NEURONS IN CAT PRIMARY AUDITORY CORTEX SENSITIVE TO

NEURONS IN CAT PRIMARY AUDITORY CORTEX SENSITIVE TO C O R R E L A T E S OF A U D I T O R Y M O T I O N IN THREE-DIMENSIONAL SPACE by E r i k a Stumpf B . S c , M c G i l l U n i v e r s i t y , 1988

A THESIS SUBMITTED IN PARTIAL F U L F I L L M E N T OF THE REQUIREMENTS FOR T H E DEGREE OF MASTER OF ARTS in THE F A C U L T Y OF GRADUATE STUDIES (Department of Psychology)

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ii

ABSTRACT

The p r i m a r y auditory cortex (area A l ) plays a n important role i n the localization of static sound sources. However, little is k n o w n concerning how i t processes information about sound source motion. T h i s study was undertaken to investigate the responses of single neurons i n the p r i m a r y auditory cortex of the cat to correlates of auditory motion i n space. Diotic and dichotic changes i n sound intensity presented through earphones simulated auditory motion i n four directions: toward and away from the receiver along the m i d l i n e , into the ipsilateral hemifield a n d into the contralateral hemifield. Different rates of intensity change simulated sound source velocity. Results indicate t h a t A l neurons can be h i g h l y selective to intensity correlates of auditory motion. Three major classes of neurons were encountered: neurons sensitive to motion toward or a w a y from the receiver, neurons sensitive to ipsilateral- or contralateraldirected motion, a n d monaural-like neurons.

The different classes of direction-

selective neurons were spatially segregated from each other a n d appeared to occur i n clusters or columns i n the cortex. I n addition to their selectivity for different directions of simulated sound source motion, A l neurons also responded selectively to the rate and excursion of intensity changes, a correlate of sound source velocity. The major determinants of direction a n d velocity selectivity were interactions between the following response properties of A l neurons: b i n a u r a l interaction type, ear dominance, on/off responses, a n d monotonicity of rate/intensity function. These findings suggest that n e u r a l processing of auditory motion m a y involve n e u r a l mechanisms distinct from those i n v o l v e d i n static sound localization, a n d indicate t h a t some neurons i n the p r i m a r y auditory cortex m a y be part of a specialized motion-detecting m e c h a n i s m i n the auditory system.

iii

TABLE OF CONTENTS

ABSTRACT

ii

LIST

iv

OF FIGURES

INTRODUCTION 1 Sound localization 1 A u d i t o r y system 4 P r i m a r y a u d i t o r y cortex 8 The role of the p r i m a r y auditory cortex i n the encoding of sound source location 9 R e a l a n d s i m u l a t e d movement 12 Implementation and predictions 15 METHODS A n i m a l preparation Stimuli Calibration D a t a collection Data analysis

18 18 19 22 22 23

RESULTS Directional selectivity A . M o t i o n i n depth B. Motion in azimuth C. Monaural-like units D . D i s t r i b u t i o n of u n i t types Velocity selectivity Effect of c h a n g i n g frequency

25 25 27 38 44 48 48 GO

DISCUSSION M e c h a n i s m s of direction a n d velocity selectivity A . Motion i n depth B. Motion i n azimuth C. Monaural-like units D. Velocity selectivity E . A model for direction a n d velocity selectivity Technical considerations A n a l o g i e s to v i s i o n Specialized motion-detecting mechanisms i n the auditory system?

61 61 61 62 63 63 64 66 68 69

REFERENCES

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iv LIST O F F I G U R E S

Figure 1

Ascending auditory pathways

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Figure 2

B i n a u r a l i n t e r a c t i o n classes

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Figure 3

S t i m u l u s conditions

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Figure 4

S u m m a r y of directional preferences for population of neurons encountered

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Figure 5

P o s t - s t i m u l u s time histograms: toward-preferring n e u r o n

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Figure 6

P o l a r plots: toward-preferring neurons

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Figure 7

P o s t - s t i m u l u s time histograms: away-preferring n e u r o n

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Figure 8

P o l a r plots: a w a y - p r e f e r r i n g neurons

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Figure 9

Plot of preferred direction of motion i n depth versus response to b i n a u r a l onset a n d offset 35 P l o t of breadth of t u n i n g for motion i n depth versus b i n a u r a l

F i g u r e 10

interaction

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F i g u r e 11

P o s t - s t i m u l u s time histograms: ipsilateral-preferring neuron... 39

F i g u r e 12

P o l a r plots: a z i m u t h - p r e f e r r i n g n e u r o n s

40

F i g u r e 13

P l o t of preferred direction of motion i n a z i m u t h versus ear dominance

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F i g u r e 14

P o s t - s t i m u l u s time histograms: m o n a u r a l - l i k e n e u r o n

45

F i g u r e 15

P o l a r plots: m o n a u r a l - l i k e n e u r o n s

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F i g u r e 16 F i g u r e 17

S c h e m a t i c electrode p e n e t r a t i o n s P o l a r plots and rate/intensity functions: monotonic, velocitydependent unit

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F i g u r e 18 F i g u r e 19

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P o l a r plots a n d rate/intensity functions: non-monotonic, velocity-dependent unit

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P o l a r plots and rate/intensity functions: idiosyncratic u n i t

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V F i g u r e 20 F i g u r e 21

P o l a r plots: and rate/intensity functions: unit

velocity-independent

M o d e l of direction a n d velocity selectivity

58 65

1 EmtODUCTION

One role of sensory systems is to convey information to l i v i n g organisms about s t i m u l i i n the environment. L i v i n g organisms are equipped w i t h receptor end-organs specialized to transduce physical s t i m u l i of a specific sensory modality into electrical impulses; these signals from the receptor organs are then relayed to the central nervous system, where they undergo extensive processing. The result of this signal processing provides organisms w i t h information concerning the nature of s t i m u l i i n the environment (what), a n d the location of these s t i m u l i w i t h respect to the organism (where). T h e focus of this research is the latter aspects of sensory processing, and more precisely on the role of the auditory cortex i n the localization of sound sources m o v i n g i n space.

