Detection of small across-channel timing di¡erences bycochlear implantees

Robert P. Carlyon a;*, Luc Geurts b, Jan Wouters b

a MRC Cognition and Brain Sciences Unit, 15 Chaucer Rd., Cambridge, CB2 2EF, UKb Lab. Exp. ORL, KU Leuven, Kapucijnenvoer 33, 3000 Leuven, Belgium

Received 12 March 1999; received in revised form 18 November 1999; accepted 26 November 1999

Abstract

Five post-lingually deafened users of the LAURA cochlear implant were presented with two trains of biphasic pulses appliedconcurrently to two widely separated channels. They could all discriminate between stimuli where pulses on the two channels werenearly synchronous (inter-channel delay = 0.1 ms) and those where there was a longer delay applied to one channel. All showed anasymmetry, being more sensitive when the longer delay was on either the more basal or, depending on the listener, the more apicalchannel. For four out of the five listeners this asymmetry could be at least partly attributed to one stimulus, with a 0.1-ms delay ineither the apical (three listeners) or basal (one listener) channel, sounding markedly different from all other stimuli used in theexperiment. Both the overall sensitivity of listeners and the general pattern of results survived the presentation of maskers onintermediate channels, and did not vary markedly with changes in the polarity of the pulses applied to one channel. Although theresults varied substantially across listeners, it is concluded that they demonstrate a genuine sensitivity to the relative timing ofstimulation applied to discrete populations of auditory nerve fibers. ß 2000 Elsevier Science B.V. All rights reserved.

Key words: Cochlear implant; Across-channel timing; Phase e¡ect

1. Introduction

This article examines the ability of cochlear implant-ees to discriminate ¢ne timing di¡erences between pul-satile stimuli applied concurrently to two channels,which innervate widely separated regions of the cochlea.The ability, if it exists, can be thought of as an electricalanalog of the sensitivity of the normal auditory systemto timing di¡erences between the envelopes of acousticstimuli occupying widely separated frequency regions(Strickland et al., 1989; Yost and Sheft, 1989; Carlyon,1994). As discussed below, there are theoretical reasonsto expect that the sensitivity of implantees to across-channel timing di¡erences might exceed that of normallisteners to across-frequency asynchronies. A demon-stration of such ¢ne sensitivity in conditions wherethe two channels excite discrete populations of auditory

nerve (AN) ¢bers would lead to two important conclu-sions. First, it would show that acoustical stimulationunderestimates the ability of the central auditory systemto compare the pattern of activity between di¡erentpopulations of AN ¢bers. Second, it would indicatethat, even for widely separated channels, the relativetiming between electrical pulses can a¡ect the perceptsexperienced by cochlear implantees. This in turn mightmean that the across-channel delays implemented in the`continuous interleaved sampling (CIS)' strategy (Wil-son et al., 1991) are perceptible, and could have impli-cations for the values of such delays used in future CIS-based algorithms. However, as also discussed below,existing evidence obtained with electrical stimulationdoes not support the existence of a mechanism sensitiveto across-channel timing di¡erences.

Psychoacoustical experiments have shown that nor-mally hearing listeners can detect phase di¡erences ofabout 30^60³ between the envelopes of sinusoidally am-plitude-modulated tones with di¡erent carrier frequen-cies (Strickland et al., 1989; Yost and Sheft, 1989). In

0378-5955 / 00 / $ ^ see front matter ß 2000 Elsevier Science B.V. All rights reserved.PII: S 0 3 7 8 - 5 9 5 5 ( 9 9 ) 0 0 2 1 5 - 4

* Corresponding author. Tel. : +44 (1223) 355294, ext. 720;Fax: +44 (1223) 359062; E-mail: bob.carlyon@mrc-cbu.cam.ac.uk

