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Differential neural coding of acoustic flutter within primate auditory cortex

Abstract

A sequence of acoustic events is perceived either as one continuous sound or as a stream of temporally discrete sounds (acoustic flutter), depending on the rate at which the acoustic events repeat. Acoustic flutter is perceived at repetition rates near or below the lower limit for perceiving pitch, and is akin to the discrete percepts of visual flicker and tactile flutter caused by the slow repetition of sensory stimulation. It has been shown that slowly repeating acoustic events are represented explicitly by stimulus-synchronized neuronal firing patterns in primary auditory cortex (AI). Here we show that a second neural code for acoustic flutter exists in the auditory cortex of marmoset monkeys (Callithrix jacchus), in which the firing rate of a neuron is a monotonic function of an acoustic event's repetition rate. Whereas many neurons in AI encode acoustic flutter using a dual temporal/rate representation, we find that neurons in cortical fields rostral to AI predominantly use a monotonic rate code and lack stimulus-synchronized discharges. These findings indicate that the neural representation of acoustic flutter is transformed along the caudal-to-rostral axis of auditory cortex.

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Figure 1: Stimulus synchronization to acoustic pulse trains.
Figure 2: Monotonic response properties.
Figure 3: Examples of positive and negative monotonic synchronized responses.
Figure 4: Examples of positive and negative monotonic unsynchronized responses.
Figure 5: Temporal response dynamics of synchronized and unsynchronized neurons.
Figure 6: Flutter rate codes are insensitive to temporal irregularity.
Figure 7: Comparison of the proportion of response types by cortical region.
Figure 8: Sound-level invariance in monotonic rate-coding neurons.

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Acknowledgements

Support was contributed by US National Institutes of Health grants DC 03180 (X.W.) and F31 DC 006528 (D.B.). We thank A. Pistorio for assistance with animal care and Y. Zhou for valuable comments and suggestions related to this manuscript.

Author information

Authors and Affiliations

Authors

Contributions

D.B. and X.W. designed the experiment and co-wrote the paper. D.B. carried out the electrophysiological recordings and data analysis.

Corresponding authors

Correspondence to Daniel Bendor or Xiaoqin Wang.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Fig. 1

Description of acoustic stimulus set. (PDF 141 kb)

Supplementary Fig. 2

Individual monotonic responses. (PDF 73 kb)

Supplementary Fig. 3

Additional examples of monotonic unsynchronized neurons. (PDF 511 kb)

Supplementary Fig. 4

Single neuron examples of non-monotonic responses. (PDF 99 kb)

Supplementary Fig. 5

Area comparison of stimulus synchronization and peak response latencies. (PDF 76 kb)

Supplementary Fig. 6

Sound level dependent changes in the response slopes of monotonic neurons. (PDF 76 kb)

Supplementary Table 1

Number of neurons for each response type by cortical region. (PDF 101 kb)

Supplementary Audio 1

Acoustic pulse train within the perceptual range of flutter. Audio file (.wav) of a 1 second long acoustic pulse train (Gaussian narrowband pulse, 3 kHz carrier frequency, σ = 0.89) with a repetition rate of 25 Hz. (WAV 293 kb)

Supplementary Audio 2

Acoustic pulse train above the perceptual range of flutter. Audio file (.wav) of a 1 second long acoustic pulse train (Gaussian narrowband pulse, 3 kHz carrier frequency, σ = 0.89) with a repetition rate of 60 Hz. (WAV 293 kb)

Supplementary Audio 3

Acoustic pulse train below the perceptual range of flutter. Audio file (.wav) of a 1 second long acoustic pulse train (Gaussian narrowband pulse, 3 kHz carrier frequency, σ = 0.89) with a repetition rate of 5 Hz. (WAV 293 kb)

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Bendor, D., Wang, X. Differential neural coding of acoustic flutter within primate auditory cortex. Nat Neurosci 10, 763–771 (2007). https://doi.org/10.1038/nn1888

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