Bidirectional Shifting Effects of the Sound Intensity on the Best Frequency in the Rat Auditory Cortex

Can Tao,Ying Xiong,Yi Zhou,Guangwei Zhang,Sumei Yan,Chang Zhou,Lijuan Wang

doi:10.1038/srep44493

Abstract

Frequency and intensity are two independent attributes of sound stimuli. Psychoacoustic studies have found that the sound intensity can affect the perception of frequency; however, the underlying neuronal mechanism remains largely unknown. To investigate if and how the sound level affects the frequency coding for auditory cortical neurons, we recorded the activities of neuronal ensembles and single neurons, as well as the synaptic input evoked by pure tones of different frequency and intensity combinations, in layer 4 of the rat primary auditory cortex. We found that the best frequency (BF) shifted bidirectionally with the increases in intensity. Specifically, the BF of neurons with a low characteristic frequency (CF) shifted lower, whereas the BF of neurons with a higher CF shifted higher. Meanwhile, we found that these shifts in the BF can lead to the expansion of high- and low-frequency areas in the tonotopic map, increasing the evenness of the BF distribution at high intensities. Our results revealed that the frequency tuning can bidirectionally shift with an increase in the sound intensity at both the cellular and population level. This finding is consistent with the perceptual illusions observed in humans and could provide a potential mechanism for this psychoacoustic effect.

Highlights

Frequency and intensity are two basic aspects of sound information
We first conducted in vivo multiunit extracellular recordings between 420 μm to 450 μm, which corresponds to layer 4 (L4) in A1, in anesthetized rats (Fig. 1A, see the Methods for details) to obtain the Tonal receptive fields (TRFs) of neuronal ensembles
The frequency preferences of the entire A1 region can be mapped based on the characteristic frequency (CF) of each recording site, producing what is known as a tonotopic map (Fig. 1B)

Summary

Introduction

Frequency and intensity are two basic aspects of sound information. The frequency determines whether a pure tone sounds “high” or “low”[1,2,3], and the accurate perception of frequency allows an animal to process a sound signal, evaluate the degree of risk and decide whether to run or fight. In 1935, Steven reported that a tone may sound somewhat lower or higher with an increase in intensity, and this is called Steven’s rule[6] This result suggested that the perception of frequency and intensity are not independent. The primary auditory cortex can either faithfully inherit the ascending information from the thalamus[17] or can enhance or depress specialized functions through local circuits[18,19,20,21,22] Both excitatory and inhibitory synaptic inputs can contribute to the final response of the A1. We observed a significant shift in best frequency (BF) with the increasing intensity for both neuronal ensembles and individual neurons in the primary auditory cortex of both urethane-anesthetized and awake rats This shift in the BF was bidirectional. Our results demonstrate the influence of sound pressure on the frequency at the single neuron and population level in the primary auditory cortex

Methods

Results

Conclusion