Evolutionary Convergence and Shared Computational Principles in the Auditory System

Carr, Catherine E.; Soares, Daphne

doi:10.1159/000063565

Cited by 101 publications

(109 citation statements)

References 116 publications

(176 reference statements)

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“…The systematic arrangement of axons with different conduction times tunes neurons to different ITDs, creating a place code whereby the location of peak activity forms a map of auditory space. This arrangement has been verified both structurally and physiologically for the bird ITD detection system (for review, see Carr and Soares, 2002;Grothe et al, 2004). Mammals, however, developed ITD processing independently (Manley et al, 2004) and the structural and functional mechanisms of ITD processing in mammals are not as well understood.…”

Section: Introductionmentioning

confidence: 84%

Interaural Time Difference Processing in the Mammalian Medial Superior Olive: The Role of Glycinergic Inhibition

Pecka

Brand²,

Behrend³

et al. 2008

Journal of Neuroscience

213

268

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The dominant cue for localization of low-frequency sounds are microsecond differences in the time-of-arrival of sounds at the two ears [interaural time difference (ITD)]. In mammals, ITD sensitivity is established in the medial superior olive (MSO) by coincidence detection of excitatory inputs from both ears. Hence the relative delay of the binaural inputs is crucial for adjusting ITD sensitivity in MSO cells. How these delays are constructed is, however, still unknown. Specifically, the question of whether inhibitory inputs are involved in timing the net excitation in MSO cells, and if so how, is controversial. These inhibitory inputs derive from the nuclei of the trapezoid body, which have physiological and structural specializations for high-fidelity temporal transmission, raising the possibility that well timed inhibition is involved in tuning ITD sensitivity. Here, we present physiological and pharmacological data from in vivo extracellular MSO recordings in anesthetized gerbils. Reversible blockade of synaptic inhibition by iontophoretic application of the glycine antagonist strychnine increased firing rates and significantly shifted ITD sensitivity of MSO neurons. This indicates that glycinergic inhibition plays a major role in tuning the delays of binaural excitation. We also tonically applied glycine, which lowered firing rates but also shifted ITD sensitivity in a way analogous to strychnine. Hence tonic glycine application experimentally decoupled the effect of inhibition from the timing of its inputs. We conclude that, for proper ITD processing, not only is inhibition necessary, but it must also be precisely timed.

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Section: Introductionmentioning

confidence: 84%

Interaural Time Difference Processing in the Mammalian Medial Superior Olive: The Role of Glycinergic Inhibition

Pecka

Brand²,

Behrend³

et al. 2008

Journal of Neuroscience

213

268

View full text Add to dashboard Cite

show abstract

“…Parallel evolution should be expected if there are computational advantages to a particular solution [21,59]. Selective pressure to encode higher frequency sounds may have driven the appearance of similar features of the auditory systems of archosaurs and mammals.…”

Section: Discussionmentioning

confidence: 99%

“…Endbulb terminals may have emerged as an adaptation for accurate transmission of phase information for frequencies above 1000 Hz, perhaps associated with the evolution of higher-frequency hearing in land vertebrates [21,69]. Large somatic terminals have been found in all amniote groups examined.…”

Section: Presynaptic Specializations For Encoding Temporal Informationmentioning

confidence: 96%

“…Coincidence detectors in mammals, birds and crocodilians share a common morphological organization [21]. Almost all are bitufted neurons with inputs from each ear segregated on the dendrites.…”

Section: Coincidence Detectors In Birds and Mammalsmentioning

confidence: 99%

“…Both sections will be used to support the hypothesis that birds and mammals use similar strategies for auditory coding, including ''slope'' coding at low best frequency ITDs, and ''peak coding'' for higher best frequencies. In the discussion we will identify similarities among the brainstem circuits that detect interaural time differences in birds and mammals, and argue that these are the result of parallel evolution (see review in [21]). Evidence for parallel evolution comes from the observation that tetrapod tympanic ears are not homologs, and may have evolved independently at least five times (modern representatives given in brackets) in synapsids (mammals), lepidosauromorph diapsids (snakes and lizards), archosauromorph diapsids (birds and crocodilians), probably turtles, and amphibians [23,69,70].…”

