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An auditory feature detection circuit for sound pattern recognition.

Schöneich S, Kostarakos K, Hedwig B - Sci Adv (2015)

Bottom Line: We focused on acoustically communicating field crickets and show how five neurons in the brain of females form an auditory feature detector circuit for the pulse pattern of the male calling song.The processing is based on a coincidence detector mechanism that selectively responds when a direct neural response and an intrinsically delayed response to the sound pulses coincide.This circuit provides the basis for auditory mate recognition in field crickets and reveals a principal mechanism of sensory processing underlying the perception of temporal patterns.

View Article: PubMed Central - PubMed

Affiliation: Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK.

ABSTRACT
From human language to birdsong and the chirps of insects, acoustic communication is based on amplitude and frequency modulation of sound signals. Whereas frequency processing starts at the level of the hearing organs, temporal features of the sound amplitude such as rhythms or pulse rates require processing by central auditory neurons. Besides several theoretical concepts, brain circuits that detect temporal features of a sound signal are poorly understood. We focused on acoustically communicating field crickets and show how five neurons in the brain of females form an auditory feature detector circuit for the pulse pattern of the male calling song. The processing is based on a coincidence detector mechanism that selectively responds when a direct neural response and an intrinsically delayed response to the sound pulses coincide. This circuit provides the basis for auditory mate recognition in field crickets and reveals a principal mechanism of sensory processing underlying the perception of temporal patterns.

No MeSH data available.


Related in: MedlinePlus

Pulse interval sensitivity of LN3 and pulse interval selectivity of LN4.(A and C) Intracellular recordings (upper traces) of synaptic and spike activity in LN3 (A) and LN4 (C) upon stimulation (lower traces) with pairs of sound pulses with 60-, 20-, 5-, and 0-ms pulse intervals (PI). In both neurons, the EPSP and spike response to the second pulse were increased at a pulse interval of 20 ms; recordings were obtained from different specimens. Scale bar, 20 mV (LN3); 10 mV (LN4). (A) Gray arrows indicate delayed depolarization of LN3 with the peak always occurring 40 to 45 ms after the offset of the sound pulse. (C) For LN4, gray arrows indicate initial inhibition and black arrow indicates spiking. (B and D) Quantitative analysis of systematic paired-pulse stimulation. The spike responses of LN3 (B) (N = 7) and LN4 (D) (N = 4) to the first pulse are interval-independent; their spike responses to the second pulse are significantly increased for the 15- to 25-ms pulse intervals.
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Figure 3: Pulse interval sensitivity of LN3 and pulse interval selectivity of LN4.(A and C) Intracellular recordings (upper traces) of synaptic and spike activity in LN3 (A) and LN4 (C) upon stimulation (lower traces) with pairs of sound pulses with 60-, 20-, 5-, and 0-ms pulse intervals (PI). In both neurons, the EPSP and spike response to the second pulse were increased at a pulse interval of 20 ms; recordings were obtained from different specimens. Scale bar, 20 mV (LN3); 10 mV (LN4). (A) Gray arrows indicate delayed depolarization of LN3 with the peak always occurring 40 to 45 ms after the offset of the sound pulse. (C) For LN4, gray arrows indicate initial inhibition and black arrow indicates spiking. (B and D) Quantitative analysis of systematic paired-pulse stimulation. The spike responses of LN3 (B) (N = 7) and LN4 (D) (N = 4) to the first pulse are interval-independent; their spike responses to the second pulse are significantly increased for the 15- to 25-ms pulse intervals.

Mentions: We tested the temporal tuning of neurons LN3 and LN4 by challenging them with pairs of 20-ms sound pulses with varying pulse intervals. At a pulse interval of 60 ms, LN3 generated two similar and separate responses (Fig. 3, A and B). For each pulse, the membrane potential showed an initial depolarization driving a response of 1.8 ± 0.6 spikes/pulse (N = 7 each) and a delayed subthreshold depolarization. The initial depolarization results from a sequence of temporally summing small EPSPs, whereas the delayed depolarization appears to be a single EPSP with a larger amplitude and longer time course (fig. S1). For all intervals above 35 ms, each sound pulse elicited a similar response of 1 to 2 spikes (first versus second: P > 0.2 for each interval tested; N = 7). With a 20-ms interval, however, the delayed depolarization to the first sound pulse coincides with the initial depolarization elicited by the second pulse. As a consequence, the response significantly increases from 1.6 ± 0.5 spikes for the first pulse to 3.2 ± 0.3 spikes for the second pulse (first versus second: P < 0.001; t = 6.5; N = 7). For intervals below 10 ms, both responses merged, and a delayed depolarization only occurred after the second pulse. In contrast with the initial depolarization, the delayed depolarization was strictly coupled to the sound offset (see arrows in Fig. 3A) with a constant latency of 43.5 ± 2.4 ms (N = 4) for the depolarization maximum. The LN3 response to the second pulse was strongest, with 3.0 ± 0.5 spikes/pulse (N = 7) for intervals of 15 to 25 ms, corresponding to the pulse interval range of the species-specific song. On the basis of these data, LN3 qualifies as a coincidence detector; its band-pass sensitivity for interval duration is established by the summation of direct and delayed excitatory inputs, coupled to the sound pulse onset and offset, respectively.


