properties of auditory neurons found in the bat FAF and auditory cortex (AC) to simple sounds (pure tones). Anatomical studies have shown that the latter provides feedforward inputs to the former. Our results show that bat FAF neurons are responsive to sounds, and however, when compared to AC neurons, they presented sparser, less precise spiking and longer‐lasting responses. Based on the results of an integrate‐and‐fire neuronal model, we suggest that slow, subthreshold, synaptic dynamics can account for the activity pattern of neurons in the FAF. These properties reflect the general function of the frontal cortex and likely result from its connections with multiple brain regions, including cortico‐cortical projections from the AC to the FAF.

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“…The latter might be important for bats that have to cope with faint signals during navigation (i.e. echoes) often in noisy environments (Corcoran & Moss, 2017).…”

Section: Discussionmentioning

confidence: 99%

Precision of auditory responses deteriorates on the way to frontal cortical areas

López‐Jury

Mannel

García‐Rosales

et al. 2019

Preprint

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Frontal areas of the mammalian cortex are thought to be important for cognitive control and complex behaviour. These areas have been studied mostly in humans, non-human primates and rodents. In this article, we present a quantitative characterization of response properties of a frontal auditory area responsive to sound in the bat brain, the frontal auditory field (FAF).Bats are highly vocal animals and they constitute an important experimental model for studying the auditory system. At present, little is known about neuronal sound processing in the bat FAF. We combined electrophysiology experiments and computational simulations to compare the response properties of auditory neurons found in the bat FAF and auditory cortex (AC) to simple sounds (pure tones). Anatomical studies have shown that the latter provide feedforward inputs to the former. Our results show that bat FAF neurons are responsive to sounds, however, when compared to AC neurons, they presented sparser, less precise spiking and longer-lasting responses. Based on the results of an integrate-and-fire neuronal model, we speculate that slow, low-threshold, synaptic dynamics could contribute to the changes in activity pattern that occur as information travels through cortico-cortical projections from the AC to the FAF.

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Sensing in a noisy world: lessons from auditory specialists, echolocating bats

Cited by 69 publications

References 146 publications

Fast-moving bat ears create informative Doppler shifts

Fast-moving bat ears create informative Doppler shifts

Modified synaptic dynamics predict neural activity patterns in an auditory field within the frontal cortex

Precision of auditory responses deteriorates on the way to frontal cortical areas

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