Sound localization The receptor organs of the v i s u a l , auditory a n d somatosensory systems i n m a m m a l s follow a specific arrangement: r e t i n a l ganglion cells, cochlear h a i r cells a n d cutaneous receptors are organized i n a n orderly a r r a y or sensory epithelium. T h e spatial organization of the sensory e p i t h e l i u m i n these three systems is preserved i n the projections to the central nervous system, i n a socalled point-to-point projection: receptors from neighboring regions of sensory e p i t h e l i u m project to neighboring regions of sensory cortex. I n the v i s u a l and somatosensory systems, this arrangement preserves information about the location of s t i m u l i i n space. I n the v i s u a l system, portions of the r e t i n a receive i n p u t from specific parts of the v i s u a l field, and i n t u r n project to distinct areas of v i s u a l cortex; a s i m i l a r arrangement exists i n the somatosensory system. Therefore, spatial information is preserved i n the ascending v i s u a l and somatosensory pathways and is directly available i n the cortex b y virtue of

2 retinotopic a n d somatotopic projections. T h i s does not hold for the auditory system. The sensory epithelium of the auditory system is the basilar membrane located i n the cochlea of the i n n e r ear. The b a s i l a r membrane codes for sound source frequency (pitch) along its length, and the receptor organs (the h a i r cells of the organ of Corti) also have a n orderly spatial arrangement: h a i r cells located at the base of the b a s i l a r membrane respond to h i g h frequency sound, a n d those located at the apex respond to low frequency sound. T h i s arrangement is due to the mechanical properties of the membrane itself. T h i s tonotopic organization is preserved i n the projections of the auditory pathway to various brainstem nuclei a n d most areas of the auditory cortex. A l t h o u g h frequency coding provides crucial information about the nature of auditory s t i m u l i , i t gives no information about the spatial location of such s t i m u l i because sound sources from a l l directions impinge on a common sensory e p i t h e l i u m extended i n frequency rather t h a n space. Information about sound source location must then be computed a n d extracted b y the central nervous system. O r g a n i s m s equipped w i t h two auditory end-organs can solve the problem of sound localization: the p r i n c i p a l cues for sound localization are differences i n the signals reaching the two ears. These b i n a u r a l cues depend on the spatial location a n d frequency spectrum of the sound source, a n d on the size a n d shape of the receiver's head. The distance between the two ears imposes a n i n t e r a u r a l time difference (ITD) on a r r i v i n g s t i m u l i , r e s u l t i n g i n i n t e r a u r a l disparities i n transient a r r i v a l time a n d i n on-going phase.

I T D s are i m p o r t a n t i n localizing

low frequency sound sources (below about 1500 H z i n humans). The acoustic shadow of the head a n d pinnae generate i n t e r a u r a l intensity differences (IID) w h i c h are useful i n localizing h i g h frequency sound sources (above 1500 H z ) . T h i s so-called duplex theory of sound localization describes accurately how

3 m a m m a l s localize pure tones, u s i n g temporal cues for the lower portion of the audible spectrum a n d intensive cues for the higher portion (Stevens & N e w m a n , 1936). A n o t h e r consequence of the shadowing effect of the head a n d pinnae is the creation of i n t e r a u r a l frequency disparities (IFD), w h i c h m a y be helpful for localizing complex broadband sound sources (Mendelson & Cynader, 1983). The external ear (pinna) also plays a n important role i n sound localization. I n addition to generating i n t e r a u r a l intensity differences, the convolutions of the pinnae and the resonances i n the ear canal differentially amplify or dampen certain frequencies, r e s u l t i n g i n a transformation of the frequency spectrum from the free sound field to the e a r d r u m (Calford & Pettigrew, 1984; P h i l l i p s , Calford, Pettigrew, A i t k i n , & Semple, 1982; Shaw, 1974). T h i s cue is especially important i n localizing broadband sound w i t h h i g h frequency components a n d is thought to underlie vertical sound localization (Brown, Schessler, Moody & Stebbins, 1982; B u t l e r , 1969; Middlebrooks, M a k o u s , & Green, 1989) a n d the resolution of front-to-back ambiguities (Musicant & Butler, 1984). A l l the b i n a u r a l sound localization cues l i s t e d above (ITD, I I D a n d I F D ) can be generated w i t h the head i n a fixed position. However, head movements are widely used by animals attempting to locate a sound source. H e a d movements produce a series of changing b i n a u r a l cues w h i c h l i m i t the possible positions of a sound source relative to the receiver ( M i l l s , 1972) a n d significantly improve l o c a l i z a t i o n accuracy i n humans (Thurlow, M a n g e l s , & Runge, 1967; T h u r l o w & Runge, 1967). I n addition to m o v i n g the head, a n i m a l s w i t h moveable pinnae frequently use p i n n a movements w h e n l o c a l i z i n g sound sources. Because most electrophysiological a n d psychophysical studies focus on static localization cues, the importance of head movements i n sound localization is u s u a l l y overlooked.

