Hearing Research, 4 (1981) 299-307 0 Elsevier/North-Holland Biomedical Press

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RESPONSES OF SINGLE NEURONS IN PHYSIOLOGICALLY DEFINED AREA AI OF CAT CEREBRAL CORTEX: SENSITIVITY TO INTERAURAL INTENSITY

DIFFERENCES

D.P. PHILLIPS and D.R.F. IRVINE

Neuropsychology Laboratory, Department of Psychology, Monash University, Clayton, vie. 3168, 4ustralia

(Received 21 July 1980;accepted 3 February 1981)

In I5 cats, cortical area AI was defined by its frequency organization, and cells within that field were tested for sensitivity to interaural intensity differences (IIDs) using sealed stimulus delivery sys- tems. Of 39 cells tested quantitatively, 26 were sensitive to IIDs. In 70% of cases, sensitivity to IIDs reflected suppressive binaural interactions, and was manifested as a sigmoidal relation of spike count to IID. For 8 other cells, facilitative binaural interactions generated unit sensitivity to IIDs; three of these neurons demonstrated nonmonotonic dependency of spike count on IID, with peak filing rates at or near 0 dB IID. Analysis of spike count versus IID functions in terms of the auditory azimuths known to generate the IIDs used revealed that the majority of cells were most sensitive to IIDs associ- ated with azimuths in the contralateral sound field. These data are compatible with other evidence on the sensitivity of cortical and brainstem cells to binaural sound-localization cues, and suggest that each side of the auditory brain is independently capable of localizing sound sources in the contralateral field.

Key words: auditory cortex; single neurons; sound localization; interaural intensity differences.

INTRODUCTION

Behavioral studies have consistently supported the hypothesis of a role of the auditory cortex in the performance of tasks involving the localization of a sound source in space, although the precise nature of that role is unclear [9,15,16,26,27,35]. One of the major binaural cues for sound localization is the interaural intensity difference (IID) created by the sound-shadowing effect of the head and pinnae. Since the majority of auditory corti- cal neurons are binaurally influenced [3,7,14,18], it is pertinent to examine their sensitiv- ity to IIDs.

There has been only one such study of the cat auditory cortex [7]. Brugge et al. described in detail the responses of a number of cortical neurons to IID, but the location of their cells with respect to the recently mapped and re-defined cortical fields [22,24] is unclear. Moreover, there is little evidence on the range of IIDs over which cortical cells show greatest sensitivity. This issue is of particular interest because a recent study [25] has provided parametric data on the magnitude of the IIDs generated by the cat’s head as a function of the azimuth of tonal stimuli of different frequencies. Accordingly, the aim of the present study was to examine the sensitivity of cells in physiologically defined AI

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to binaural stimuli involving IlDs in the behaviorally relevant range. Preliminary data have been presented elsewhere [28,29].

METHODS

The data to be reported were obtained from 15 adult cats with middle and outer ears free of infection. The cats were anesthetized initially with sodium pentobarbital (40 mg/kg, i.p.) and surgical anesthesia was maintained by supplemental doses of ketamine hydrochloride (3 mglkg, i-m.) and/or pentobarbital(7 mg/kg, i.v.).

Detailed descriptions of surgical, stimulating and recording procedures have been pro- vided elsewhere [ 19,201. Briefly, the trachea was cannulated, the skull was exposed, and the head was supported by a head-holder which left the external meatuses unobstructed. The cistemum magnum was opened to reduce cortical pulsations. The meatuses were cleared of surrounding tissue and were transected to allow insertion of the stimulus deliv- ery systems; co&dear potentials were monitored continuously by means of stainless-steel spring electrodes located on the round windows and cemented to the tympanic bullae. These electrodes provided a continuous monitor of peripheral auditory system sensitivity, and revealed that for each cat, the absolute sensitivities of the two ears were similar (within 5 dB). The skull was opened to expose the left ectosylvian gyri; the cortex was photographed and then protected by cotton or Gelfoam soaked in warmed mineral oil or saline. Rectal temperature was maintained at 37S”C.

