Auditory Cortical Areas Activated by Slow Frequency-Modulated Sounds in Mice

Yuusuke Honma,Masao Horie,Ryuichi Hishida,Katsuei Shibuki,Sugata Takahashi,Yamato Kubota,Manavu Tohmi,Kuniyuki Takahashi,Hiroaki Tsukano,Shinsuke Ohshima,Li I Zhang

doi:10.1371/journal.pone.0068113

Abstract

Species-specific vocalizations in mice have frequency-modulated (FM) components slower than the lower limit of FM direction selectivity in the core region of the mouse auditory cortex. To identify cortical areas selective to slow frequency modulation, we investigated tonal responses in the mouse auditory cortex using transcranial flavoprotein fluorescence imaging. For differentiating responses to frequency modulation from those to stimuli at constant frequencies, we focused on transient fluorescence changes after direction reversal of temporally repeated and superimposed FM sweeps. We found that the ultrasonic field (UF) in the belt cortical region selectively responded to the direction reversal. The dorsoposterior field (DP) also responded weakly to the reversal. Regarding the responses in UF, no apparent tonotopic map was found, and the right UF responses were significantly larger in amplitude than the left UF responses. The half-max latency in responses to FM sweeps was shorter in UF compared with that in the primary auditory cortex (A1) or anterior auditory field (AAF). Tracer injection experiments in the functionally identified UF and DP confirmed that these two areas receive afferent inputs from the dorsal part of the medial geniculate nucleus (MG). Calcium imaging of UF neurons stained with fura-2 were performed using a two-photon microscope, and the presence of UF neurons that were selective to both direction and direction reversal of slow frequency modulation was demonstrated. These results strongly suggest a role for UF, and possibly DP, as cortical areas specialized for processing slow frequency modulation in mice.

Highlights

Animal vocalizations have FM components that are essential for vocal communication [1], [2], [3]
The fluorescence responses to the FM sounds were observed in the belt region that include ultrasonic field (UF) and dorsoposterior field (DP), which has been identified as areas adjacent to anterior auditory field (AAF) and A1 using electrophysiological recordings [22]
Cortical responses to a FM sweep are transient in nature, and such transient responses might not be reflected in flavoprotein fluorescence signals

Summary

Introduction

Animal vocalizations have FM components that are essential for vocal communication [1], [2], [3]. Rodents can discriminate direction of FM sweeps as slow as a few kilohertz per second, while lesions of the auditory cortex reduce the discrimination abilities [19], [20], [21]. FM-responsive neurons are found in the core region and in the belt region including UF and DP [22]. It is unclear whether these cortical areas selectively respond to slow FM sweeps. To clarify this point, cortical responses to frequency modulation in slow FM sweeps have to be differentiated from those to tonal stimuli at constant frequencies within the FM range

Methods

Results

Conclusion