Auditory midbrain neurons that count

Edwards, Christofer J.; Alder, Todd B.; Rose, Garrett S.

doi:10.1038/nn916

Cited by 121 publications

(92 citation statements)

References 11 publications

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“…These band-suppression, interval-counting neurons respond well to long-duration tone bursts apparently because these stimuli elicit sufficient optimal interspike intervals in the afferents (Edwards and Rose, 2003). To the best of our knowledge, this is the first evidence that long-pass neurons also show interval-counting properties (Edwards et al, 2002) and PRR selectivity. In these cells, enhancement of excitation overcomes inhibition at fast PRRs.…”

Section: Prr Specificitymentioning

confidence: 61%

Midbrain Auditory Neurons Integrate Excitation and Inhibition to Generate Duration Selectivity: AnIn VivoWhole-Cell Patch Study in Anurans

Leary

Edwards

Rose³

2008

J. Neurosci.

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Sound duration can play a pivotal role in the reproductive behavior of anuran amphibians. Here, we report the first whole-cell recordings from duration-selective neurons in the anuran torus semicircularis, in vivo. We show that most short-pass duration-selective cells exhibited short-latency inhibition and delayed excitation. The duration of the inhibition increased with tone burst duration. Hence, for long-duration tone bursts, inhibition overlapped with excitation, reducing or eliminating spikes; no postinhibitory rebound was present. Other short-pass cells, however, showed inhibition only for long-duration tone bursts. Bandpass duration selectivity also involved interplay between inhibition and excitation; inhibition negated excitation with tone bursts that exceeded the optimum duration. Additionally, however, bandpass selectivity arose from stimulus-dependent excitation; tone bursts of sufficiently long duration were required to elicit excitation. Similarly, long-pass neurons showed inhibition and duration-dependent enhancement of excitation; long-pass selectivity resulted from enhanced excitation outlasting the transient inhibition or, in some cases, excitation overriding concurrent inhibition. Last, we evaluated the stimulus specificity of duration-selective neurons to variations in pulse repetition rate. We show that (1) most neurons that exhibited long-pass selectivity for tone-burst duration nonetheless responded to short-duration pulses when repeated at particular rates, and (2) some neurons that showed selectivity for tone burst duration also showed selectivity for pulse train duration. These novel response profiles appear to result from interplay between inhibition and time-and activity-dependent changes in excitation strength. These findings are discussed in the context of prevailing models of duration selectivity and acoustic communication in anurans.

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Section: Prr Specificitymentioning

confidence: 61%

Midbrain Auditory Neurons Integrate Excitation and Inhibition to Generate Duration Selectivity: AnIn VivoWhole-Cell Patch Study in Anurans

Leary

Edwards

Rose³

2008

J. Neurosci.

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“…There is ample evidence that animals have memories for acoustic objects and can achieve simple counting (Brannon & Terrace, 1998), and single neurons with acoustic response properties that are sensitive to the number of distinct elements in a sequence have been reported (Edwards, Alder, & Rose, 2002). Elaboration of recognition, classification, and memory capacities in species such as vocal learners that produce long temporal strings of component signals may help explain why starlings were adept at the syntactic pattern classification tasks reported here.…”

Section: Discussionmentioning

confidence: 78%

Mechanisms of Temporal Auditory Pattern Recognition in Songbirds

Gentner

2007

Language Learning and Development

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“…The counting mechanism proposed for readout is similar to that of frogs that also communicate with rhythmic patterns of sound pulses and quiet intervals. Specific neurons in the frog's auditory midbrain integrate the number of acoustic pulses and respond only if a minimal number of appropriate pulses and interpulse intervals arrive (Alder and Rose, 1998;Edwards et al, 2002Edwards et al, , 2007. Combined excitation and inhibition determine the dependence of the responses on the duration of the acoustic elements Leary et al, 2008).…”

Section: Discussionmentioning

confidence: 99%

Timescale-Invariant Representation of Acoustic Communication Signals by a Bursting Neuron

Creutzig

Wohlgemuth²,

Stumpner³

et al. 2009

J. Neurosci.

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Acoustic communication often involves complex sound motifs in which the relative durations of individual elements, but not their absolute durations, convey meaning. Decoding such signals requires an explicit or implicit calculation of the ratios between time intervals. Using grasshopper communication as a model, we demonstrate how this seemingly difficult computation can be solved in real time by a small set of auditory neurons. One of these cells, an ascending interneuron, generates bursts of action potentials in response to the rhythmic syllable-pause structure of grasshopper calls. Our data show that these bursts are preferentially triggered at syllable onset; the number of spikes within the burst is linearly correlated with the duration of the preceding pause. Integrating the number of spikes over a fixed time window therefore leads to a total spike count that reflects the characteristic syllable-to-pause ratio of the species while being invariant to playing back the call faster or slower. Such a timescale-invariant recognition is essential under natural conditions, because grasshoppers do not thermoregulate; the call of a sender sitting in the shade will be slower than that of a grasshopper in the sun. Our results show that timescale-invariant stimulus recognition can be implemented at the single-cell level without directly calculating the ratio between pulse and interpulse durations.

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Auditory midbrain neurons that count

Cited by 121 publications

References 11 publications

Midbrain Auditory Neurons Integrate Excitation and Inhibition to Generate Duration Selectivity: AnIn VivoWhole-Cell Patch Study in Anurans

Midbrain Auditory Neurons Integrate Excitation and Inhibition to Generate Duration Selectivity: AnIn VivoWhole-Cell Patch Study in Anurans

Mechanisms of Temporal Auditory Pattern Recognition in Songbirds

Timescale-Invariant Representation of Acoustic Communication Signals by a Bursting Neuron

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