4 I n t e r a u r a l intensity differences show m a r k e d dependence on the frequency a n d a z i m u t h a l location of the sound source (Irvine, 1987; M a r t i n & Webster, 1989). The I I D / a z i m u t h function is monotonic for the frontal region of space ( w i t h i n about 45 degrees of the m i d l i n e on either side) and i s frequency dependent, being steepest at h i g h frequencies (8 k H z i n the cat). T h i s agrees well w i t h psychophysical data w h i c h shows that localization acuity i n cats a n d monkeys is greatest for h i g h frequency sounds ( M a r t i n & Webster, 1987; Casseday & Neff, 1973) and for s t i m u l i located close to the m i d l i n e (Brown et al., 1982; Heffner & Heffner, 1988). Interaural time differences are also frequency dependent although this effect is relatively independent of the pinnae. A s i n the case of IIDs, I T D s generated by sound sources close to the m i d l i n e provide useful localization cues (Roth, K o c h h a r , & H i n d , 1980). L o c a l i z a t i o n of sound sources implies extracting information about the spatial location of s t i m u l i largely from the b i n a u r a l cues generated by that source. H o w e v e r this process can be reversed: presenting b i n a u r a l sound localization cues through earphones produces a fused auditory image located w i t h i n the head instead of i n the free acoustic field, a n d listeners can locate the sound source accordingly. T h i s task i s called l a t e r a l i z a t i o n (in contrast w i t h the u s u a l task of localization). The b i n a u r a l temporal and intensive disparities that are thought to underlie sound localization of pure tones can be used to lateralize tonal s t i m u l i ; localization a n d l a t e r a l i z a t i o n acuity are s i m i l a r , suggesting that s i m i l a r mechanisms underlie l o c a l i z i n g i n t e r n a l a n d external sound sources (Jeffress & Taylor, 1961). Moreover, the lateralization acuities of cats a n d humans are comparable (Wakeford & Robinson, 1974; Yost, 1974).

Auditory system The organization of the central auditory system is more complex t h a n that

5 of other sensory systems: i n contrast w i t h the somatosensory system where information can reach the cortex w i t h as few as two synapses, or the v i s u a l system where there i s only one major relay nucleus, information from the h a i r cells i n the i n n e r ear passes through several nuclei before reaching the auditory cortex, a n d the interconnections between the various nuclei are intricate. Several distinct auditory areas exist at the level of the cortex. I n addition, parallel descending pathways add to the complexity of this system. A simplified scheme of the ascending auditory pathway is shown on figure 1. Neurons w i t h cell bodies i n the spiral ganglion synapse w i t h the h a i r cells of the organ of Corti; the axons form the auditory nerve (the auditory part of the eighth c r a n i a l nerve) and terminate i n the dorsal a n d v e n t r a l divisions of the cochlear nucleus. F r o m the cochlear nucleus, fibers ascend i n the dorsal acoustic stria (stria of Monakow) and the intermediate stria of H e l d to the contralateral l a t e r a l lemniscus a n d inferior colliculus, sending collaterals along the w a y to b r a i n s t e m nuclei. Fibers from the cochlear nucleus also ascend i n the trapezoid body, sending collaterals to the superior olivary complex of the b r a i n s t e m before synapsing c o n t r a l a t e r a l ^ i n the l a t e r a l lemniscus and/or the inferior colliculus. T h e m e d i a l superior olive is p a r t i c u l a r l y noteworthy: i t is the first nucleus i n the ascending auditory pathway w h i c h receives i n p u t from both ears. F i b e r s from the superior olivary complex project b i l a t e r a l l y to the l a t e r a l lemniscus a n d the inferior colliculus. The latter i s the m i d b r a i n auditory area; it sends fibers to the thalamic auditory nucleus (the m e d i a l geniculate body), w h i c h i n t u r n projects to the auditory cortex. A l t h o u g h ascending projections from the cochlear nucleus are largely contralateral, there are significant crossed connections from the level of the l a t e r a l lemniscus u p w a r d , that the inferior colliculus, the m e d i a l geniculate body and the auditory cortex a l l receive b i n a u r a l information. A s c e n d i n g projections preserve the tonotopic organization of the

6

Figure 1. Schematic representation of the m a m m a l i a n ascending auditory

pathways. D C N : dorsal cochlear nucleus; V C N : v e n t r a l cochlear nucleus; L S O : l a t e r a l superior olive; M S O : medial superior olive; N T B : nucleus of the trapezoid body; L L : l a t e r a l lemniscus; I C : inferior colliculus; M G : m e d i a l geniculate nucleus of the thalamus; S H : stria of H e l d ; S M : s t r i a of M o n a k o w (from M o l l e r , 1983).

7 cochlea so that frequency coding is present at a l l levels of the auditory pathway. The auditory cortex is made up of several distinct auditory areas. In the cat, as m a n y as eight distinct fields have been identified, and about a t h i r d of the auditory cortex is non-tonotopically organized (Reale & Imig, 1980). The most prominent are the p r i m a r y and secondary auditory fields ( A l a n d A l l ) , the anterior auditory field ( A A F ) , and the posterior a n d ventroposterior auditory fields ( P A F a n d V P A F ) . C o n t r a r y to what its name may i m p l y , the p r i m a r y auditory cortex is not the only site receiving direct thalamic input; rather, several parallel projections r u n from the m e d i a l geniculate body to the different auditory fields so the a l l fields receive equally direct thalamic input. There are two largely segregated thalamocortical auditory projection systems i n the cat: a tonotopic projection to A l , A A F , P A F a n d V P A F , a n d a non-tonotopic projection to A l l and other secondary regions (Andersen, K n i g h t , & M e r z e n i c h , 1980). I n addition, various i n t r a c o r t i c a l a n d interhemispheric connections also exist (Brugge & Imig, 1978; M a t s u b a r a & P h i l l i p s , 1988). A l l nuclei of the ascending pathway receive i n p u t from higher levels. The descending auditory pathway of made up of two systems: the corticothalamic system w h i c h terminates i n the m e d i a l geniculate body, a n d the corticocochlear system w h i c h is a widely distributed network of connections to a l l nuclei of the ascending pathway, extending to the cochlear h a i r cells ( H a r r i s o n & Howe, 1975). The descending pathways are thought to exert a n i n h i b i t o r y influence of the activity of the ascending pathway. A salient feature of signal processing i n the auditory system (which is probably true of other sensory systems as well) is its increasing complexity as one ascends the auditory pathway. The m a n y nuclei of the ascending auditory pathway are not mere relays; signals from the cochlear h a i r cells are extensively processed. I n the i n n e r ear a n d auditory nerve, one can record the cochlear

8 microphonic, a n electrical potential w h i c h faithfully reproduces the waveform of a sound w i t h little distortion. Neurons at lower levels of the pathway respond throughout the length of the stimulus; these sustained responses are gradually replaced by transient responses at higher levels, a n d are v i r t u a l l y absent from the cortex. B r a i n s t e m auditory neurons show phase-locking; again, these responses gradually disappear at the level of the m i d b r a i n a n d are absent i n the thalamus a n d cortex. I n the auditory cortex, r a p i d l y adapting neurons predominate; transient excitatory responses are common a n d responses to sound offset also appear. Cortical neurons also respond w e l l to frequency a n d amplitude modulated sound (Mendelson & Cynader, 1985; P h i l l i p s , Mendelson, Cynader, & Douglas, 1985; Schreiner & U r b a s , 1988). O v e r a l l , neurons i n lower auditory centers show l i t t l e adaptation; i n higher centers a n d especially i n the cortex, neurons show more adaptation, g i v i n g more transient responses, a greater variety of response patterns and strong excitatory a n d i n h i b i t o r y responses.

