Functional classes of neurons in primary auditory cortex of the cat distinguished by sensitivity to sound location

Could neurons in the primary auditory cortex (AI) encode the spatial location of sounds? Is location sensitivity a parameter of stimulus coding relevant to topographical organization in AI? We have mapped receptive fields of single units in AI of the cat by varying systematically the location of a tonal stimulus within a sound field free of acoustic obstructions and reflections. By orienting tangential electrode penetrations parallel to the mediolateral axes along which neurons are tuned to the same stimulus frequency, we have explored the possibility that this axis could be concerned with spatial features of sound stimuli. Approximately half of the neurons encountered were selective for the location of sounds. The locationselective units could be divided into two discrete populations. Hemifield units responded only to sounds presented in the contralateral sound field, with receptive fields extending from a well defined medial border to beyond the contralateral pole of the sound field. Axial units had small, completely circumscribed receptive fields that were constant in location for all such units in each cortical hemisphere studied. The location of axial receptive fields coincided with the acoustical “axis” of the contralateral pinna which was defined by acoustical measurements of the directionality of the ear. Axial units were restricted to the rostra1 pole of AI where neurons are tuned for high frequencies, while hemifield units were located more caudally and were tuned for lower frequencies. The location-insensitive, omnidirectional, units were distributed across the entire length of AI sampled. Some of the properties of the measured receptive fields could be inferred by comparing the passive acoustical properties of the ear with binaural interactions previously described in AI. There was no indication of a systematic map of sound space in AI. Instead, the mediolateral axis of AI contained spatially segregated regions of different unit classes. This organization was consistent with the previously described pattern of binaural interaction bands. The location-selective and location-insensitive unit classes might represent stages of fundamentally different lines of processing that are segregated within AI. The primary auditory cortex (AI) of the cat contains a topographical representation of the auditory sensory ’ The recording phase of these experiments was carried out in the laboratory of Dr. Masakazu Konishi at the California Institute of Technology. We are indebted to Dr. Konishi for his hospitality and advice throughout the course of this study. Dr. Eric I. Knudsen also was very helpful. The “hoop” was a product of the mechanical ingenuity of Herb Adams and the assistance of the Spencer Foundation. The manuscript benefitted from the critical reading by Drs. W. M. Jenkins, E. I. Knudsen, M. M. Merzenich, and J. M. Zook. This project was supported by a grant from the West Coast Neuroscience Consortium (to J. C. M.), National Institutes of Health-United States Public Health Service Grants EY 1909 and EY 1391 (to J. D. P.) and Grant NS-10414 (to Dr. M. M. Merzenich). epithelium, the cochlear partition (Merzenich et al., 1975). This is manifest as a caudal to rostra1 map of the audible frequency domain (tonotopic organization). In the visual system, the representation of the two dimensions of the retina fills the two dimensions of the visual cortex (e.g., Hubel and Wiesel, 1962). In contrast, the representation in the auditory cortex of the one-dimensional sound frequency domain is expanded laterally so that points on the cochlea (i.e., single frequencies) are represented as mediolaterally oriented lines in AI (isofrequency contours). This re-representation of single frequencies as isofrequency contours could provide a substrate for the topographical representation of some parameter of sound stimuli that is independent of sound frequency (e.g., Tunturi, 1952; Suga, 1977). ’ Current address: National Vision Research Institute, 386 Cardigan The response to binaural stimulation is one parameter St., Carlton 3053 Victoria, Australia. that varies with location within an isofrequency contour. 108 Middlebrooks and Pettigrew Vol. 1, No. 1, Jan. 1981 In AI of the cat, neurons with similar responses to binaural stimulation form radial columns extending through the depth of the cortex (Abeles and Goldstein, 1970; Imig and Adrian, 1977). Units with different responses to binaural stimulation are topographically segregated within AI, forming rostrocaudally oriented bands (“binaural interaction bands”) that cross the axis of isofrequency contours (Imig and Brugge, 1978; Middlebrooks et al., 1980). It has been suggested that bands of units that are sensitive to different features of dichotic stimuli might form independent processing units within AI (e.g., Middlebrooks et al., 1980). Such a topographical segregation of functional subunits has been demonstrated in