Relating cluster and population responses to natural sounds and tonal stimuli in cat primary auditory cortex Yaron Rotman, Omer Bar-Yosef, Israel Nelken * Department of Physiology, Hebrew University-Hadassah Medical School and the Interdisciplinary Center for Neural Computations, Hebrew University, P.O. Box 12272, Jerusalem 91120, Israel Received 27 December 1999; accepted 16 October 2000 Abstract Most information about neuronal properties in primary auditory cortex (AI) has been gathered using simple artificial sounds such as pure tones and broad-band noise. These sounds are very different from the natural sounds that are processed by the auditory system in real world situations. In an attempt to bridge this gap, simple tonal stimuli and a standard set of six natural sounds were used to create models relating the responses of neuronal clusters in AI of barbiturate-anesthetized cats to the two classes of stimuli. A significant correlation was often found between the response to the separate frequency components of the natural sounds and the response to the natural sound itself. At the population level, this correlation resulted in a rate profile that represented robustly the spectral profiles of the natural sounds. There was however a significant scatter in the responses to the natural sound around the predictions based on the responses to tonal stimuli. Going the other way, in order to understand better the non-linearities in the responses to natural sounds, responses of neuronal clusters were characterized using second order Volterra kernel analysis of their responses to natural sounds. This characterization predicted reasonably well the amplitude of the response to other natural sounds, but could not reproduce the responses to tonal stimuli. Thus, second order non-linear characterizations, at least those using the Volterra kernel model, do not interpolate well between responses to tones and to natural sounds in auditory cortex. ß 2001 Elsevier Science B.V. All rights reserved. Key words: Cat; Primary auditory cortex; Natural sound; Population coding; Rate pro¢le; Volterra kernel 1. Introduction Most of the parameters whose coding has been studied in auditory cortex are extracted from responses to pure tones or slightly more complex stimuli, such as two-tone combinations for testing inhibitory sidebands. Due to the inherent non-linearity of the auditory sys- tem, pure tones do not allow a complete characteriza- tion of the system's response. It has been suggested in the past that natural stimuli (Wollberg and Newman, 1972; Suga, 1992), especially those comprising an ani- mal's `acoustic biotope' (Aertsen et al., 1979; Smolders et al., 1979) are more suitable for characterizing the full response properties of auditory neurons. However, the acoustic biotope, if it indeed can be de¢ned in a useful way, is necessarily so rich and complicated that it may be extremely di¤cult to collect responses to it and ana- lyze them in a simple, transparent way. In this study, we attempted to relate the responses of units in cat primary auditory cortex (AI) to tonal stim- uli and to natural sounds. Our approach was based on a hierarchy of models. First, the ability of linear and second order models, based on single- or two-tone re- sponses, to explain responses to natural sounds was studied. Second, Volterra series representations of the responses to natural stimuli were used to predict the responses to single tones and to other natural sounds. The main result of this paper is that although the rela- tionship between the responses of any single recording 0378-5955 / 01 / $ ^ see front matter ß 2001 Elsevier Science B.V. All rights reserved. PII:S0378-5955(00)00243-4 * Corresponding author. Abbreviations: AI, primary auditory cortex; BF, best frequency; FRA, frequency response area; EE, excitatory^excitatory; EI, excita- tory^inhibitory; EO, excitatory^no response; FM, frequency modu- lation Hearing Research 152 (2001) 110^127 www.elsevier.com/locate/heares