C o r t i c a l neurons respond best to change a n d show r a p i d adaptation;

the i n c r e a s i n g complexity i n signal processing i n the ascending auditory p a t h w a y allows these neurons to enhance change, a n d i n t u r n , neuronal adaptation saves channel capacity i n the cortex (Moller, 1983).

Primary auditory cortex Information about sound source frequency is preserved i n the p r i m a r y auditory cortex. A r e a A l is tonotopically arranged: isofrequency bands r u n dorsoventrally, w i t h h i g h frequencies located r o s t r a l l y a n d l o w frequencies more caudally (Merzenich, K n i g h t , & R o t h , 1975; P h i l l i p s & Irvine, 1981a). Neurons i n area A l are sharply tuned to sound frequency; i n addition, neurons found w i t h i n the same perpendicular penetration show s i m i l a r frequency t u n i n g , w h i c h is evidence for some form of columnar organization i n the auditory cortex w i t h

9 respect to frequency (Merzenich et a l . , 1975). There is also a gradient for breadth of frequency t u n i n g i n A l : neurons i n the dorsal part show narrower frequency t u n i n g and those i n more v e n t r a l locations are more broadly tuned (Schreiner & Cynader, 1984). T h e rate/intensity functions of the responses of p r i m a r y auditory neurons can be monotonic or non-monotonic, although the latter are less frequent (Phillips & Irvine, 1981a). M o s t neurons i n A l respond well to s t i m u l a t i o n of the contralateral ear, a n d respond differently to m o n a u r a l a n d b i n a u r a l s t i m u l a t i o n . The responses of A l neurons to b i n a u r a l s t i m u l a t i o n can be classified i n one of three functional categories: 1- E E units (excitatory/excitatory) i n w h i c h the response evoked by s t i m u l a t i o n of the dominant ear is facilitated by simultaneous s t i m u l a t i o n of the other ear; 2- E I a n d I E units (excitatory/inhibitory and vice versa) i n w h i c h the response evoked by s t i m u l a t i o n of the dominant ear is i n h i b i t e d b y simultaneous s t i m u l a t i o n of the other ear; 3- E O units (monaural) i n w h i c h the response evoked by s t i m u l a t i o n of one ear is unaffected by b i n a u r a l s t i m u l a t i o n (Imig & A d r i a n , 1977; figure 2). Neurons found along the same electrode penetration tend to display s i m i l a r b i n a u r a l interactions, suggesting that area A l is organized i n v e r t i c a l b i n a u r a l interaction columns. These columns are grouped together i n bands w h i c h are oriented orthogonal to the isofrequency bands (Middlebrooks, Dykes, & Merzenich, 1980).

The role of the primary auditory cortex in the encoding of sound source location Three k i n d s of experiments have attempted to delineate the role of the p r i m a r y auditory cortex i n sound localization: electrophysiological experiments u s i n g sealed systems to present b i n a u r a l sound localization cues, electrophysiological experiments u s i n g free-field s t i m u l i , a n d studies of sound localization behavior following selective cortical lesions. The first type of

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Binaural interaction types

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EE

EI

IE

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contralateral ear stimulation ipsilateral ear stimulation binaural stimulation

Figure 2. B i n a u r a l interaction classes of p r i m a r y auditory cortex neurons. E E : excitatory/excitatory (binaural facilitation); E I : excitatory/inhibitory (contralateral-ear-dominated w i t h b i n a u r a l inhibition); I E : inhibitory/excitatory (ipsilateral-ear-dominated w i t h b i n a u r a l inhibition); E O : m o n a u r a l (no b i n a u r a l interaction).

11

experiments has demonstrated that neurons i n the p r i m a r y auditory cortex of the cat are sensitive to b i n a u r a l sound localization cues (IIDs, I T D s , and IFDs) corresponding to the frontal and contralateral regions of auditory space (Brugge, Dubrovsky, A i t k i n , & Anderson, 1969; Kitzes, Wrege, & Cassady, 1980; Mendelson & Cynader, 1983; P h i l l i p s & Irvine, 1981b; Reale & Kettner, 1986). The selectivity of A l neurons to i n t e r a u r a l time, intensity a n d frequency differences is related to b i n a u r a l response category. Preferences for IIDs a n d I T D s seem to result from the interaction of excitatory and/or i n h i b i t o r y events evoked by s t i m u l a t i o n of each ear; the b i n a u r a l response i n such cells is dependent on the t i m i n g of the sequence of excitatory and inhibitory events at the site of interaction, w h i c h i n t u r n depends on stimulus intensity (Brugge et a l . , 1969; K i t z e s et a l . , 1980). Free-field studies have demonstrated that A l neurons are sensitive to the spatial location of pure tone a n d noise s t i m u l i . A g a i n , A l neurons seem to respond best to sound sources located i n the frontal a n d contralateral sound fields (Eisenman, 1974; Benson, H i e n z , & Goldstein, 1981). Middlebrooks and Pettigrew (1981) have proposed that p r i m a r y auditory neurons can be classified i n one of three classes of spatial receptive fields based on their sensitivity to s t i m u l u s location: hemifield units, w h i c h respond to sound i n the contralateral sound hemifield; a x i a l units, w h i c h respond to sound i n the acoustic axis of the contralateral p i n n a ; a n d omnidirectional units, w h i c h respond to sound from any direction i n front of the a n i m a l . These auditory spatial receptive fields are computational: they are not derived from a point-to-point map from the i n n e r ear to the cortex b u t are computed from comparisons of the signals at the two ears. However, despite the existence of location-sensitive units i n the p r i m a r y auditory cortex of the cat, there is no indication of a systematic map of auditory space i n area A l (Middlebrooks & Pettigrew, 1981).

