Neural maps in insect versus vertebrate auditory systems

Hildebrandt, K. Jannis

doi:10.1016/j.conb.2013.08.020

Cited by 24 publications

(24 citation statements)

References 64 publications

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“…The auditory system of insects might thus be thought of as a special-purpose, rigid system, adapted to detect only a handful of signals, mostly mate and predator calls. This view accords with the finding that information within the insect brain is quickly distributed into multiple parallel (and decorrelated) streams for the separate extraction of individual stimulus features [77]. The vertebrate auditory system, in contrast, is a general-purpose and more flexible system that is shaped by learning [78][79][80][81], affected by mood [82], focused by attention [83][84][85], and one that influences and is influenced by other parts of the brain, both sensory [86] and motor [87] areas, to detect and interpret any sound that may be subjectively important at any particular moment.…”

Section: Curbio 13179supporting

confidence: 84%

“…Tonotopy is one of the fundamental organizational principles of the vertebrate inner ear, including the mammalian cochlea. As in vertebrates, the projection patterns of first-order sensory neurons in insect auditory systems can retain this tonotopic organization [113], but, unlike the situation in vertebrates, the tonotopy does not appear to extend to downstream interneurons [77]. Perhaps most strikingly of all, even the spectral decomposition of sound by way of dispersive wave propagation, which enables frequency analysis in the cochlea, has been found in an insect (Copiphora gorgonensis) [114].…”

Section: Discussionmentioning

confidence: 99%

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Comparative Aspects of Hearing in Vertebrates and Insects with Antennal Ears

Albert¹,

Kozlov

2016

Current Biology

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The evolution of hearing in terrestrial animals has resulted in remarkable adaptations enabling exquisitely sensitive sound detection by the ear and sophisticated sound analysis by the brain. In this review, we examine several such characteristics, using examples from insects and vertebrates. We focus on two strong and interdependent forces that have been shaping the auditory systems across taxa: the physical environment of auditory transducers on the small, subcellular scale, and the sensory-ecological environment within which hearing happens, on a larger, evolutionary scale. We briefly discuss acoustical feature selectivity and invariance in the central auditory system, highlighting a major difference between insects and vertebrates as well as a major similarity. Through such comparisons within a sensory ecological framework, we aim to emphasize general principles underlying acute sensitivity to airborne sounds.Introduction Auditory physiology offers a distinctive perspective on the interaction between a sensory system and its environment. On the one hand, auditory systems in vertebrates and insects with sensitive hearing are capable of remarkable performances on multiple levels, both within the sensory periphery where the minute energies associated with sound are converted into electrical signals, as well as within higher-order brain areas where complex natural stimuli such as human speech are processed. For example, displacements caused by acoustical stimuli in the inner ear at the threshold of hearing are sub-nanometer and comparable to the distance between atoms in molecules [1]. Furthermore, thermal fluctuations in the ear's mechanotransduction apparatus not only are significant, but also can be larger than the faintest audible signals, making signal detection a challenging task [2]. Ascending the sensory hierarchy, one encounters other marvels of evolution, such as the ability of individual neurons to encode -using millisecond-long action potentials -inter-aural time differences of only about ten microseconds, and to use this information to localize the source of the sound [3,4]. No engineered system has yet been designed that could understand distorted speech in a noisy and reverberating environment with multiple speakers. That our auditory system achieves this feat is testament to its remarkable performance.On the other hand, an engineer could argue that the auditory system's performance is objectively poor, even in animals with sensitive hearing: at the very first step, during the mechanoelectrical transduction in the inner ear, external sounds are distorted, or even completely suppressed, while new tones are generated by the ear itself [5]. Forward and backward masking, illusory percepts of nonexistent tones (such as the Zwicker illusion [6]), perceptual merging of separate auditory streams, the precedence effect suppressing the perception of echoes that has been demonstrated in insects and vertebrates [7,8] (and which some blind people can unsuppress), auditory hallucinations, and a frustrating inab...

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Section: Curbio 13179supporting

confidence: 84%

Section: Discussionmentioning

confidence: 99%

Comparative Aspects of Hearing in Vertebrates and Insects with Antennal Ears

Albert¹,

Kozlov

2016

Current Biology

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“…In line with these tasks, peripheral frequency filtering and object categorization is well known (Wohlers and Huber 1978;Wyttenbach et al 1996;Hildebrandt 2014). At the network level of the peripheral auditory system of the cricket, AN1 and AN2 represent the two channels of information transmission associated with such a categorical perception, as given by their differential tuning for low and high carrier frequencies (Wohlers and Huber 1978;Hennig 1988) and their ability to modulate behavior (for AN1: Schildberger and Hörner 1988; for AN2: Nolen and Hoy 1984;Marsat and Pollack 2006).…”

Section: Firing-rate Resonances Of Neurons and Behavioral Relevancementioning

confidence: 99%

Firing-rate resonances in the peripheral auditory system of the cricket, Gryllus bimaculatus

et al. 2015

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In many communication systems, information is encoded in the temporal pattern of signals. For rhythmic signals that carry information in specific frequency bands, a neuronal system may profit from tuning its inherent filtering properties towards a peak sensitivity in the respective frequency range. The cricket Gryllus bimaculatus evaluates acoustic communication signals of both conspecifics and predators. The song signals of conspecifics exhibit a characteristic pulse pattern that contains only a narrow range of modulation frequencies. We examined individual neurons (AN1, AN2, ON1) in the peripheral auditory system of the cricket for tuning towards specific modulation frequencies by assessing their firing-rate resonance. Acoustic stimuli with a swept-frequency envelope allowed an efficient characterization of the cells' modulation transfer functions. Some of the examined cells exhibited tuned band-pass properties. Using simple computational models, we demonstrate how different, cell-intrinsic or network-based mechanisms such as subthreshold resonances, spike-triggered adaptation, as well as an interplay of excitation and inhibition can account for the experimentally observed firing-rate resonances. Therefore, basic neuronal mechanisms that share negative feedback as a common theme may contribute to selectivity in the peripheral auditory pathway of crickets that is designed towards mate recognition and predator avoidance.

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“…Surprisingly, however, most of the detailed frequency representation of the periphery is lost centrally due to strong neuronal convergence (for rare exceptions, see Stumpner 1998). So we may ask what the tonotopic arrangement of the periphery is good for (Hildebrandt 2014). Here, I suggest four cases of auditory processing in ecologically important contexts, where spectral information through the series of frequency filters in the ear can be used: (1) estimation of distance to signalers, (2) intensity discrimination, (3) novelty detection, and (4) improvement of SNR for temporal processing (see also Pollack and Imaizumi 1999;Hennig et al 2004;Hildebrandt et al 2014).…”

Section: The Tuned Frequency-filter Paradox In Katydidsmentioning

confidence: 99%

Matched Filters in Insect Audition: Tuning Curves and Beyond

Römer

2015

The Ecology of Animal Senses

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Neural maps in insect versus vertebrate auditory systems

Cited by 24 publications

References 64 publications

Comparative Aspects of Hearing in Vertebrates and Insects with Antennal Ears

Comparative Aspects of Hearing in Vertebrates and Insects with Antennal Ears

Firing-rate resonances in the peripheral auditory system of the cricket, Gryllus bimaculatus

Matched Filters in Insect Audition: Tuning Curves and Beyond

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