the auditory cortex of the mustache bat, where neurons whose responses are suitable for the detection of low intensity sounds are segregated from neurons that could be useful for sound localization (Manabe et al., 1978). The auditory cortex of the cat has been implicated in the representation of the spatial locations of sounds. For example, single units in AI of the cat tested with dichotic stimuli (sounds delivered independently to the two ears) are sensitive to interaural disparities that provide spatial information which is not available from one ear alone (Hall and Goldstein, 1968; Brugge et al., 1969). Some neurons in the auditory cortex respond preferentially to sounds presented in limited regions of the sound field (Evans, 1968; Eisenman, 1974; Sovijarvi and Hyvarinen, 1974). Bilateral ablations of the temporal cortex cause deficits in the ability of a cat to go to the source of a sound (see Neff et al., 1975 for review). The present study was undertaken to examine the role of sound location in the functional organization within AI. Can single units in AI of the cat encode the location of a sound source? Might the mediolateral dimension of AI be concerned with spatial features of sound stimuli? We have addressed these questions by recording from single units in AI while presenting tonal stimuli in a free sound field. The receptive fields of auditory neurons were mapped by plotting the boundaries of spatial regions within which stimuli elicited a given neural response. Tangential electrode penetrations were oriented mediolaterally, approximately parallel to isofrequency contours, to explore the possibility that the spatial sensitivity of units might vary along the dimension where binaural interactions previously have been shown to vary. Using simple criteria based on characteristics of sensitivity to sound location, we could distinguish three classes of units in AI, two of which had sharply defined spatial receptive fields. These unit types were topographically segregated within isofrequency contours. By comparing the location sensitivity of cortical neurons with the acoustical transfer function of the external ear, we can begin to relate this data to the existing body of data collected in experiments using dichotic stimulation. These results are relevant to the neural bases of auditory behavior in the cat as well as to the understanding of the functional principles of organization within the primary auditory cortex. Preliminary reports of this work have appeared elsewhere (Middlebrooks and Pettigrew, 1980a, b). Materials and Methods Animal preparation and single unit recording. We studied 21 young adult cats from an inbred colony of specific-pathogen-free tabbies. Among these inbred cats, we found relatively little variation in the cortical sulcal pattern or in the location of the primary auditory cortical field (AI) relative to the sulcal pattern. This is in contrast to the great variation seen among cats from random sources. In addition, the cats from this closed colony were relatively free from ear mites and other pathology of the external and middle ear that is common among other cats. The neurophysiological data presented here are from 15 cats in which good recordings were obtained from AI. The data on the passive acoustics of the ear are from two additional cats. Surgical anesthesia was induced with intramuscular injections of ketamine hydrochloride (Ketaset, 20 mg/ kg) and diazepam (Valium, 1 mg/kg). Supplementary doses of ketamine were given as needed, with smaller doses necessary once the animal was comfortably suspended in its hammock for recording (see below). Under even the lightest conditions of anesthesia used, we observed no spontaneous movements of the pinnae nor were there any movements observed in response to sound stimuli. Following induction of anesthesia, cats were positioned temporarily in a stereotaxic device using blunt ear and eye bars. This facilitated alignment of the animal in a standard coordinate system. A stainless steel bar was attached to the skull with screws and acrylic cement. This bar extended behind the cat’s head and was used later for holding the head in position in the sound chamber. The skull was opened over the middle ectosylvian gyrus in the left hemisphere and a recording chamber was mounted over the skull opening. The scalp was closed around the chamber and supporting bar, and the pirmae were restored to a normal-appearing configuration. At this point, the cat was removed from the stereotaxic device. Its body was suspended in a canvas hammock and the head was supported, still in alignment with stereotaxic coordinates, by clamping the steel bar from behind the head. Thus, the animal was positioned in a well defined coordinate frame with no obstructions in the sound path to its ears. This entire setup was positioned in the sound chamber with the cat’s Horsley-Clarke horizontal plane parallel to the floor and the interaural axis aligned with the axis of the sound stimulation apparatus (Fig. 1). The activity of sing