12 L e s i o n to the p r i m a r y auditory cortex spare intensity a n d frequency d i s c r i m i n a t i o n abilities but produce permanent sound localization deficits i n the sound field contralateral to the lesion. T h i s conclusion has been reached i n studies w i t h cats (Jenkins & Masterton, 1982), dogs (Heffher, 1978) and monkeys (Heffner & M a s t e r t o n , 1975). Comparisons between lesions to area A l and to other auditory cortical fields indicate that among other auditory cortical fields, i n t e g r i t y of area A l is necessary and sufficient for n o r m a l b i n a u r a l sound localization behavior. A r e a A l i n each hemisphere contributes p r i m a r i l y to location representation i n the contralateral sound field (Phillips & Gates, 1982; J e n k i n s & M e r z e n i c h , 1984). The sensitivity of auditory neurons to b i n a u r a l sound localization cues and to the spatial location of sound sources, and the importance of the p r i m a r y auditory cortex for accurate sound localization indicate that area A l of the auditory cortex plays a n essential role i n directional hearing.

Real and simulated auditory movement A l l of the research cited above has been carried out u s i n g stationary sound sources, or correlates of such sounds. Y e t , a conspicuous feature of auditory s t i m u l i i n the environment is their motion w i t h respect to the receiver. Despite this prominence, auditory movement as a stimulus feature has largely been overlooked b y most investigators of the psychophysics a n d neurophysiology of sound localization. A l t h o u g h m u c h progress has been made i n understanding static sound localization, little is k n o w n about how the auditory system extracts information about s t i m u l u s motion. A s sound sources move across the auditory field, they provide the auditory system w i t h a series of changing b i n a u r a l disparities. I n particular, movement of a sound source i n a z i m u t h produces modulations of i n t e r a u r a l differences i n

13 intensity, on-going phase a n d frequency spectrum; the rate of change i n these b i n a u r a l cues is a correlate of sound source velocity. Therefore i t is possible to simulate sound source movement without actually p r o v i d i n g real motion, by presenting correlates of motion (modulated IIDs, I T D s a n d I F D s ) to a listener v i a earphones or speakers; dichotic modulations of both I T D s a n d IIDs can produce simulated auditory motion, a n d subjects can lateralize such s t i m u l i . Briggs and Perrott (1972), and Perrott (1974) demonstrated auditory apparent movement by presenting h u m a n subjects w i t h dichotic noise s t i m u l i of v a r y i n g i n t e r s t i m u l u s onset. A t optimal i n t e r s t i m u l u s onset, subjects perceived two sounds as one continuous m o v i n g sound; these findings concerning auditory motion perception coincided w i t h those obtained from free-field studies. However, the temporal disparities used i n this study to simulate auditory motion (tens or hundreds of milliseconds) were not faithful representations of the actual temporal cues used by the auditory system for sound localization, w h i c h are i n the order of tenths of milliseconds. A l t a i a n a n d V i s k o v (1977) used continuous modulations of i n t e r a u r a l phase differences i n a dichotic p a r a d i g m (click trains of v a r y i n g i n t e r a u r a l time delays) to simulate auditory motion; these s t i m u l i were derived from actual I T D s generated by sound sources m o v i n g i n a z i m u t h . S u c h s t i m u l i produced a fused auditory image ( F A I ) w h i c h moved w i t h i n the head, and evoked a distinct sensation of auditory motion i n h u m a n subjects.

I n addition, subjects

could make velocity discriminations based on perceived F A I movement. G r a n t h a m (1984, 1986) came to s i m i l a r conclusions by presenting subjects w i t h amplitude modulated narrow-band noise v i a distant speakers to simulate horizontal auditory motion. In a n attempt to delineate the role of the auditory cortex i n localizing m o v i n g sound sources, A l t m a n a n d K a l m y k o v a (1986) lesioned the auditory cortex of dogs a n d tested their subsequent ability to lateralize signals s i m u l a t i n g

14

auditory movement. B i l a t e r a l lesions completely eliminated the a b i l i t y to discriminate the direction of simulated auditory motion, and u n i l a t e r a l lesions produced a lateralization deficit on the side contralateral to the lesion. These lesion effects parallel those found w i t h static s t i m u l i (Jenkins & Masterton, 1982; Heffner, 1978; Heffner & Masterton, 1975). However, because different regions of auditory cortex were not selectively lesioned, no conclusions could be d r a w n regarding w h i c h auditory field i n p a r t i c u l a r is involved i n processing of information about stimulus motion. A l t h o u g h these findings have not been replicated i n free-field situations, they still highlight the importance of the auditory cortex for dynamic sound localization. Because neurons i n the p r i m a r y auditory cortex are sensitive to the location of sound sources but show r a p i d adaptation to static s t i m u l i , one might expect t h a t some neurons i n area A l w o u l d respond w e l l to sound source movement w i t h i n their spatial receptive fields. A l s o , given the fact that A l neurons are sharply tuned to b i n a u r a l disparities corresponding to certain sound source locations, a n d given the propensity of auditory cortical neurons for change, one could presume that the direction a n d rate of change of b i n a u r a l disparities (which are correlates of direction a n d velocity of auditory motion, respectively) could evoke strong responses from these neurons. S u r p r i s i n g l y , there are few reports of sensitivity to movement of sound sources by neurons of the auditory cortex. Sovijarvi and H y v a r i n e n (1974) presented continuous pure tones m o v i n g horizontally a n d vertically i n a free field situation, a n d found neurons i n the p r i m a r y auditory cortex of the cat w h i c h were sensitive to the direction of sound source movement. A l t m a n (1987) studied the responses of A l neurons to modulations of i n t e r a u r a l phase disparity i n a sealed system, a n d found neurons w h i c h responded selectively to the direction of phase change, a correlate of sound source motion i n a z i m u t h . These two reports were the first to

15

point to the existence of motion detecting mechanisms i n the auditory cortex. However, i n neither report was the degree of directional selectivity quantified or further analyzed i n terms of possible u n d e r l y i n g mechanisms.

