Research ArticleBEHAVIORAL NEUROSCIENCE

An auditory feature detection circuit for sound pattern recognition

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Science Advances  11 Sep 2015:
Vol. 1, no. 8, e1500325
DOI: 10.1126/sciadv.1500325
  • Fig. 1 Pulse period recognition by a delay line and coincidence detection mechanism.

    Flow diagram based on the concept of Reiss (19) and Weber and Thorson (20) for the sequence of auditory processing; the first sound pulse entering the auditory pathway is indicated by an asterisk. See the text for detailed explanation.

  • Fig. 2 Typical responses of auditory neurons to the pulse pattern of calling song chirps.

    (Top) Intracellular recordings (upper trace) and acoustic stimulation (lower trace); AN1 and LN2-LN4 are spiking neurons and LN5 is a nonspiking neuron. In the LN4 recording, gray arrow indicates initial inhibition and black arrows indicate spikes. Scale bar, 35 mV (AN1); 25 mV (LN2); 5 mV (LN5); 20 mV (LN3); 10 mV (LN4). (Bottom) The diagrams of spiking neurons show poststimulus time histograms (colored bar charts) and average spike frequency (black line) in response to artificial standard chirps (n = 50 each) with a sound frequency of 4.8 kHz. AN1 and LN2 copy the sound pattern, with the strongest spike response to the first pulse of the chirp. LN3 and LN4 respond most strongly to the second pulse (asterisks). Depolarizing current injection fails to elicit spiking in LN5, which confirms that it is a nonspiking interneuron. Neuron recordings were obtained from different specimens and are aligned to the start of the sound stimulus.

  • Fig. 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.

  • Fig. 4 Nonspiking interneuron LN5 generates a delayed excitatory response by PIR depolarization.

    (A) Confocal image of LN5. Neurite arborizations are in the immediate vicinity of AN1 terminals in the brain (see also figs. S2 and S3 for more details). In the inset, only the left AN1 and the right LN5 are depicted to indicate the location of the neurons in the brain. (B) Intensity-invariant responses to 20-ms sound pulses of 55, 65, and 75 dB SPL (signal averages, n = 5). (C) Rebound depolarization after a 20-ms injection of −3 nA intracellular current (signal average, n = 20). (D and E) For sound and current pulses of different duration, the rebound is always time-coupled to the sound offset (D) or the release from hyperpolarization (E) (signal averages, n = 5).

  • Fig. 5 Circuitry and processing mechanism of the auditory feature detector network.

    (A) Circuitry based on the response properties and the latency of neural responses. Triangular and rectangular symbols indicate excitatory and inhibitory synapses, respectively. (B and C) The typical responses of the five auditory neurons are aligned to the onset of a single (B) and a pair (C) of sound pulses with a 20-ms pulse interval. (B) AN1 spiking is immediately followed by a fast depolarization of LN2 and a gradually increasing depolarization in LN3 (first dashed line). Inhibition in LN4 and LN5 follows the spike activity of LN2 with short latency (second dashed line). The timing of the PIR depolarization in LN5 corresponds to the delayed EPSP in LN3 (blue arrow). The spike activity in LN3 precedes the excitatory response in LN4. (C) The LN3 response is enhanced for a second sound pulse presented after an interval of 20 ms as the direct (via AN1) and delayed (via LN5) excitatory inputs coincide. Driven by a stronger LN3 activity, LN4 now overcomes its inhibition and spikes (black arrow). Scale bar, 35 mV (AN1); 25 mV (LN2); 5 mV (LN5); 20 mV (LN3); 10 mV (LN4). Neural response patterns were recorded in different specimens and are aligned to the start of the sound stimulus.

  • Fig. 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.

Supplementary Materials

  • Supplementary material for this article is available at http://advances.sciencemag.org/cgi/content/full/1/8/e1500325/DC1

    Table S1. Summary of key properties of the six synaptic connections in the proposed circuit.

    Fig. S1. Processing of AN1 spike activity by LN2 and LN3.

    Fig. S2. Confocal whole-mount scans of AN1 and LN3.

    Fig. S3. Confocal whole-mount scans of an LN5 neuron labeled with Lucifer yellow.

    Fig. S4. LN5 responses to the standard chirp pattern.

    Fig. S5. Sound intensity–invariant responses of delay-line neurons LN2 and LN5.

    Fig. S6. Mean threshold curves for spiking responses of AN1, AN2, LN2, and LN3 and for synaptic responses of LN3, LN4, and LN5.

    Fig. S7. AN1 spike activity and LN5 PIR.

  • Supplementary Materials

    This PDF file includes:

    • Table S1. Summary of key properties of the six synaptic connections in the proposed circuit.
    • Fig. S1. Processing of AN1 spike activity by LN2 and LN3.
    • Fig. S2. Confocal whole-mount scans of AN1 and LN3.
    • Fig. S3. Confocal whole-mount scans of an LN5 neuron labeled with Lucifer yellow.
    • Fig. S4. LN5 responses to the standard chirp pattern.
    • Fig. S5. Sound intensity–invariant responses of delay-line neurons LN2 and LN5.
    • Fig. S6. Mean threshold curves for spiking responses of AN1, AN2, LN2, and LN3 and for synaptic responses of LN3, LN4, and LN5.
    • Fig. S7. AN1 spike activity and LN5 PIR.

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