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those experiments, care was taken to eliminate cuesbased on interactions in neural populations having cen-ter frequencies (CFs) between the two carriers. Typicalprecautions included a narrowband noise presented in afrequency region intermediate to the two carriers, andthe use of well-separated carrier frequencies. Carlyon(1994) performed some similar measurements usingacoustic stimuli more akin to the pulse trains commonlyused in cochlear implant research. He measured thedetection of timing di¡erences between pairs of multi-component complex tones that had been ¢ltered intoseparate frequency regions. For these stimuli, whichresembled bandpass ¢ltered pulse trains, thresholdswere approximately 2.5 ms at all fundamental frequen-cies (F0s). It was concluded that ringing on the basilarmembrane prevented thresholds from dropping belowthis value. Not only will the ringing `smooth out' thestimulus waveform, but it will also do so to a di¡erentdegree in the two frequency regions. In this sense, lis-teners performing an across-frequency timing discrimi-nation are not comparing `like with like' as they arewhen detecting interaural time di¡erences between stim-uli in the same frequency region. In the latter case ring-ing will smooth the two inputs by a similar amount ineach ear, and listeners can detect asynchronies of about10 Ws (e.g. Hafter and Dye, 1983).

In contrast to the acoustic case, concurrent pulsatileelectrical stimulation of di¡erent regions of the cochleamay allow the listener to compare very similar patternsof stimulation applied to di¡erent neural populationsinnervating the same cochlea. Moreover, at least at cur-rent levels well above the threshold of single neurons,auditory nerve responses to electric pulses are verytightly time-locked, and can have latencies whose stand-ard deviations are as low as 8 Ws (van den Honert andStypulkowski, 1987). However, two psychophysicalstudies have concluded that implantees have very poorsensitivity to across-channel timing di¡erences. Tongand Clark (1986) presented two listeners with 100-ppspulse trains concurrently to two electrode channels, andasked them to discriminate between an inter-channeldelay of 5 ms and a larger delay. Thresholds increasedfrom less than 0.5 ms at small electrode separations to1.5 ms and 2.5 ms (depending on the listener) at thewidest separations tested (3.0 and 6.0 mm respectively).They concluded that the lower thresholds obtained atsmall channel separations were due to the two channelsexciting a common population of AN ¢bers. McKayand McDermott (1996) presented periodic pulse trainsto each of two electrode pairs, with each period of eachtrain consisting of one `large' (high-current) pulse andfour smaller ones. They asked listeners to discriminatebetween the case where the delay between the largepulse on one electrode channel and that on the otherwas 1 ms, and conditions where this delay was longer.

They found that performance was at chance when thespatial separation between the electrode channels wasgreater than 4 mm. McKay and McDermott concludedthat listeners could not compare the temporal patternof activation between channels that stimulated non-overlapping populations of AN ¢bers.

One reason for the generally poor performance in thestudies by Tong and Clark and by McKay and McDer-mott may be that, unlike in the psychoacoustical stud-ies, the reference stimulus did not consist of simultane-ous pulses on the two channels. Listeners in acousticexperiments have reported that the percept producedby an above-threshold asynchrony is that of the soundbreaking into two separate sources (Carlyon andShackleton, 1994). It may be that, once this segregationhas occurred, further across-frequency timing di¡eren-ces are not easily detected (cf. van Noorden, 1975). Ifso, then implantees may be better at discriminating be-tween a reference stimulus in which the pulses on twochannels are simultaneous and a signal containing asmall across-channel delay, than they are at discrimi-nating between two large delays (cf. Tong and Clark,1986). A problem with testing this hypothesis is that, inorder to avoid direct electrical interaction betweenchannels, many modern devices ^ including theLAURA implant used by our subjects ^ prohibit trulysimultaneous stimulation. Our approach was to use areference stimulus which was as nearly synchronous aspossible on the two channels (delay = 0.1 ms), and toperform additional controls for the use of within-chan-nel cues. These included, in addition to the selection ofwidely separated channels, the presentation of maskersin electrode channels between the two to be compared.