I n addition,

relatively few motion-sensitive units were reported, a n indication that such units i n the p r i m a r y auditory cortex of the cat may be relatively rare, as opposed to the more common location-sensitive units (Middlebrooks & Pettigrew, 1981). The a i m of this study is twofold: to confirm a n d assess the existence and prevalence of motion-sensitive neurons i n the p r i m a r y auditory cortex of the cat, and to investigate the mechanisms u n d e r l y i n g this sensitivity to auditory motion i n terms of k n o w n response characteristics of auditory cortical neurons.

Implementation and predictions A s previously mentioned, moving sound sources produce a series of changing b i n a u r a l disparities. One correlate of auditory motion i n space i s modulation of sound intensity at the receiver's ears. W h e n a sound source moves toward or away from the receiver along the m i d l i n e , the two ears receive correlated (diotic) increases or decreases i n sound intensity. W h e n a sound source moves across the receiver's auditory field along the horizontal plane, the two ears receive opposite-directed (dichotic) changes i n sound intensity: sound intensity increases i n one ear a n d simultaneously decreases i n the other ear. Presenting these diotic and dichotic changes i n intensity at the two ears through earphones produces a s i m u l a t i o n of auditory motion: a fused auditory image appears to move w i t h i n the head, as was produced by A l t a i a n and V i s k o v (1977) w i t h modulations of i n t e r a u r a l time delay. To determine the sensitivity of auditory neurons to modulated IIDs, one can present this correlate of sound source motion directly into the ears of a n a n i m a l a n d simultaneously record the electrical activity of A l neurons evoked by this stimulus.

16 P r e s e n t i n g modulated i n t e r a u r a l intensity differences t h r o u g h earphones can simulate motion of real world sound sources without actually p r o v i d i n g that motion. T h i s p a r a d i g m has advantages a n d shortcomings. One obvious l i m i t a t i o n of u s i n g earphones instead of free-field s t i m u l i is the fact that the modifying effects of the head and pinnae on the incoming signal are bypassed altogether.

T h i s results i n a stimulus containing less information, because some

sound l o c a l i z a t i o n cues n o r m a l l y present i n the free sound field are missing. A n o t h e r l i m i t a t i o n is due to the signal itself: modulations of IIDs as the only auditory motion cue is a n incomplete stimulus. U s i n g the same p a r a d i g m but adding other motion cues to the stimulus (modulations of frequency spectrum, time of a r r i v a l a n d on-going phase) w o u l d produce a more accurate s i m u l a t i o n of auditory motion. I n t u r n , a more complete stimulus m a y help uncover a neural m e c h a n i s m specialized to detect m o v i n g sound sources by p r o v i d i n g additional information to such a system. T h e l i m i t a t i o n s of t h i s p a r a d i g m may result i n perceptual ambiguities: for example, i t is impossible for a receiver to distinguish between the intensity changes associated w i t h sound source movement toward or away from the receiver and actual modulation of the intensity of a stationary sound source. O n a more positive side, modulations of IIDs produce a n appropriate (albeit simplified) s i m u l a t i o n of sound source movement that can be easily implemented i n a calibrated, sealed sound delivery system. I n addition, presenting only one motion cue eliminates possible interactions among stimulus parameters a n d facilitates the interpretation of results. Aside from responses to intensity correlates of auditory motion, other response characteristics of A l neurons w i l l be investigated: a u r a l dominance, b i n a u r a l interaction category, transient on a n d off responses, a n d monotonicity of the rate/intensity function. F r o m these response characteristics, some predictions can be made regarding selectivity to direction of auditory motion: 1-

17 neurons w i l l prefer simulated auditory motion into the hemifield corresponding to the dominant ear; 2- neurons w i t h facilitatory b i n a u r a l interactions w i l l prefer simulated auditory motion toward the receiver; 3- neurons w i t h i n h i b i t o r y b i n a u r a l interactions w i l l prefer simulated auditory motion i n a z i m u t h , away from the ear producing i n h i b i t i o n and toward the ear producing excitation; 4neurons w i t h off responses w i l l prefer simulated auditory motion i n directions opposite those specified above; 5- a neuron's preference for slow or fast simulated auditory motion w i l l depend on the monotonicity of its rate/intensity function. These predictions w i l l be verified, along w i t h possible interactions among the response characteristics of the units encountered a n d their r e s u l t i n g sensitivity and selectivity to direction of simulated auditory motion.

