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Auditory Frequency-Following Responses in Rat Ipsilateral Inferior Colliculus

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Auditory Frequency-Following Responses in Rat Ipsilateral Inferior Colliculus AUDITORYAND VESTIBULAR SYSTEMS NEUROREPORT Auditory frequency-following responses in rat ipsilateral inferior colliculus Junli Pinga,NanxinLia, Gary C. Galbraithb,c, Xihong Wua,b and Liang Lia,b aDepartment of Psychology,Key Laboratory on Machine Perception (Ministry of Education), bSpeech and Hearing Research Center,Peking University, Beijing, China and cMental Retardation Research Center,Department of Psychiatry and Biobehavioral Sciences, David Ge¡en School of Medicine, University of California, Los Angeles, USA Correspondence to Dr Liang Li, PhD,Department of Psychology,Peking University,Beijing,100871,China Tel: +8610 6275 6804; fax: +8610 62761081; e-mail: [email protected] Received 9 May 2008; accepted 9 June 2008 DOI: 10.1097/WNR.0b013e32830c1c fa Auditory frequency-following responses (FFRs) are sustained ipsilaterally driven FFRs, which, however, were signi¢cantly potentials based on phase-locked neural activity preserving low- enhancedby blocking the contralateral dorsal nucleus of the lateral frequency information. Some neurons in rat inferior colliculus are lemniscus. Thus, FFRs in inferior colliculus to ipsilateral stimulation excited by stimuli at either ear.This study shows that FFRs in infer- were facilitated by excitatory projections from the contralateral ior colliculus can be elicited by presenting pure tone bursts with inferior colliculus but suppressed by inhibitory projections from frequencies from 225 to 4025 Hz at the ipsilateral ear in anesthe- the contralateral dorsal nucleus of the lateral lemniscus. tized rats. Moreover, chemical block of glutamate transmissions NeuroReport 19 :137 7^13 8 0 c 2008 Wolters Kluwer Health | in the contralateral inferior colliculus markedly reduced the Lippincott Williams & Wilkins. Keywords: dorsal nucleus of lateral lemniscus, frequency-following response, g-aminobutyric acid, glutamate, inferior colliculus, kynurenic acid Introduction were studied by microinjecting the broad-spectrum gluta- The frequency-following response (FFR) is a short latency mate receptor blocker kynurenic acid (KYNA) into the response that mimics many acoustic waveform properties contralateral central nucleus of the inferior colliculus and [1,2]. Human studies show that the FFR can be affected by the contralateral dorsal nucleus of the lateral lemniscus. top-down influences because of selective attention [3–5], language experience [6], and clinical syndromes such as Methods Rett’s syndrome [7] and learning problems [8]. However, in Animal preparation humans it is very difficult to investigate the neural Experiments were conducted in 24 male adult Sprague– mechanisms underlying the mediation or modulation of Dawley albino rats (300–400 g) obtained from the Beijing FFRs at the circuitry level. Thus, establishing animal models Vital River Experimental Animals Technology Ltd. (Beijing, is critical in this line of investigation. China). They were assigned randomly to two parts of the Among the important auditory nuclei, the inferior research: experiment 1 (n¼12) and experiment 2 (n¼12). colliculus is the last nucleus in the primary auditory Animals were housed individually in a 12-h light–dark cycle pathway where FFRs can reliably be recorded, because (lights on at 7 : 00 h) with ad-libitum food and water and precise neural phase-locking is increasingly lost at succes- were allowed 1 week to adapt to the laboratory environment sively higher levels of the brainstem-to-cortex pathway [9]. before surgery. All efforts were made to minimize animal Moreover, comparisons of recordings in auditory nuclei suffering and to use only the number of animals necessary and far-field placements implicate inferior colliculus as a to produce reliable scientific data. The anesthetic and primary source of scalp-recorded FFRs [10,11]. experimental protocol met all requirements regarding the However, specific coding mechanisms in inferior collicu- care and use of small animal subjects in accordance with lus underlying FFRs remain elusive, especially the dynamic guidelines of the Beijing Laboratory Animal Center, guide- interaction of excitatory and inhibitory influences conver- lines of the Canadian Council of Animal Care, and the ging on the central nucleus of the inferior colliculus. The Policies on the Use of Animals and Humans in Neuro- present research directly evaluates the major excitatory science Research revised and approved by the Society for projection from the contralateral central nucleus of the Neuroscience (1995). inferior colliculus through the commissure of inferior colliculus, as well as the contralateral dorsal nucleus of lateral lemniscus that has been shown to be