2. Experiment 1: Psychometric functions

2.1. Method

The stimuli consisted of two concurrent pulse trainsapplied to di¡erent channels of the LAURA cochlearimplant, which contains eight bipolar channels eachconsisting of a pair of ball electrodes (channel 1 beingthe most apical, channel 8 the most basal). The pulsesin each train were biphasic with a duration of 40 Ws/phase and were presented at a rate of 100 pps. Thepulse trains were 400 ms long and were gated on ando¡ with 50-ms linear ramps, the purpose of which wasto discourage the use of di¡erences in onset time be-tween the two channels, as in the psychoacousticalstudy by Carlyon (1994).

All stimuli were checked using a fully functioning testimplant, each channel of which had a 2.2-k6 resistorbetween its two electrodes, and could be connected toone input of a Le Croy 9304AM four-channel digital

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oscilloscope. The oscilloscope traces showed that thepulses had rise-fall times of less than 10 Ws. The two`target' channels were chosen for each subject to be asfar apart as possible (as measured along the length ofthe electrode array) with the constraint that each chan-nel should be capable of producing a sound of su¤cientloudness (see below) for a 100-pps 40 Ws/phase pulsetrain. Details of the target channels are shown foreach listener in Table 1a. X-rays of the prostheses im-planted in two listeners were available and are shown inFig. 1a. Note that for these two listeners the targetchannels, indicated by solid lines, were separated byapproximately one half-turn of the cochlea. (The signif-

icance of the electrodes connected by dashed lines willbe explained in a later section.) Note also that listenersAE (shown) and AP (not shown) were implanted with amore recent version of the electrode array than theother three; the other components of the implant, how-ever, did not di¡er. A schematic representation of thetwo electrode arrays is provided in Fig. 1b.

Before the main experiment, the currents on the twotarget channels were adjusted to be equally loud. First,the current on either the basal (listeners AP and SV) orapical (JV, AE, DD) channel was adjusted, with a res-olution of 10 WAî , until it was judged to correspond tothe middle point, labelled `normal', on a ¢ve-point scale

Fig. 1. a: Tracings of X-rays showing electrode placement for listeners AE and SV. The two electrodes making up each channel used in experi-ment 1 are joined by solid lines. Those joined by dashed lines are the maskers used in experiments 3 and 5. Only one masker could be usedfor listener AE as channel 3 overlapped physically with channel 4, and because it was not possible to produce a su¤ciently loud percept withthe present stimuli on channels 1 and 2. The di¡erent appearance of the X-rays for the two listeners arises from the fact that AE was ¢ttedwith version 5.7 of the array whereas SV was ¢tted with version 5.6. Schematic representations of these two versions of the array are shown inpart (b), where the electrode contacts are indicated by `+' signs.

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ranging from `very quiet' to `very loud'. The currentlevel on the other channel was then adjusted so that itwas judged to be equal in loudness to the ¢rst, follow-ing a procedure in which pulse trains on the `¢xed' and`adjustable' channels were presented in the order `¢xed-adjustable-¢xed', with a 500-ms gap between them. Atthe start of half of the loudness matching runs the loud-ness of the adjustable channel corresponded to `loud'on the ¢ve-point scale; on the other half it corre-sponded to `quiet'. Listeners AE, AP, and SV per-formed six loudness matches each; time constraintsmeant that listeners JV and DD each performed onlytwo matches. All of the adjusted levels were averagedfor each listener to obtain the current to be used forthat channel in the main part of the experiment, and areshown in the rightmost column of Table 1a.1 Note thatany minor di¡erences between the loudnesses of the twoindividual channels would not have provided a reliablecue in the main part of the experiment, in which bothchannels were always stimulated for every presentation.

In the main experiment listeners were required todiscriminate between two stimuli in which both chan-nels were stimulated concurrently, and which di¡eredonly in the relative timing between the two channels.