Section: Introductionmentioning

confidence: 99%

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Coding interaural time differences at low best frequencies in the barn owl

Carr

Köppl

2004

Journal of Physiology-Paris

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In birds and mammals, precisely timed spikes encode the timing of acoustic stimuli, and interaural acoustic disparities propagate to binaural processing centers. The Jeffress model proposes that these projections act as delay lines to innervate an array of coincidence detectors, every element of which has a different relative delay between its ipsilateral and contralateral excitatory inputs. Thus, interaural time difference (ITD) is encoded into the position of the coincidence detector whose delay lines best cancel out the acoustic ITD. Neurons of the avian nucleus laminaris and mammalian MSO phase-lock to both monaural and binaural stimuli but respond maximally when phase-locked spikes from each side arrive simultaneously, i.e. when the difference in the conduction delays compensates for the ITD. McAlpine et al. [Nat. Neurosci. 4 (2001) 396] identified an apparent difference between avian and mammalian ITD coding. In the barn owl, the maximum firing rate appears to encode ITD. This may not be the case for the guinea pig, where the steepest region of the function relating discharge rate to interaural time delay (ITD) is close to midline for all neurons, irrespective of best frequency (BF). These data suggest that low BF ITD sensitivity in the guinea pig is mediated by detection of a change in slope of the ITD function, and not by maximum rate. We review coding of low best frequency ITDs in barn owls and mammals and discuss whether there may be differences in the code used to signal ITD in mammals and birds.

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Timing is everything: Organization of timing circuits in auditory and electrical sensory systems

Carr

2004

J of Comparative Neurology

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Auditory and electrosensory systems are specialized to encode incoming sensory information, often with microsecond precision (Trussell, 2002). This kind of accurate coding is metabolically costly (Laughlin, 2001), but precise encoding of temporal information has direct behavioral relevance for sound localization and communication and appears to be the subject of selection. It is certainly true that the kinds of physiological and morphological adaptations that could improve temporal coding are found in the auditory brainstem of both birds and mammals and in the electrosensory system (Carr and Soares, 2002).Why do the auditory and electrosensory systems go to so much expense to preserve temporal information? Most timing information is directed to the goal of accurately detecting time differences between two signals. Once the time difference is computed, the temporal code can be transformed into a new and less energetically expensive code of time or phase difference. Comparative studies of temporal coding in the auditory and electrosensory systems, including one from Matsushita and Kawasaki in this issue of the Journal, have identified circuits to detect time differences in all systems. All of these timing circuits share similar computational strategies and many morphological features.In the auditory system, the secure and precise transmission of the phase-locked discharges of the auditory nerve fibers to their postsynaptic targets is mediated by the giant end-bulb synapse, which ensures fast, reliable, high-frequency excitatory transmission. Similarly shaped caliciform synapses are also present in higher order auditory neurons of mammalian time coding pathways, including neurons of the medial nucleus of the trapezoid body (Forsythe, 1994) and the type II neurons of the ventral nucleus of the lateral lemniscus (Wu, 2000) and in the chick ciliary ganglion (Paysan et al., 2000). In this issue, Matsushita and Kawasaki describe a new giant synapse in the electrosensory system of the weakly electric fish, Gymnarchus. The synapse originates from an electrosensory giant cell, which forms a socket-like structure around the cell body of an ovoidal cell. This study has two novel results. First, their discovery of a new nonfenestrated giant synapse raises the question of how such a synapse might function. Second, they describe a new circuit for detection of temporal disparity, leading to fresh insights into the functional organization of time coding circuits in auditory and electrosensory circuits.

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Evolutionary Convergence and Shared Computational Principles in the Auditory System

Cited by 101 publications

References 116 publications

Interaural Time Difference Processing in the Mammalian Medial Superior Olive: The Role of Glycinergic Inhibition

Interaural Time Difference Processing in the Mammalian Medial Superior Olive: The Role of Glycinergic Inhibition

Coding interaural time differences at low best frequencies in the barn owl

Timing is everything: Organization of timing circuits in auditory and electrical sensory systems

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