18

METHODS

Animal preparation Acute experiments were performed on 7 healthy adult cats. S u r g i c a l anesthesia was induced w i t h sodium pentothal (10 mg/kg i.v. i n i t i a l l y ) ; additional doses were administered d u r i n g surgery to m a i n t a i n areflexia. To prevent excessive salivation and respiratory difficulties, a single dose of atropine sulfate (0.2 mg, i.v.) was administered. Dexamethasone (0.5 mg, i.m.) was administered to prevent b r a i n edema. A tracheotomy was performed a n d a n endotracheal tube inserted. The a n i m a l was supported by a head-holder w h i c h left the s k u l l a n d pinnae free from obstruction. T h e s k u l l a n d auditory meatuses were cleared of s u r r o u n d i n g tissue. A 5-mm diameter hole was d r i l l e d i n the s k u l l overlying the left ectosylvian gyrus (area A l ) , a n d the intact d u r a was covered w i t h petroleum jelly to keep i t from drying. The auditory meatuses were transected a n d the pinnae reflected anteriorly to allow insertion of the stimulus delivery system (hollow a l u m i n u m acoustic couplers) directly into the ear canals. A l l wounds a n d pressure points were i n f i l t r a t e d w i t h a long-acting local anesthetic (bupivacaine hydrochloride 2.5%). W h e n surgery was completed, sodium pentothal anesthesia was discontinued. The a n i m a l was paralyzed (gallamine triethiodide 20 mg, i.v.) a n d artificially respired w i t h a 70:30 m i x t u r e of nitrous oxide and oxygen. T h e a n i m a l was m a i n t a i n e d on a continuous intravenous infusion of gallamine triethiodide (10 mg/kg/hr), sodium pentobarbital (1 mg/kg/hr) and 5% lactated dextrose (10 ml/hr) i n Ringer's. E n d - t i d a l CO2, heart rate, blood pressure a n d E E G were monitored continuously. Rectal temperature was m a i n t a i n e d at 38°C u s i n g a feedback-controlled heating blanket; expired CO2 was m a i n t a i n e d at about 4% by adjusting the rate of the respiration pump.

19

Stimuli P u r e tone sinusoids were generated by a Wavetek model 110 function generator.

Signals to the speakers were controlled by two digital-to-analog

converters of the P D P / 1 1 computer, a n d fed through a n analog m u l t i p l i e r and an amplifier (Technics SU-700 stereo integrated amplifier). T h e s t i m u l u s delivery system consisted of two loudspeakers (Pioneer W X X - 1 7 2 ) connected to hollow a l u m i n u m acoustic couplers w h i c h fitted snugly into the transected auditory meatuses. The s t i m u l i employed were amplitude modulated pure tones w h i c h simulated auditory motion i n four canonical directions. L i k e - d i r e c t e d changes i n sound intensity at both ears simulated movement toward or away from the head along the m i d l i n e ; opposite-directed changes i n sound intensity simulated sound m o v i n g along the a z i m u t h a l plane, toward one ear a n d away from the other, and vice versa (figure 3 A , B ) . Since the duration of the A M ramp was constant at 250 msec, A M r a m p rate a n d excursion i n these experiments are correlates of sound source velocity: increased r a m p excursion a n d rate correspond to higher velocities of sound source motion. E a c h of the four simulated directions of motion was presented at four different rates of rise of the A M ramp; the four different intensity levels spanned 24 d B , i n four 6 d B increments (figure 3C). The s t i m u l i were shaped w i t h envelope generators to produce rise and fall times of 5 ms; i n t e r a u r a l phase was always zero. S t i m u l u s time course is shown on figure 3 D . S t i m u l u s onset occurred at 150 msec a n d was followed by a 295 ms plateau; the A M ramps s i m u l a t i n g auditory motion occurred between 450 and 700 msec, a n d were followed by another 295 ms plateau and stimulus offset at 1000 msec. Total data collection time was 1300 ms, w i t h a 200 ms w a i t time between each stimulus presentation. There were 40 presentations for each condition, for a total of 640 stimulus presentations (4 directions of motion x 4

20

Figure 3 . Representation of s t i m u l i used to simulate auditory motion i n space. P u r e tones are presented to the two ears through a sealed system. A: Correlated increases or decreases i n sound level at the two ears simulate auditory motion i n depth. B: Opposite-directed changes i n sound level at the two ears simulate auditory motion i n a z i m u t h . C: F o u r different ramp rates a n d excursions corresponding to the four velocity conditions. D: S t i m u l u s time course.

21

22 r a m p excursions x 40 presentations) for each unit.

Calibration A probe microphone ( I V I E 1300) was inserted i n the acoustic couplers for in situ measurement of sound pressure levels near the tympanic membrane.

A

waveform analyzer (DataPrecision D a t a 6000) produced fast F o u r i e r transforms of the sound spectra. The output of a B r u e l and Kjaer pistonphone (124 d B at 250 H z ) was used to convert relative intensity measurements into sound pressure level (dB S P L re 20 ( i N / m ) . V a r i a t i o n s i n sound intensity at different frequencies 2

were corrected w i t h reference to the output of the waveform analyzer. Sound levels were calibrated at the beginning of each experiment a n d monitored on-line throughout the experiment.

Data collection The a n i m a l was located i n a sound-attenuating chamber ( I A C Controlled Acoustic E n v i r o n m e n t s ) . Except for the sound delivery system, microdrive, stereotaxic apparatus, table and a n i m a l , a l l of the equipment used (infusion pump, respirator, computer, etc.) was located outside the chamber.

The

responses of single neurons i n area A l were recorded e x t r a c e l l u l a r l y u s i n g glass-insulated p l a t i n u m - i r i d i u m microelectrodes w i t h impedances of 1-1.5 M Q at 1 k H z (Wolbarsht, M a c N i c h o l , & Wagner, 1960). Electrodes were advanced perpendicularly through the dura a n d cortex u s i n g a remote controlled microdrive. Signals from the electrode were bandpass filtered (500 H z to 12 k H z ) , amplified (lOOOx), discriminated w i t h a window discriminator a n d monitored on a n oscilloscope a n d a n audio monitor (Grass A M 8 ) . S t i m u l u s presentation and on-line data collection a n d display were controlled by the P D P / 1 1 computer v i a a n I B M P C serving as a n intelligent t e r m i n a l .

23 W h i t e noise and pure tone bursts were used as search s t i m u l i . W h e n a u n i t was encountered, its characteristic frequency ( C F ) was determined. S t i m u l u s presentation was done at C F , although additional frequencies were sometimes used. The 16 stimulus conditions delineated above were i n d i v i d u a l l y interleaved a n d presented i n a randomized order. T h i s process was repeated for a total of 40 trials at w h i c h point data collection for a n i n d i v i d u a l unit terminated. The total length of a n experiment was 2-3 days; recording time was 12-36 hours. W h e n recording was completed, the a n i m a l was k i l l e d w i t h a n intravenous injection of sodium pentobarbital (100 mg/kg). The s k u l l was opened to verify electrode placement u s i n g anatomical l a n d m a r k s a n d previous maps of the auditory cortex surface (Schreiner & Cynader, 1984).