In one condition the reference stimulus had pulses inthe more basal channel delayed by 0.1 ms (onset toonset) relative to those on the more apical channel,and the signals had delays on the apical channel. Inthe other condition, the pulses in the reference stimuluswere delayed by 0.1 ms on the apical channel, and thepulses in the signal were delayed on the basal channel.In each case, ¢ve di¡erent values of signal delay, rang-ing from 0.1 to 2.0 ms, were used. A schematic repre-sentation of the ¢rst two pulses in each pulse train isshown for a trial in which the signal had a 2-ms basaldelay in the top row of Fig. 2, with a trial containing anapically delayed signal shown in the bottom row. Thecomparisons made in each of these two trials are indi-cated by open triangles on the ¢gure; the meaning ofthe ¢lled triangles will be described later. Close-ups ofthe ¢rst pulse in each channel are shown in Fig. 3a forstimuli with a 0.1-ms delay on the basal (left column)and apical (right column) channel. The other parts ofFig. 3, together with the arrows in part (a), will bedescribed in Section 3.1. All delays are speci¢ed as on-set to onset, and so with a 0.1-ms delay the time be-tween the o¡set of the pulses in one channel and theonset of those in the other was 20 Ws (1003(2U40) Ws;see Fig. 3a). The reference and signal were presented inrandom order with an inter-stimulus delay (o¡set^on-set) of 500 ms. Listeners were required to say whetherthe signal was presented ¢rst or second. In each blockof trials the channel that was delayed in the signal in-terval was always the same, and the reference stimulus

Table 1(a) Details of the target channels are shown for each listener; (b) results of the loudness matching procedure used for the maskers of experi-ment 3

(a) Apical pair(width, mm)

Basal pair(width, mm)

Separ (mm) Electrode array version Current, WAî

(apical, basal)

JV 2 (3) 7 (1.3) 11.1 5.6 (600, 723)AE 4 (3) 8 (2) 7.5 5.7 (1000, 1050)DD 3 (1.3) 6 (1.3) 6.2 5.6 (550, 940)AP 2 (3) 7 (3) 10.0 5.8 (663, 750)SV 2 (3) 6 (1.3) 9.1 5.6 (675, 800)

(b) Channel number Balanced with ATE Balanced with BTE Average Ratio (dB)

JV Apical mask 4 460 467.5 464 0.15Basal mask 8 1127.5 1115 1121 0.10

AE Single mask 6 805 820 812.5 0.16DD Apical mask 4 495 502.5 499 0.13

Basal mask 8 685 750 717.5 0.79AP Apical mask 4 537.5 622.5 580 1.27

Basal mask 8 922.5 932.5 927.5 0.09SV Apical mask 4 613 568 590 0.66

Basal mask 8 840 845 842.5 0.05

(a) Columns two and three show the apical and basal target channels used for each listener. The ¢gures in parentheses give the separation be-tween the electrodes in each channel, in millimeters. The fourth column shows the separation between the two electrode channels measuredfrom points midway between the two electrodes (measured longitudinally, along the axes of the electrode arrays shown in Fig. 1b) in eachchannel. The version of the electrode array implanted in each listener is given in the penultimate column. (b) ATE, apical target electrode;BTE, basal target electrode. The last column shows the ratio in dB between the loudness matches to the two target electrodes.

1 It is possible that some inaccuracy arose in our loudness matchingprocedure from the fact that the adjustable channel was always pre-sented second, and from the fact that listeners sometimes show ordere¡ects. Evidence that such e¡ects are either small or absent will bepresented in Section 4.

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always contained a 0.1-ms delay on the other channel.Each block consisted of ten trials at each inter-channeldelay. The order of the blocks was randomized with theconstraint that blocks of trials with basally delayed sig-nals were interleaved with those containing apically de-layed signals. Ten blocks were run for each signal delay,making a total of 100 trials per point.

As no feedback was given after each trial, the deci-sion as to which of two stimuli to label the signal andwhich the reference is to some extent arbitrary. Notehowever that all listeners had participated in a pilotexperiment using an adaptive procedure in which feed-back was given, with the response being labelled ascorrect whenever the stimulus with the longer inter-channel delay was identi¢ed as the signal. Note alsothat the main experiment included some trials wherethe signal contained a 0.1-ms delay on one channeland the reference contained an identical delay on theother channel. Because the signal was de¢ned as theapically delayed stimulus in some blocks and as thebasally delayed stimulus in others, this meant thatabove-chance performance on one of these conditionswould necessarily lead to below-chance performance onthe other. Indeed, had feedback been provided in these

trials, listeners would have received inconsistent infor-mation as to which stimulus to treat as the signal.