The cat was located in an electrically shielded, sound-attenuating room. Tonal stimuli were generated by a Rockland Frequency Synthesizer, were shaped to 100 ms duration including 10 ms rise-fall times, and were presented at a rate of one per second. The stim- uli were transduced by Briiel and Kjaer type 4133 condenser microphones which were housed in sound delivery systems incorporating calibrated probe microphone assemblies for on-line measurement of sound pressure level (SPL: dB re 0.0002 dyne/cm*). Single neurons were recorded extracellularly using glass-insulated, platinum-plated tungsten mi- croelectrodes which were advanced using a remotely controlled stepper motor. Unit spikes were led to a Schmitt trigger; stimulus and response event times were recorded and analyzed on-line by a Nova computer programmed for spike-count and response histo- gram analyses.

When a single unit was isolated, its threshold best frequency (BF) was ascertained, and spike-count versus intensity functions for monaural and binaural BF tones were obtained. To assess sensitivity to IIDs, the cat was stimulated with binaural BF tones, the average binaural intensity (ABI: the average of the intensities at the two ears) of which was held constant; IlDs were introduced by symmetrically varying the contralateral and ipsilateral intensities about the ABI. The summed responses of the unit to 50 stimulus presentations at each IID were then plotted as a function of IID (expressed as the level of the ipsilateral stimulus relative to the contralateral). For each cell, IlDs were tested in pseudorandom order, and generally at an ABI near the peak of the contralateral intensity function.

The IlDs produced by this procedure correspond to those produced when a real sound source located at different positions along an arc from one side of the head to the other. That is, the changes in IID are associated with a reciprocal increase and decrease in the absolute stimulus levels at the two ears. Comparison of the IID function with the contra-

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lateral spike count function over the intensity range used in the IID stimuli enables assess- ment of the contributions to the IID function of the changing contralateral intensity and of the interaural intensity differences per se.

RESULTS

Area AI was identified in each cat by the generation of partial maps of the orderly pro- gression of unit BFs across the middle ectosylvian gyrus [30]. Quantitative IID data have been obtained for 39 cells whose BFs ranged from 1.5 to 17.0 kHz.

Thirteen cells (31% of those tested) exhibited discharge rates which were not syste- matically influenced by IIDs. The majority of these (12 cells) were excited by monaural stimulation of each ear. Data for one such unit are shown in panels A and B of Fig. 1. This neuron had a BF of 9 kHz, and, as is illustrated in Fig. 1 A, stimulation of either the contralateral (open squares) or ipsilateral (open circles) ear elicited intensity-dependent

UNIT 45-10. SF.9000 Hz

UNIT 40 -16. SF.6000 Hz

_‘f ‘fy_

-,. 10 50 60 70 80 -20 0 *zo

INTENSITY I.I.D.

(dB SPL) (IPSI dB rc CONTRA)

Fig. 1. A, C, E: Spike count versus intensity functions for monaural contralateral (a), monaural ipsi_ lateral (0) and binaural, equally-intense (b) best frequency stimuli for each of three cells. B, D, F: Spike-count versus IID functions for the same cells, tested at the average binaural intensity (ABI) indie

cated. Solid lines represent IID functions; dashed lines represent contralateral intensity functions for the range of intensities involved in the IID conditions.

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excitatory responses, although the thresholds for the monaural responses were some 30 dB different. For the most part, up to 60 dB, the binaural responses (open triangles) were

weaker than the responses to stimulation of the contralateral ear alone. The IID function for this unit is shown in Fig. 1B (solid line) and is superimposed over

the contralateral intensity function (dashed line) for the intensity range involved in gener- ating the IIDs, viz., 40-60 dB. This cell, like the vast majority of units excited by mon-

aural stimulation of each ear, was relatively insensitive to IIDs. Thus, over a 40 dB range of IIDs, its discharge rate varied by only 30% and in an irregular fashion.

The remaining 26 cells (69%) exhibited marked sensitivity to IIDs. Two forms in which such sensitivity was manifested are illustrated by the data for individual units in

Fig. 1, C-F. Unit 51-8 (Fig. 1C) was excited by monaural contralateral BF stimuli, and, as indi-

cated by the fact that the binaural response was negligible over a wide intensity range, was inhibited by ipsilateral stimulation. When IIDs were employed (Fig. ID), the response

of the cell declined sharply as the level of the ipsilateral stimulus increased relative to that of the contralateral. Comparison of the IID curve with the contralateral intensity func- tion (broken line in Fig. 1D) reveals the contributions to the IID function of the declining

contralateral intensity and the interaural intensity difference. Over the range of IIDs to which the neuron showed greatest sensitivity (ipsilateral intensity 20 dB less than contra- lateral to 0 dB IID), the contralateral spike-count function decreased by approximately 25% while the dichotic spike-count function fell almost to zero. These data indicate that although the declining contralateral intensity contributed to the IID function, the increas- ing strength of inhibition from the ipsilateral ear was the dominant influence on the neu- ron’s IID sensitivity. This was the most common pattern of activity observed, and it char- acterized 18 of the units sensitive to IIDs.

