Modulatory Effect of Cortical Activation on the Lemniscal AuditoryThalamus of the Guinea PigJUFANG HE,1,2YAN-QIN YU,1YING XIONG,1TSUTOMU HASHIKAWA,2AND YING-SHING CHAN31Department of Rehabilitation Sciences, The Hong Kong Polytechnic University, Hung Hom, Kowloon, Hong Kong;2Laboratory for Neural Architecture, Brain Science Institute, The Institute of Physical and Chemical Research, Wako,Saitama 351-0198, Japan; and3Department of Physiology, The University of Hong Kong, Sassoon Road, Hong KongReceived 8 January 2002; accepted in final form 22 April 2002He, Jufang, Yan-Qin Yu, Ying Xiong, Tsutomu Hashikawa, andYing-Shing Chan. Modulatory effect of cortical activation on thelemniscal auditory thalamus of the guinea pig. J Neurophysiol 88:1040–1050, 2002; 10.1152/jn.00014.2002. In the present study, weinvestigated the point-to-point modulatory effects from the auditorycortex to the thalamus in the guinea pig. Corticofugal modulation onthalamic neurons was studied by electrical activation of the auditorycortex. The modulation effect was sampled along the frontal orsagittal planes of the auditory thalamus, focusing on the ventraldivision (MGv) of the medial geniculate body (MGB). Electricalactivation was targeted at the anterior and dorsocaudal auditory fields,to which the MGv projects and from which it assumptively receivesreciprocal projections. Of the 101 MGv neurons examined by activa-tion of the auditory cortex through passing pulse trains of 100–200␮A current into one after another of the three implanted electrodes(101 neurons ⫻ 3 stimulation sites ⫽ 303 cases), 208 cases showed afacilitatory effect, 85 showed no effect, and only 10 cases (7 neurons)showed an inhibitory effect. Among the cases of facilitation, 63 casesshowed a facilitatory effect ⬎100%, and 145 cases showed a facili-tatory effect from 20–100%. The corticofugal modulatory effect onthe MGv of the guinea pig showed a widespread, strong facilitatoryeffect and very little inhibitory effect. The MGv neurons showed thegreatest facilitations to stimulation by the cortical sites, with theclosest correspondence in BF. Six of seven neurons showed an ele-vation of the rate-frequency functions when the auditory cortex wasactivated. The comparative results of the corticofugal modulatoryeffects on the MGv of the guinea pig and the cat, together withanatomical findings, hint that the strong facilitatory effect is generatedthrough the strong corticothalamic direct connection and that the weakinhibitory effect might be mainly generated via the interneurons of theMGv. The temporal firing pattern of neuronal response to auditorystimulus was also modulated by cortical stimulation. The mean first-spike latency increased significantly from 15.7 ⫾ 5.3 ms with onlynoise-burst stimulus to 18.3 ⫾ 4.9 ms (n ⫽ 5, P ⬍ 0.01, paired t-test),while the auditory cortex was activated with a train of 10 pulses.Taking these results together with those of previous experimentsconducted on the cat, we speculate that the relatively weaker inhibi-tory effect compared with that in the cat could be due to the smallernumber of interneurons in the guinea pig MGB. The corticofugalmodulation of the firing pattern of the thalamic neurons might enablesingle neurons to encode more auditory information using not only thefiring rate but also the firing pattern.INTRODUCTIONThe auditory cortex receives projections from the thalamus,and in turn, projects to the thalamus and also to the inferiorcolliculus (Andersen et al. 1980; Herbert et al. 1991; Liu et al.1995a; Montero 1991; Ojima 1994; Winer et al. 1998). Corti-cofugal projection to the thalamus and the inferior colliculushas been suggested as performing the following: 1) a gating orgain control function in the transmission of information fromthe periphery to the cortex (Crick 1984; Harth et al. 1987; He1997; Murphy and Sillito 1987; Villa et al. 1991); and 2)asharpening of the tuning curves of the frequency and temporalfeatures of the auditory information in the auditory system(Gao and Suga 1998, 2000; Jen et al. 1998, 2001; Suga et al.1997, 2000; Sun et al. 1989, 1996; Yan and Suga 1996, 1998,1999; Zhang et al. 1997; Zhang and Suga 1997, 2000; Zhouand Jen 2000).Earlier investigators adopted a cooling technique to inacti-vate the cortex and compare the neuronal responses to auditorystimuli (Orman and Humphrey 1981; Ryogo and Weinberger1976; Villa et al. 1991). However, this methodology has thefollowing two weak points: 1) it is difficult to selectivelyinactivate a small region of the cortex by cooling; and 2) theeffects of cortical cooling on thalamic activity may be difficultto observe in an anesthetized animal, which may already havedepressed cortical activity to some degree. Most of the recentstudies adopt electrical stimulation to selectively activate thedefined auditory cortex (Chowdhury and Suga 2000; He 1997;Jen et al. 2001; Ma and Suga 2001a; Sakai and Suga 2001; Yanand Suga 1996, 1998; Zhang and Suga 2000; Zhou and Jen2000). Investigators have used a very wide range of electricalstimulation current, from 100 nA to 1 mA, to activate thecortex (Chowdhury and Suga 2000; Edeline et al. 1994b; He1997; Jen et al. 2001; Ma and Suga 2001a,b; Sakai and Suga2001; Suga et al. 2000; Weinberger et al. 1995; Xiao and Suga2002; Yan and Suga 1996, 1998; Zhang and Suga 2000; Zhouand Jen 2000). This fundamental parameter, which will largelyaffect data interpretation, urgently needs to be standardized.The present study examined the parameter for cortical activa-tion in the guinea pig.A mainly corticofugal facilitatory effect has been observedin the ventral nucleus (MGv) of the medial geniculate bodyAddress for reprint requests: J. He, Department of Rehabilitation Sciences,The Hong Kong Polytechnic University, Hung Hom, Kowloon, Hong Kong(E-mail: [email protected]).The costs of publication of this article were defrayed in part by the paymentof page charges. The article must therefore be hereby marked ‘‘advertisement’’in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.J Neurophysiol88: 1040–1050, 2002; 10.1152/jn.00014.2002.1040 0022-3077/02 $5.00 Copyright © 2002 The American Physiological Society www.jn.org(MGB) (He 1997), which has been recognized as the recipientof the most direct ascending auditory pathway, as the nucleuswith the most clear-cut cochleotopic representation, as thenucleus that projects to the primary auditory cortex (AI), and asthe major recipient