Details of the ¢ve post-lingually deafened subjectswho participated in the experiments are shown in Table2. The last two columns of the table show the percent-age of vowels (10-alternative forced choice) and conso-nants (16-alternative forced choice) correctly identi¢edby each listener in the study by van Wieringen andWouters (1999). All ¢ve scored above the average(42%, S.D. = 19) obtained by 25 listeners in that pre-vious study on the vowel test, and all except AP per-formed above the average (33%, S.D. = 13) consonantidenti¢cation. Four other listeners took part in the pilotexperiment with the adaptive procedure but were not

Fig. 2. (a) Schematic representation of the relative timing of thepulses applied to the basal (B) and apical (A) target channels in theexperiments. Two subsequent pulses in each channel are shown. Thetop row shows a trial in which the signal comes second and con-tains a 2-ms basal delay; in the bottom row the signal comes ¢rstand contains a 2-ms apical delay. The open triangles indicate thecomparisons made during each trial of the main part of experiment1 (inverted triangle = basally delayed signal, upright = apically de-layed signal). Filled triangles correspond to the additional conditionin which the same channel was delayed for both the reference andsignal stimuli. The 0.1-ms asynchronies in the reference stimuli havebeen exaggerated for clarity.

Fig. 3. Schematic showing a close-up of the adjacent pulses on thebasal and apical channels for a 0.1-ms delay applied to the basal(left column) and apical (right column) target channels. Part (a)shows the condition used in experiment 1, which also formed partof experiment 2, where it was termed the `uninverted' condition.Parts (b) and (c) show the `basally inverted' and `both-inverted' con-ditions of experiment 2. The label `apical cathodic' on the right-hand side of the ¢gure indicates the polarity, so that half-pulses inwhich the more apical member of the electrode pair is the cathodeare shown by upward de£ections of the plots. The arrows in parts(a) and (c) indicate speci¢c half-pulses referred to in the text; foreach stimulus, one arrow indicates the half-pulse in which the moreapical electrode in the apical channel is the cathode, and the otherindicates the half-pulse where the more apical electrode of the basalchannel is the anode.

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selected to participate in the present study. One of themwas congenitally deaf and had di¤culty in performingall tasks that we have tested her on, including the adap-tive task and the loudness balancing used here. Twoothers could do the loudness balancing but could nottrack a threshold in the adaptive across-channel asyn-chrony experiment. Both had performed below averageon the vowel and consonant identi¢cation tests (vanWieringen and Wouters, 1999). A fourth could doboth tasks but was rejected because the only two chan-nels which could give rise to su¤ciently loud perceptsfor the present stimuli were channels 2 and 4, whichwere deemed too close to preclude signi¢cant peripheralinteractions.

2.2. Results

The open symbols in each panel of Fig. 4 show thepsychometric functions for one listener. Note that in

this and in subsequent ¢gures, a deviation from chanceperformance in either direction (above or below 50%correct, dashed line) indicates that subjects could dis-criminate between the standard and signal. The mostsalient features of the results are that there are substan-tial inter-listener di¡erences but that all listeners per-formed well above chance in at least one condition.Listeners JV, AE, DD, and AP could all distinguishbetween a stimulus having a 0.1-ms delay on the basalchannel and one having a 0.1-ms apical delay. The ¢rstthree of these listeners (top row) identi¢ed the basallydelayed stimulus as the `signal', and so percent correctfor the basal signal is above 50%, and that for theapical signal below 50%. These listeners also showedhigher scores for basal than for apical signals over arange of larger delays. The converse was true for listen-er AP. Listener SV di¡ered from the others in that hecould not discriminate between basal and apical delaysof 0.1 ms. He did, however, also show an asymmetry in

Fig. 4. Connected open symbols show sensitivity averaged across 100 trials/point for conditions where the signal had a delay on the basal (in-verted triangles) or apical (upright triangles) channel. In these conditions the reference had a 0.1-ms delay on the other channel. Filled uncon-nected symbols show data from a condition where the reference and signal had delays on the same channel; they have been shifted horizontallyby a small amount for clarity. Note that although the ordinate is labelled `% correct', any deviation from chance performance (50%, dashedline) indicates that listeners could discriminate between the standard and signal.