Five IID-sensitive cells demonstrated more complex binaural interactions, and a repre-

sentative case is illustrated in Fig. 1, E and F. Inspection of the intensity function data for unit 40.16 reveals that monaural contralateral stimuli were excitatory over a 30 dB dynamic range, and that while equal-intensity ipsilateral BF tones were ineffective on their own, they facilitated the contralateral response when presented simultaneously. The sensitivity of this neuron to IIDs (Fig. 1F) in part reflects the decreasing strength of the contralateral responses over the intensity range contributing to the IID stimuli. However,

the IID curve is much steeper than the contralateral intensity function, and it is apparent that the cell’s sensitivity to IIDs is produced by both a facilitative (for ipsilateral intensi- ties less than or equal to the contralateral intensity) and a suppressive (for ipsilateral intensities greater than contralateral intensities) influence from the ipsilateral ear.

Three further cells demonstrated IID sensitivity explicable in terms of purely facilita- tive interactions, and data for one such cell are shown in Fig. 2. This unit was tested for IID sensitivity at an average binaural intensity of 60 dB, an intensity at which stimulation of either the contralateral (CA) or ipsilateral (IA) ear alone produced only very weak responses. This neuron, however, exhibited strong binaural facilitation, and testing with IIDs revealed a sharply nonmonotonic relation of spike count to IID which peaked at +6 dB (ipsilateral intensity re contralateral). Two other cells showed similar monaural and binaural responsiveness, and their IID functions each peaked at 0 dB IID.

For the 23 cells exhibiting sigmoidal relations of spike count to IID, it was most com-

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UNIT 52-4 BF. 14.0 kHz

L _-______~~________S~O~

, -20 -10 0 +I0 *20 .30

IID IIPSI dB re CONTRA)

Fig. 2. IID function for a cell demonstrating facilitative binaural interaction. CA and IA refer to the responses to stimulation of the contralateral and ipsilateral ear alone at 60 dB. Details as for Fig. 1.

monly the case (21/23 units) that the cells responded more strongly to stimuli involving IIDs favoring the contralateral ear, i.e., when the contralateral stimulus level exceeded the ipsilateral, However, individual cells varied with respect to the precise range of IIDs over

I I I 8 I I I -30 -20 -10 0 +lO l 20 +30

INTERAURAL INTENSITY DIFFERENCE tIPSI dB re CONTRA)

Fig. 3. IID functions for 5 cells, illustrating differences in the range of IIDs over which neurons were most sensitive.

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which they were most sensitive, as indicated by the steepness of the spike count func- tions. This point is illustrated in Fig. 3 which shows IID functions for 5 cells for which discharge rate has been expressed in percentage terms to eliminate differences in overall spike counts between units. Most neurons had steeply declining functions within the range of IIDs from -2.5 dB to +I0 dB (ipsilateral intensity re contralateral). Thus, unit 36-16 was most sensitive to changes in IID between -20 dB and -6 dB (ipsilateral inten- sity re contralateral); unit 49-6 between -6 dB and 0 dB, and unit 34-13 was most sensi- tive in the range -8 dB to t8 dB. Only one cell was sensitive to IIDs outside the range generated by the sound shadow of the cat’s head.

IID functions for 17 neurons were sufficiently detailed to enable precise specification of their 80% ‘dynamic ranges’ (viz., IID range over which spike count declined from 90 to 10% of the maximum spike output), and subsequent estimation of the auditory azimuthal ranges with which these IID ranges were associated. The latter data were obtained by extrapolation from detailed plots of azimuth-induced IIDs reported by Moore and Irvine [25 1. For each unit, the IID/azimuth data at the frequency closest to the cell’s BF were employed.

These data for 17 cells are shown in Fig. 4. Each arrow represents the range of azi- muths corresponding to the IID ‘dynamic range’ of an individual unit. For purposes of presentation, the arrows for different units have been arbitrarily located on a series of equally spaced, concentric circles. The direction of each arrow indicates the direction in which spike count increases. Although IIDs are approximately symmetrical for azimuths in front of and behind the interaural axis, estimated azimuthal ranges have for conveni- ence been plotted only in the frontal field.

