HWRlflC RESBlRCH ELSEVIER Hearing Research 72 (1994) 223-236 Population responses to multifrequency sounds in the cat auditory cortex: Four-tone complexes I. Nelken *, Y. Prut, E. Vaddia, M. Abeles Drpurtmcxt of zyxwvutsrqponmlkjihgfedcbaZYXWVUTSRQPONMLKJIHGFEDCBA Physiolo~, The Iludassah Medical Scl~ool. Jemralem 91010, Irrael (Received 27 February 1993; Revision rrceived 1 September 1903: Accepted 15 September IYYi) Abstract Population responses to two-tone and four-tone sounds were recorded in primary auditory cortex of anesthetized cats. The stimuli were delivered through a sealed, calibrated sound delivery system. The envelope of the neural signal (short time mean absolute value, MABS) was recorded extracellularly from six microelectrodes simultaneously. A new method was developed to describe the responses to the four-tone complexes. The responses were represented as sums of contributions of diffcrcnt orders, The first order contributions described the effect of the single frequencies appearing in the stimulus. The second order contributions described the modulatory effect of the pairs of frequencies. Higher order contributions could in principle bc computed. This paper concentrates on the mean onset responses. The extent to which the first and second order contributions described the onset responses was assessed in two ways. First, the actual rcsponscs to two-tone stimuli were compared with those predicted using the contributions computed from the four-tone stimuli. Second, the residual variance in the responses, after the substraction of the first and second order contributions. was computed and compared with the variability in the rcsponscs to repetitions of the same stimulus. The first type of analysis showed good quantitative agreement between the predicted and the measured two-tone responses. The second type of analysis showed that the first and second order contributions wcrc often sufficient to predict the responses to four-tone stimuli up to the level of the variability in the rcsponscs to rcpctitions of a single stimulus. In conjunction with the results of the companion paper (Nelken et al., 1994a) it is concluded that the onset rcsponscs to multifrcquency sounds are shaped mainly by the single frequency content of the sound and by two-tone interactions, and that higher order interactions contribute much less to the responses. It follows that single-tone cffccts and two-tom interactions arc necessary and sufficient to explain the mean population onset rcsponscs to the four-tone stimuli. Marc information can bc coded in the temporal evolution of the responses. Keq’ scuds: Primary Auditory Cortex; Complex Sounds; Non-linear modeling: Cat 1. Introduction The study of the coding of complex sounds in the activity of the central nervous system is still in its infancy. On the one hand, it is known that the re- sponses of neural elements (nerve fibers, neurons and populations of neurons) to complex stimuli often can- not be predicted on the basis of their responses to simple stimuli (e.g. Oonishi and Katsuki, 1965; Whit- field and Evans, 1965; Abeles and Goldstein, 1972; Newman and Wollberg, 1973; Smolders et al., 1979, * Corresponding author. The Johns Hopkins School of Medicine. Center for Hearing Sciences. 720 Rutland Avenue, Baltimore. MD 21205. USA Eggermont et al., 1981; Phillips and Cynader. 1985: Ehret and Merzenich 1988; Sutter and Schreiner. 1991; Spirou and Young, 1991; Nelken et al.. 1994a; Shamma et al., 1993). On the other hand, once beyond the use of simple stimuli, i.e. those described by one or two parameters, the wealth of possible sounds is enormous. It is impossible to map the responses of a neuron or a population of neurons to all possible stimuli; on the other hand, since there is no clear understanding of the processing of complex sounds by neural elements. it is hard to choose apriori a subset of all possible sounds which would completely characterize the rc- sponses of these neural elements, in the sense that their response to any other sound can be predicted from their responses to this subset. Previous work studying the coding of complex sounds can usually be categorized into one of three groups. 037X-5955/94/$07.00 0 1994 Elsevier Science B.V. All rights reserved SSDI 037X-5’)55(93)E0157-7