Table 2Details of the ¢ve listeners who participated in the experiments

Listener Age Duration of profound deafness (years) Aetiology Years since implant Vowels (%) Cons (%)

JV 16 3 meningitis 3 53 45AE 41 3 Menie©re's 1 79 51DD 31 1 trauma 2 61 35AP 59 3 Cochlear. otosclerosis 1 53 29SV 29 6 unknown 3 73 58

The third column shows the delay between the onset of profound deafness and implantation. The last two columns show the percentage ofvowels and consonants recognized correctly by each listener in a previous study (van Wieringen and Wouters, 1999). Vowels: 10-alternativeforced-choice, /hVt/ context. Consonants: 16-alternative forced-choice, /aCa/ context.

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that he was generally better at detecting longer delayson the basal than on the apical channel. A furtherunique feature of SV is that he was the only one whoexplicitly described the signals as containing an `echo'.The others described the signals using the Flemish word`zachter', which means `softer' both in the sense of `qui-eter' and `more mu¥ed'.

Before discussing the results in more detail, it isworth noting that, although there was substantial var-iability between listeners, the reliability of the measuresfor a single listener and condition was very high. This isdemonstrated by a reliability coe¤cient of 0.972 (calcu-lated using the Spearman-Brown formula (Fergusonand Takane, 1989, pp. 466^478)) between the ¢rst andsecond halves of the responses making up each datapoint in Fig. 4. It is also worth noting that substantialinter-listener variations have been reported in the detec-tion of interaural time di¡erences between pulse trainspresented to the two implants of bilaterally impairedlisteners (Lawson et al., 1999), a point we will returnto in Section 7.

At ¢rst sight, the results of listeners JV, AE, and DDsuggest that they were exquisitely sensitive to delays onthe basal channel, and less sensitive to apical delays.However, an alternative explanation stems from thefact that the reference stimulus for the basally delayedsignals was di¡erent from that used for the apicallydelayed signals. It may be that this reference stimulus,in which the apical channel was delayed by 0.1 ms,sounded `special' in the sense of producing a perceptthat was qualitatively di¡erent from all other stimuliused in the experiment. Similarly, to account for theresults of listener AP, one could propose that the refer-ence containing a 0.1-ms basal delay was special. Sup-port for this interpretation comes from an additionalexperiment in which JV, AE, and AP had to discrim-inate between a basally or apically delayed signal and areference having a (shorter) 0.1-ms delay in the samedirection. This experiment can be understood withreference to Fig. 2 if one assumes that the two stimulito be compared in each trial are shown in the samecolumn (comparison indicated by the ¢lled symbols),rather than in the same row. The ¢lled symbols inFig. 4 show that the asymmetry in performance re-versed, so that JV and AE were better at detectingthe apical delay, and AP was better at detecting thebasal delay: In other words, the level of performancewas determined by the reference stimulus rather than bythe signal. Note, however, that not all of the results canbe interpreted in terms of one stimulus sounding `spe-cial', as listeners AE, DD, and AP performed abovechance both when the reference contained a basal delayand the signal an apical delay, and vice versa. In addi-tion, the explanation cannot account for the data oflistener SV, who could not discriminate between basal

and apical delays of 0.1 ms but who was sensitive tolonger delays on the basal channel.