Data analysis The computer generated post-stimulus histograms a n d spike counts for a l l s t i m u l u s conditions. A u r a l dominance a n d b i n a u r a l i n t e r a c t i o n category were determined by comparing responses to s t i m u l a t i o n of the contralateral ear alone, stimulation of the i p s i l a t e r a l ear alone and s t i m u l a t i o n of both ears d u r i n g s t i m u l u s onset. Responses to stimulus offset were examined i n a s i m i l a r way. Responses to correlates of the four different directions of motion were determined b y a n a l y z i n g responses d u r i n g the A M ramps. Preferred direction of movement i n depth was determined by comparing responses to simulated sound source movement toward and away from the receiver (correlated b i n a u r a l increases a n d decreases i n sound levels, respectively); s i m i l a r l y , preferred direction of movement i n a z i m u t h was determined b y comparing responses to i p s i l a t e r a l - a n d contralateral-directed simulated sound source movement (increasing sound level i n one ear a n d decreasing sound level i n the other ear, a n d vice versa). U n i t s w h i c h gave weak responses to A M ramps (less t h a n one

24 spike per sweep) were classified as insufficiently responsive a n d not evaluated further. A 2:1 ratio between responses to opposed directions of motion along one dimension (depth or azimuth) was t a k e n as the criterion for directional selectivity. I n addition, responses to simulated auditory motion i n one dimension h a d to be at least 1.5 times stronger t h a n those evoked by simulated auditory motion i n the other dimension. F o r a l l analyses, spontaneous activity was subtracted from the spike counts and response latencies were t a k e n into account.

/

25

RESULTS

D a t a were obtained for a total of 80 neurons. Nineteen neurons d i d not respond well to the A M ramps and w i l l not be described further.

The

characteristic frequencies of the r e m a i n i n g 61 units ranged from 2 to 44 k H z . In general, sharp s t i m u l u s onsets (5 msec rise times) typically produced strong transient responses; the discharge elicited by the A M ramps was more sustained.

Directional selectivity Three-quarters (61/80) of the units encountered responded to correlates of auditory motion. The majority of these A M - s e n s i t i v e units (54/61) responded selectively to the direction of auditory motion a n d were classified according to preferred direction of s i m u l a t e d sound source motion. Three broad categories of directional selectivity were observed: 1- selectivity for correlates of auditory motion i n depth (toward or away from the receiver), 2- selectivity for correlates of auditory motion i n a z i m u t h (ipsilateral- or contralateral-directed), a n d 3selectivity for auditory motion directed both toward the receiver a n d i n a z i m u t h (monaural-like responses).

A s m a l l number of units (n=7) responded to A M

ramps but d i d not show any selectivity for a particular direction of motion. The d i s t r i b u t i o n of units falling into each of the major groups is s u m m a r i z e d i n figure 4. I n this figure the perspective is from above the head of the a n i m a l and the receiver is positioned at the bottom of the figure. The horizontal axis represents a z i m u t h ; the vertical axis represents depth. Recordings were made from the left hemisphere; hence the left ear is i p s i l a t e r a l to the recording site, a n d the right ear contralateral. The length of each arrow is proportional to the n u m b e r of u n i t s preferring a p a r t i c u l a r direction of s i m u l a t e d sound source

26

away 3

monaural-like (contra) 20 toward

Figure 4. Summary of directional preferences for all direction-selective units encountered (n=54). The perspective is from directly above the head of the animal. The vertical axis corresponds to depth; the horizontal axis corresponds to azimuth. Recordings are assumed to be made from left hemisphere. The length of each arrow is proportional to the number of units preferring a particular direction of simulated sound source motion; the numeral next to each arrow indicates the number of such units that were encountered. Oblique arrows refer to monaural-like units; these units showed equal preference for increases in sound level in both ears and in one ear alone. Units not included in this figure were those which did not show any directional preference (n=7), and those which did not respond to correlates of sound source motion (n=19).

27 motion; the accompanying n u m e r a l indicates the number of units i n each category. Oblique arrows refer to units w h i c h responded equally well to motion directed toward the receiver and i n one a z i m u t h a l direction (monaural-like units; see section C). N o t included i n this figure are seven units w h i c h showed no directional preference, and nineteen units w h i c h d i d not respond to A M ramps.

A . Motion in depth U n i t s preferring simulated sound source motion i n depth comprised 37% (23/61) of a l l motion-sensitive units sampled. M a n y more of these units responded selectively to increases t h a n to decreases i n sound level (more towardt h a n away-preferring units were found; see figure 4). Toward-preferring units gave transient responses to b i n a u r a l stimulus onset a n d sustained responses d u r i n g A M ramps i n both ears. F i g u r e 5 shows post-stimulus time histograms depicting the t i m i n g of a toward-preferring neuron's discharge i n relation to the time course of the stimulus (shown below each histogram), for the four directions of s i m u l a t e d auditory motion. T h i s neuron responds well to m o n a u r a l stimulus onset i n the contralateral ear (top left panel) but gives weak responses to stimulus onset i n the i p s i l a t e r a l ear (bottom left panel). The response to b i n a u r a l stimulus onset is stronger t h a n the s u m of both m o n a u r a l responses (bottom r i g h t panel), i n d i c a t i n g strong facilitation ( E E b i n a u r a l interaction type). O n each histogram, a horizontal l i n e m a r k s the responses to intensity correlates of auditory motion. There is v i r t u a l l y no response above background for ipsilateral-directed auditory motion, w h e n the stimulus increases i n amplitude i n the i p s i l a t e r a l ear and decreases i n the contralateral ear (top left panel); the reversed condition, i n w h i c h sound level increases i n the contralateral ear a n d decreases i n the ipsilateral ear, produces a weak response (bottom left panel). B y contrast, the

28

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