Abstract

Echolocating bats rely upon spectral interference patterns in echoes to reconstruct fine details of a reflecting object’s shape. However, the acoustic modulations required to do this are extremely brief, raising questions about how their auditory cortex encodes and processes such rapid and fine spectrotemporal details. Here, we tested the hypothesis that biosonar target shape representation in the primary auditory cortex (A1) is more reliably encoded by changes in spike timing (latency) than spike rates and that latency is sufficiently precise to support a synchronization-based ensemble representation of this critical auditory object feature space. To test this, we measured how the spatiotemporal activation patterns of A1 changed when naturalistic spectral notches were inserted into echo mimic stimuli. Neurons tuned to notch frequencies were predicted to exhibit longer latencies and lower mean firing rates due to lower signal amplitudes at their preferred frequencies, and both were found to occur. Comparative analyses confirmed that significantly more information was recoverable from changes in spike times relative to concurrent changes in spike rates. With this data, we reconstructed spatiotemporal activation maps of A1 and estimated the level of emerging neuronal spike synchrony between cortical neurons tuned to different frequencies. The results support existing computational models, indicating that spectral interference patterns may be efficiently encoded by a cascading tonotopic sequence of neural synchronization patterns within an ensemble of network activity that relates to the physical features of the reflecting object surface.

Highlights

  • Rate-coding and time-coding strategies are both present in mammalian auditory cortex [1], but the relative costs and benefits of either are still poorly understood, and it is reasonable to predict that the mechanisms and contributions of both are likely to differ across animals and behavioral context [2]

  • The characteristic frequency (CF) of this neuron was 25 kHz with a minimum threshold of 30-dB sound pressure level (SPL)

  • Mean first-spike latency (FSL) measured at the CF at 80 dB SPL ranged between 10 and 35 ms

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Summary

Introduction

Rate-coding and time-coding strategies are both present in mammalian auditory cortex [1], but the relative costs and benefits of either are still poorly understood, and it is reasonable to predict that the mechanisms and contributions of both are likely to differ across animals and behavioral context [2]. We used the A1 of the Mexican free-tailed bat, Tadarida brasiliensis, as a model to investigate how spectral shape modulates the spatiotemporal patterns of neuronal activation along the tonotopic axis of A1 and evaluated whether temporal or rate-coding mechanisms, or a combination of both, provided the information needed to support encoding of biosonar target shapes. The current literature base falls far short of explaining how auditory cortex performs many basic functions, such as how the central auditory system balances the trade-off between temporal and spectral acuity Specialized systems such as bat biosonar offer clear opportunities to define how general mechanisms can be adapted to perform specialized computation processes. The results potentially have both biomedical and engineering implications, which add to its long-term impacts

Results
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