An auditory feature detection circuit for sound pattern recognition.

Schöneich S, Kostarakos K, Hedwig B - Sci Adv (2015)

Pulse interval sensitivity of LN3 and pulse interval selectivity of LN4.(A and C) Intracellular recordings (upper traces) of synaptic and spike activity in LN3 (A) and LN4 (C) upon stimulation (lower traces) with pairs of sound pulses with 60-, 20-, 5-, and 0-ms pulse intervals (PI). In both neurons, the EPSP and spike response to the second pulse were increased at a pulse interval of 20 ms; recordings were obtained from different specimens. Scale bar, 20 mV (LN3); 10 mV (LN4). (A) Gray arrows indicate delayed depolarization of LN3 with the peak always occurring 40 to 45 ms after the offset of the sound pulse. (C) For LN4, gray arrows indicate initial inhibition and black arrow indicates spiking. (B and D) Quantitative analysis of systematic paired-pulse stimulation. The spike responses of LN3 (B) (N = 7) and LN4 (D) (N = 4) to the first pulse are interval-independent; their spike responses to the second pulse are significantly increased for the 15- to 25-ms pulse intervals.
© Copyright Policy - open-access
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4643773&req=5

Figure 3: Pulse interval sensitivity of LN3 and pulse interval selectivity of LN4.(A and C) Intracellular recordings (upper traces) of synaptic and spike activity in LN3 (A) and LN4 (C) upon stimulation (lower traces) with pairs of sound pulses with 60-, 20-, 5-, and 0-ms pulse intervals (PI). In both neurons, the EPSP and spike response to the second pulse were increased at a pulse interval of 20 ms; recordings were obtained from different specimens. Scale bar, 20 mV (LN3); 10 mV (LN4). (A) Gray arrows indicate delayed depolarization of LN3 with the peak always occurring 40 to 45 ms after the offset of the sound pulse. (C) For LN4, gray arrows indicate initial inhibition and black arrow indicates spiking. (B and D) Quantitative analysis of systematic paired-pulse stimulation. The spike responses of LN3 (B) (N = 7) and LN4 (D) (N = 4) to the first pulse are interval-independent; their spike responses to the second pulse are significantly increased for the 15- to 25-ms pulse intervals.
Mentions: We tested the temporal tuning of neurons LN3 and LN4 by challenging them with pairs of 20-ms sound pulses with varying pulse intervals. At a pulse interval of 60 ms, LN3 generated two similar and separate responses (Fig. 3, A and B). For each pulse, the membrane potential showed an initial depolarization driving a response of 1.8 ± 0.6 spikes/pulse (N = 7 each) and a delayed subthreshold depolarization. The initial depolarization results from a sequence of temporally summing small EPSPs, whereas the delayed depolarization appears to be a single EPSP with a larger amplitude and longer time course (fig. S1). For all intervals above 35 ms, each sound pulse elicited a similar response of 1 to 2 spikes (first versus second: P > 0.2 for each interval tested; N = 7). With a 20-ms interval, however, the delayed depolarization to the first sound pulse coincides with the initial depolarization elicited by the second pulse. As a consequence, the response significantly increases from 1.6 ± 0.5 spikes for the first pulse to 3.2 ± 0.3 spikes for the second pulse (first versus second: P < 0.001; t = 6.5; N = 7). For intervals below 10 ms, both responses merged, and a delayed depolarization only occurred after the second pulse. In contrast with the initial depolarization, the delayed depolarization was strictly coupled to the sound offset (see arrows in Fig. 3A) with a constant latency of 43.5 ± 2.4 ms (N = 4) for the depolarization maximum. The LN3 response to the second pulse was strongest, with 3.0 ± 0.5 spikes/pulse (N = 7) for intervals of 15 to 25 ms, corresponding to the pulse interval range of the species-specific song. On the basis of these data, LN3 qualifies as a coincidence detector; its band-pass sensitivity for interval duration is established by the summation of direct and delayed excitatory inputs, coupled to the sound pulse onset and offset, respectively.

Bottom Line: We focused on acoustically communicating field crickets and show how five neurons in the brain of females form an auditory feature detector circuit for the pulse pattern of the male calling song.The processing is based on a coincidence detector mechanism that selectively responds when a direct neural response and an intrinsically delayed response to the sound pulses coincide.This circuit provides the basis for auditory mate recognition in field crickets and reveals a principal mechanism of sensory processing underlying the perception of temporal patterns.

View Article: PubMed Central - PubMed

Affiliation: Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK.

ABSTRACT
From human language to birdsong and the chirps of insects, acoustic communication is based on amplitude and frequency modulation of sound signals. Whereas frequency processing starts at the level of the hearing organs, temporal features of the sound amplitude such as rhythms or pulse rates require processing by central auditory neurons. Besides several theoretical concepts, brain circuits that detect temporal features of a sound signal are poorly understood. We focused on acoustically communicating field crickets and show how five neurons in the brain of females form an auditory feature detector circuit for the pulse pattern of the male calling song. The processing is based on a coincidence detector mechanism that selectively responds when a direct neural response and an intrinsically delayed response to the sound pulses coincide. This circuit provides the basis for auditory mate recognition in field crickets and reveals a principal mechanism of sensory processing underlying the perception of temporal patterns.

No MeSH data available.


Related in: MedlinePlus