an important Stimulus conditions GABAergic nucleus in the auditory brainstem of the rat and Pure tones (duration: 40 ms; ramps: 5 ms; intensity: 70 dB other mammals [12–15]. Effects of these projection pathways SPL) were generated by a TDT system II (Tucker-Davis 0959-4965 c Wolters Kluwer Health | Lippincott Williams & Wilkins Vol 19 No 14 17 September 2008 137 7 Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited. NEUROREPORT PING ETAL. Technologies, Alachua, Florida, USA), presented at a rate microinjection of Locke’s solution into the contralateral of 10/s, and delivered through a calibrated earphone (ED1). dorsal nucleus (n¼6). All other experiment details were One end of the 12-cm TDT sound-delivery soft tube identical to experiment 1. was connected to the ED1 earphone, and the other end was inserted into the ear canal on the side ipsilateral to Data analysis the recording electrode. TDT software (SigCal, SigGen and All neural responses were transformed from time domain BioSig, Tucker-Davis Technology) was used to calibrate the into the frequency domain by fast Fourier transformation earphone, generate acoustic stimuli, monitor neural res- and the peak spectral value at the center frequency of each ponse properties online, and store data for offline analysis. stimulus was taken as the measure of FFR amplitude. A2Â 7 (drug by frequency) within-subject analysis of Drug administration and electrophysiological recording variance was carried out to test for main effect of drug Animals were anesthetized with 10% chloral hydrate administration and possible interactions. (400 mg/kg, intraperitoneally) for the initial surgical proce- If the interaction was significant, an additional simple dure and a state of areflexia was maintained throughout effect analysis was carried out to test for differences at each the experiment by supplemental injections (0.1 ml per hour, frequency. intraperitoneally). The animals were fixed in a Kopf stereo- tactic head holder. A midline incision was made in the scalp, Histology the skin and muscles retracted laterally, and small cranio- At the end of testing, each animal was sacrificed with an tomies made on the dorsal surface of the skull. Steel overdose of chloral hydrate. Lesions were made at the electrodes (10–30 kO), insulated except at the 0.25-mm recording electrode tip by an anodal DC current (500 mA diameter tip, and cannula guides were lowered to target for 10 s). The brains were removed, stored in 10% formalin nuclei and the assembly fastened to the skull with dental with 30% sucrose until they sank, and then sectioned at acrylic. 50-mm intervals in the frontal plane in a cryostat (À201C) The following two brain structures were approached and the sections examined to assess electrode placements vertically based on coordinates referring to bregma: in inferior colliculus, as well as injection canal placements (i) central nucleus of the inferior colliculus (electrode in inferior colliculus and dorsal nucleus of the lateral ipsilateral to ear stimulated, cannula contralateral to ear lemniscus. stimulated): anteroposterior¼8.80 mm, mediolateral¼ 71.50 mm, dorsoventral¼4.50 mm and (ii) dorsal nucleus of the lateral lemniscus (cannula contralateral to ear Results stimulated): anteroposterior¼8.72 mm, mediolateral¼ Histology 73.00 mm, dorsoventral¼6.80 mm [16]. Histological results confirmed that all recording electrodes Drug administration was via the guide cannula connected and injection cannuli reached the targeted nuclei. to a 5-ml microsyringe through polyethylene tubing (inner diameter: 0.38 mm, outer diameter: 1.09 mm; Clay Adams Frequency-following responses Division, Becton-Dickinson and Co., Parsippany, New The results of experiments 1 and 2 show that marked FFRs Jersey, USA). A total of 1À2 ml KYNA (1 mM) or Locke’s were recorded in the central nucleus of the inferior solution was injected slowly over a period of approximately colliculus between 0.2À4 kHz, which is clearly evident in 1 min. both the time and frequency domains (representative FFR recordings were carried out in a sound-attenuating sample at 425 Hz shown in Fig. 1). chamber 30 min after surgery during the light phase À (8 : 00 18 : 00 h). Brain potentials were digitized (20 kHz), Effects of blocking the contralateral inferior colliculus amplified (1000 Â ), filtered (0.1À5 kHz bandpass), and In experiment 1, injection of KYNA in the contralateral averaged (N¼500 stimulus repetitions). central nucleus of the inferior colliculus resulted in a significant overall decrease of FFR amplitudes in the Experiment 1: effects of blocking the contralateral ipsilateral central nucleus, F(1,5)¼23.70, Po0.05. The inter- inferior colliculus action between drug and frequency was also significant, Twelve rats were randomly divided into two groups that F(6,30)¼3.70, Po0.05. The results show that decreases
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