Inspection of Fig. 4 reveals that the majority of arrows are located in the contralateral sound field, indicating that the neurons are coding mainly for contralateral azimuths. The majority of cells are most sensitive to IIDs generated by azimuths over ranges which fall

I!

CONTRALATERAL IPSILATERAL

Fig. 4. Azimuthal projections of IID functions for 17 cells for which detailed data were obtained. Each arrow represents the azimuthal range corresponding to the IIDs to which an individual unit was most sensitive.

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within the region from 10” on the ipsilateral side to approximately 50” on the contra- lateral side of the mid-sagittal plane. A unit sensitive to a similar range of IIDs, but for which spike-count increases in the reverse direction, is indicated by the dashed arrow.

DISCUSSION

This study has provided evidence on some features of the IID sensitivity of cells whose allocation to the primary auditory cortex (AI) was based on the identification of that field by its frequency organization. The data confum those of Brugge et al. [7] who demonstrated the sensitivity of cortical cells with suppressive interactions to IIDs, but extend those observations by illustrating that other cell types may encode IIDs, and by providing evidence that the range of IIDs to which AI cells are most sensitive is generally associated with the contralateral sound field.

These data are compatible with observations on IID-sensitive cells in the cortex [3,7,8] and brainstem and thalamic nuclei [1,2,5,6,12,17,31] in a variety of species. The majority of studies of IID coding by neurons in the cat auditory system have described only the responses of those cells, excited by stimulation of one ear and inhibited by stimulation of the other, which demonstrate sigmoidal relations of spike count to IID [1,2,5,7,17,31]. It is apparent, however, that as in the chinchilla cortex [3] and kangaroo rat inferior colliculus [34], some cells in cat primary auditory cortex exhibiting facilita- tive interactions also encode IIDs. The finding that some such cells exhibit nonmonotonic relations of spikecount to IID, firing rates peaking at or near zero IID, is compatible with the recent description of similar cells in the awake cat’s, Al showing nonmonotonic rela- tions of spike count to interaural arrival time disparities [21].

A number of authors have drawn attention to the fact that cells which are sensitive to binaural sound localization cues generally respond more strongly when the interaural disparities favor the contralateral ear, i.e., when the contralateral stimulus arrives before, or is more intense than, the ipsilateral [2,3,33,34]. It has been postulated that such cells form a neural basis for the discrimination of sound source laterality [2,3,33,34]. The pre- sent observations confnm that cat AI cells which are sensitive to IIDs respond more strongly when the contralateral stimulus is more intense, and are compatible with evi- dence from studies employing free-field stimuli in the cat [4,1 l] and mouse [lo] which have reported that auditory cells frequently have contralateral ‘receptive fields’. Our data extend the observations from the dichotic stimulus studies, however, by indicating that the IID ranges to which such cells are most sensitive (i.e., the ranges over which response strength is a sensitive function of. IID) are predominantly associated with contralateral azimuths. Thus, these cells may encode not only sound source laterality, but also sound source azimuth. Whether or not cat Al or any other cortical field contains a topographic representation of the contralateral sound field, perhaps like that described for the barn owl midbrain [23], remains to be determined.

A number of models of sound localization mechanisms postulate that a comparison of stimulusevoked activity in the two sides of the auditory brain provides the basis for the identification of sound source lateral@ [2,3,13,32,33,38]. Our data, and the hypo- thesis derived from it, suggest that such comparisons are unnecessary and that each side of the auditory brain is independently capable of localizing sound sources in the contra-

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lateral sound field. Available evidence indicates that the effects of unilateral brainstem lesions on reflexive head orientations [37], and of unilateral cortical [35] and brachium of inferior colliculus [36] lesions on localization are restricted to the responses to sound sources in the contralateral field. These observations do not necessitate that the role of the cortex ‘in sound localization is a purely sensory one [9,15,16]; it is apparent, how- ever, that the cortex contains cells processing the acoustic sensory information required for orienting or tracking responses to auditory stimuli.

ACKNOWLEDGEMENTS

This research was supported in part by grants from the Australian Research Grants Committee. The technical assistance of Mr. T. Crowle, Mrs. J. Sack and Mr. V. Kohout is greatly appreciated.

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