BILATERAL COLLICULAR INTERACTION: MODULATION OF AUDITORY SIGNAL PROCESSING IN FREQUENCY DOMAIN L. CHENG, a1 H.-X. MEI, a1 J. TANG, a1 Z.-Y. FU, a P. H.-S. JEN b * AND Q.-C. CHEN a * a School of Life Sciences & Hubei Key Lab of Genetic Regulation and Integrative Biology, Central China Normal University, Wuhan 430079, China b Division of Biological Sciences, University of Missouri-Columbia, MO 65211, USA Abstract—In the ascending auditory pathway, the inferior col- liculus (IC) receives and integrates excitatory and inhibitory inputs from a variety of lower auditory nuclei, intrinsic projec- tions within the IC, contralateral IC through the commissure of the IC and the auditory cortex. All these connections make the IC a major center for subcortical temporal and spectral integration of auditory information. In this study, we examine bilateral collicular interaction in the modulation of frequency- domain signal processing of mice using electrophysiological recording and focal electrical stimulation. Focal electrical stimulation of neurons in one IC produces widespread inhibi- tion and focused facilitation of responses of neurons in the other IC. This bilateral collicular interaction decreases the response magnitude and lengthens the response latency of inhibited IC neurons but produces an opposite effect on the response of facilitated IC neurons. In the frequency domain, the focal electrical stimulation of one IC sharpens or expands the frequency tuning curves (FTCs) of neurons in the other IC to improve frequency sensitivity and the frequency response range. The focal electrical stimulation also produces a shift in the best frequency (BF) of modulated IC (IC Mdu ) neurons toward that of electrically stimulated IC (IC ES ) neurons. The degree of bilateral collicular interaction is dependent upon the difference in the BF between the IC ES neurons and IC Mdu neurons. These data suggest that bilateral collicular interac- tion is a part of dynamic acoustic signal processing that adjusts and improves signal processing as well as reorga- nizes collicular representation of signal parameters accord- ing to the acoustic experience. Ó 2013 IBRO. Published by Elsevier Ltd. All rights reserved. Key words: focal electrical stimulation, bilateral collicular interaction, frequency processing, neural plasticity, mice. INTRODUCTION In nature, communication sounds among animal species including humans are typical complex sounds that are composed of a complex spectro-temporal structure which varies in several parameters including amplitude, frequency and duration. To effectively analyze these signal parameters, central auditory neurons are selectively tuned to these various signal parameters that characterize the biologically relevant complex sounds. Among all these multiple parametric selectivity, frequency selectivity of auditory neurons is essential for fine frequency analysis that underlies pitch perception of any animal species. Traditionally, a neuron’s frequency selectivity is studied by measuring its threshold- or impulse-frequency tuning curve (FTC) in which a neuron’s frequency selectivity is shown by its lowest threshold or maximal number of impulses to the best tuned frequency (BF). In the ascending auditory pathway, the inferior colliculus (IC) receives and integrates excitatory and inhibitory inputs from almost all lower auditory nuclei, intrinsic projections within the IC, contralateral IC through the commisure of the IC and from the auditory cortex (Adams, 1979; Aitkin and Phillips, 1984; Shneiderman and Oliver, 1989; Huffman and Henson, 1990; Herbert et al., 1991; Saldan˜a and Mercha´n, 1992; Malmierca et al., 1995, 2003, 2005b; Saldan˜a et al., 1996; Winer et al., 1998; Casseday et al., 2002; Bajo and Moore, 2005; Cant and Benson, 2006; Herna´ndez et al., 2006; Winer, 2006). As such, the IC is a major center for subcortical temporal and spectral integration of auditory information and many studies have examined multiple-parametric selectivity of neurons in the IC. In the frequency domain, these studies have shown that the sharpness of a neuron’s FTC is primarily shaped through the interplay between excitation and inhibition both in the ascending and descending auditory pathways (Jen et al., 1998; Koch and Grothe, 1998; Lu and Jen, 2001; Jen and Zhou, 2003; Yan et al., 2005; Zhou and Jen, 2007). Other studies of colliculo– collicular interaction within the same IC have shown that acoustically or electrically stimulating an IC neuron sharpens the FTC or shifts the BF of neighboring IC neurons (Jen et al., 2002a; Zhang and Suga, 2005; Wu and Jen, 2008, 2009). As for colliculo–collicular (bilateral collicular) interaction between the two ICs, two studies show that the bilateral collicular interaction modulates frequency response area, number of impulses and monotonicity of IC neurons (Malmierca et al., 2003, 2005a). However, 0306-4522/12 $36.00 Ó 2013 IBRO. Published by Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.neuroscience.2013.01.011 * Corresponding authors. Tel: +1-573-882-7479; fax: +1-573-884- 5020 (P. H. -S. Jen). Tel: +86-27-67867229; fax: +86-27-67861936 (Q. -C. Chen). E-mail addresses: Jenp@missouri.edu (P. H.-S. Jen), qcche- n2003@yahoo.com.cn (Q.-C. Chen). 1 These authors contributed equally to this work. Abbreviations: ANOVA, analysis of variance; BF, best frequency; dB SPL, decibel sound pressure level; EI, excitatory–inhibitory binaural interaction; FTC, frequency tuning curve; IC, inferior colliculus; IC ES , electrically stimulated IC; IC Mdu , modulated IC; IPI, inter-pulse interval; MT, minimum threshold; PST, peri-stimulus-time; Q 10 , ratio between bandwidth of FTC in 10 dB above MT and BF. Neuroscience 235 (2013) 27–39 27