Neural timing of stimulus events with microsecond precision

Jinhong Luo; Silvio Macias; Torbjørn V Ness; Gaute T Einevoll; Kechen Zhang; Cynthia F Moss

doi:10.1371/journal.pbio.2006422

Neural timing of stimulus events with microsecond precision

PLoS Biol. 2018 Oct 26;16(10):e2006422. doi: 10.1371/journal.pbio.2006422. eCollection 2018 Oct.

Authors

Jinhong Luo¹, Silvio Macias¹, Torbjørn V Ness², Gaute T Einevoll^{2

3}, Kechen Zhang⁴, Cynthia F Moss¹

Affiliations

¹ Department of Psychological and Brain Sciences, Johns Hopkins University, Baltimore, Maryland, United States of America.
² Faculty of Science and Technology, Norwegian University of Life Sciences, Ås, Norway.
³ Department of Physics, University of Oslo, Oslo, Norway.
⁴ Department of Biomedical Engineering, Johns Hopkins School of Medicine, Baltimore, Maryland, United States of America.

Abstract

Temporal analysis of sound is fundamental to auditory processing throughout the animal kingdom. Echolocating bats are powerful models for investigating the underlying mechanisms of auditory temporal processing, as they show microsecond precision in discriminating the timing of acoustic events. However, the neural basis for microsecond auditory discrimination in bats has eluded researchers for decades. Combining extracellular recordings in the midbrain inferior colliculus (IC) and mathematical modeling, we show that microsecond precision in registering stimulus events emerges from synchronous neural firing, revealed through low-latency variability of stimulus-evoked extracellular field potentials (EFPs, 200-600 Hz). The temporal precision of the EFP increases with the number of neurons firing in synchrony. Moreover, there is a functional relationship between the temporal precision of the EFP and the spectrotemporal features of the echolocation calls. In addition, EFP can measure the time difference of simulated echolocation call-echo pairs with microsecond precision. We propose that synchronous firing of populations of neurons operates in diverse species to support temporal analysis for auditory localization and complex sound processing.

Publication types

Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Acoustic Stimulation
Animals
Auditory Pathways / physiology
Auditory Perception / physiology*
Biophysical Phenomena
Chiroptera / anatomy & histology
Chiroptera / physiology*
Computer Simulation
Echolocation / physiology
Evoked Potentials, Auditory / physiology
Female
Inferior Colliculi / cytology
Inferior Colliculi / physiology
Male
Models, Neurological
Neurons / physiology
Sound Localization / physiology
Time Perception / physiology*

Grants and funding

National Science Foundation (grant number IOS-1010193; IOS-1460149; IOS-1734744). CFM. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Human Frontiers Science Program (grant number RGP0040). CFM. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Office of Naval Research (grant number N00014-12-1-0339; N00014-17-1-2736). CFM. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Air Force Office of Scientific Research (grant number FA9550-14-1-0398). CFM. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Human Frontier Science Program (grant number LT000279/2016-L). JL. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. European Union Horizon 2020 Research and Innovation Programme (grant number 720270 and 785907). TVN and GTE. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.