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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.


The tuning of LN3 and LN4 results from the timing of AN1 and LN5 excitation and matches the phonotactic behavior.(A) Response tuning of the coincidence detector LN3 (N = 10), the feature detector LN4 (N = 5), and the phonotactic behavior (N = 14) toward chirps with different pulse periods but constant sound energy (26). (B to G) Instantaneous spike rate of AN1 (red area; average n = 10) and changes in the membrane potential of LN5 (blue trace; signal average, n = 5) for chirps from the same paradigm as used in (A). Both interneurons were recorded subsequently in the same animal, independent of phonotaxis tests. See fig. S7 for m3ore details.
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Figure 6: The tuning of LN3 and LN4 results from the timing of AN1 and LN5 excitation and matches the phonotactic behavior.(A) Response tuning of the coincidence detector LN3 (N = 10), the feature detector LN4 (N = 5), and the phonotactic behavior (N = 14) toward chirps with different pulse periods but constant sound energy (26). (B to G) Instantaneous spike rate of AN1 (red area; average n = 10) and changes in the membrane potential of LN5 (blue trace; signal average, n = 5) for chirps from the same paradigm as used in (A). Both interneurons were recorded subsequently in the same animal, independent of phonotaxis tests. See fig. S7 for m3ore details.

Mentions: To relate the tuning mechanisms of the circuit to the band-pass tuning of the phonotactic behavior, we analyzed the neuronal responses to artificial chirps with different pulse periods (Fig. 6 and fig. S7), a standard test to characterize the phonotactic behavior (16, 17, 26). When tested for pulse periods ranging from 10 to 98 ms (PP10 to PP98), the phonotactic response exhibited clear band-pass selectivity with the maximum around PP34. This is closely reflected by the spike responses of the coincidence detector LN3 and the feature detector LN4 (Fig. 6A). The response of the coincidence detector LN3 depended on the relative timing and amplitude of the direct input from AN1 and the delayed excitation from LN5. For recordings subsequently obtained in the same animals, we therefore analyzed the spike activity of AN1 and the changes in the membrane potential of LN5 in response to chirps that either elicit strong phonotaxis (Fig. 6, D and E) or are phonotactically unattractive (Fig. 6, B, C, F, and G). For attractive pulse periods from PP34 to PP42 (17- to 21-ms intervals), the depolarization of LN5 and the spike response in AN1 are in phase and occur at the same time beginning from the second pulse onward (Fig. 6, D and E). For unattractive pulse periods of PP66 to PP98 (33- to 49-ms intervals), the AN1 response and PIR of LN5 drift out of phase (Fig. 6, F and G), and therefore, direct and delayed excitatory inputs do not add up in the coincidence detector LN3. This mechanism establishes a high-pass filter. At pulse periods below PP34 (interval shorter than 17 ms), the PIR in LN5 elicited by a sound pulse becomes increasingly reduced as it is truncated and diminished by the inhibition in response to the subsequent pulse. Additionally, AN1 activity increasingly habituates and fails to copy the fast pulse pattern in its spike activity, thereby reducing the direct input to the coincidence detector and, indirectly, the phasic inhibition of LN5 that is essential to drive its PIR (Fig. 6, B and C). These properties establish a very effective low-pass filter. Therefore, two different processing mechanisms define the band-pass selectivity of the circuit for pulse periods.


An auditory feature detection circuit for sound pattern recognition.

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

The tuning of LN3 and LN4 results from the timing of AN1 and LN5 excitation and matches the phonotactic behavior.(A) Response tuning of the coincidence detector LN3 (N = 10), the feature detector LN4 (N = 5), and the phonotactic behavior (N = 14) toward chirps with different pulse periods but constant sound energy (26). (B to G) Instantaneous spike rate of AN1 (red area; average n = 10) and changes in the membrane potential of LN5 (blue trace; signal average, n = 5) for chirps from the same paradigm as used in (A). Both interneurons were recorded subsequently in the same animal, independent of phonotaxis tests. See fig. S7 for m3ore details.
© Copyright Policy - open-access
Related In: Results  -  Collection

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Figure 6: The tuning of LN3 and LN4 results from the timing of AN1 and LN5 excitation and matches the phonotactic behavior.(A) Response tuning of the coincidence detector LN3 (N = 10), the feature detector LN4 (N = 5), and the phonotactic behavior (N = 14) toward chirps with different pulse periods but constant sound energy (26). (B to G) Instantaneous spike rate of AN1 (red area; average n = 10) and changes in the membrane potential of LN5 (blue trace; signal average, n = 5) for chirps from the same paradigm as used in (A). Both interneurons were recorded subsequently in the same animal, independent of phonotaxis tests. See fig. S7 for m3ore details.
Mentions: To relate the tuning mechanisms of the circuit to the band-pass tuning of the phonotactic behavior, we analyzed the neuronal responses to artificial chirps with different pulse periods (Fig. 6 and fig. S7), a standard test to characterize the phonotactic behavior (16, 17, 26). When tested for pulse periods ranging from 10 to 98 ms (PP10 to PP98), the phonotactic response exhibited clear band-pass selectivity with the maximum around PP34. This is closely reflected by the spike responses of the coincidence detector LN3 and the feature detector LN4 (Fig. 6A). The response of the coincidence detector LN3 depended on the relative timing and amplitude of the direct input from AN1 and the delayed excitation from LN5. For recordings subsequently obtained in the same animals, we therefore analyzed the spike activity of AN1 and the changes in the membrane potential of LN5 in response to chirps that either elicit strong phonotaxis (Fig. 6, D and E) or are phonotactically unattractive (Fig. 6, B, C, F, and G). For attractive pulse periods from PP34 to PP42 (17- to 21-ms intervals), the depolarization of LN5 and the spike response in AN1 are in phase and occur at the same time beginning from the second pulse onward (Fig. 6, D and E). For unattractive pulse periods of PP66 to PP98 (33- to 49-ms intervals), the AN1 response and PIR of LN5 drift out of phase (Fig. 6, F and G), and therefore, direct and delayed excitatory inputs do not add up in the coincidence detector LN3. This mechanism establishes a high-pass filter. At pulse periods below PP34 (interval shorter than 17 ms), the PIR in LN5 elicited by a sound pulse becomes increasingly reduced as it is truncated and diminished by the inhibition in response to the subsequent pulse. Additionally, AN1 activity increasingly habituates and fails to copy the fast pulse pattern in its spike activity, thereby reducing the direct input to the coincidence detector and, indirectly, the phasic inhibition of LN5 that is essential to drive its PIR (Fig. 6, B and C). These properties establish a very effective low-pass filter. Therefore, two different processing mechanisms define the band-pass selectivity of the circuit for pulse periods.

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.