There are two broad classes of explanation for thehigh level of performance observed in experiment 1,and, in particular, for the ¢nding that four listenerswere particularly sensitive to a 0.1-ms delay on eitherthe apical (JV, AE, DD) or basal channel (AP). First, itmay be that some neuron(s) central to the auditorynerve receive inputs from ¢bers innervating di¡erentregions of the cochlea, and respond in a way whichdepends on the relative timing of those inputs. Forexample, it may be that the response is stronger whenthe inputs are nearly synchronous than when they areasynchronous, leading to the asynchronous signalssounding `softer' than the reference stimuli. In orderto explain the observed asymmetries in performance,this account would have to assume that the toleranceof such a mechanism to deviations from synchrony dif-fered for basal and apical delays, and also di¡eredacross listeners. In Section 7 we consider the ability ofa possible neural mechanism to respond di¡erentially tosmall basal and apical delays. A second class of explan-ation is that, despite the wide electrode separation, thestimulation on the two channels interacted within acommon population of AN ¢bers, presumably withCFs intermediate between the sites of the two `target'channels. Following the distinction made by Shannon(1983b), this explanation can be sub-divided into twoseparate forms of interaction. The ¢rst occurs with si-multaneous stimulation and results from a direct sum-mation of the charge applied to the two electrode chan-nels. Although the pulses in the two channels of ourstimuli did not overlap when measured using the testimplant, which had only a resistive load between thetwo electrodes in each channel, this may not havebeen true for a device implanted in a cochlea. Speci¢-cally, the capacitive properties of the nerve membranemay have introduced some temporal smoothing result-ing in partial charge summation between temporallyproximal pulses (cf. Cartee et al., 1997; see also Shep-herd and Javel, 1999). The second form of interactionoccurs even with non-simultaneous stimulation and re-sults from an electrical `spread of excitation', allowing aneural population to respond to a composite of thetemporal patterns applied to the two channels. Notethat both of these explanations, as with the more cen-tral explanation, would have to be modi¢ed to accountfor the asymmetries observed between basal and apicaldelays, and for the variation in the asymmetries acrosslisteners.

The next two experiments test for the `peripheral in-teraction' class of explanation. Experiment 2 tests thecharge summation hypothesis by reversing the polarityof the pulses applied to the basal channel. If the asym-metries observed are due to charge summation then this

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manipulation should dramatically alter the pattern ofresults, because currents which previously added wouldnow subtract (and vice versa (Shannon, 1985)). Experi-ment 3 controls for both forms of interaction by pre-senting a train of masking pulses to channels intermedi-ate to the two targets.

3. Experiment 2: Pulse polarity

3.1. Rationale and method

Experiment 2 measured the e¡ect of pulse polarity onthe discrimination between a stimulus with a 0.1-msdelay on the basal channel and one with an identicaldelay on the apical channel. Listeners JV, AE, and APwere selected to take part, because they had all per-formed this discrimination with a high degree of accu-racy in experiment 1. As in experiment 1, no feedbackwas given. The experiment consisted of three condi-tions. Listeners performed 20 runs of each conditionin turn until they had completed 100 trials for each one.

Fig. 3a shows the relative timing between adjacentpulses in the `non-inverted' condition, in which thepulse polarity was the same as experiment 1, for basal(left column) and apical delays of 0.1 ms. One concern,referred to above, is that temporal smoothing intro-duced by the nerve membrane would cause these pulsesto overlap. For example, if the pulses excited the sameneuron then the charge on the second phase of the ¢rstpulse in each pair might subtract from that in the ¢rstphase of the second pulse, resulting in a decrease inexcitation. Fig. 3b shows the `basal channel inverted'condition in which, due to the polarity inversion onthe basal channel, the charges would sum and the op-posite e¡ect would be expected.

The reasoning behind the third condition, in whichboth channels were inverted, will be described onlybrie£y because the results were inconclusive. It arosefrom the observation that, in the non-inverted condi-tion (Fig. 3a), the stimulus with a 0.1-ms delay on thebasal channel (left-hand column) is not a time-reversedversion of that with an identical delay on the apicalchannel (right-hand column). This is illustrated by thearrows in Fig. 3a; for each stimulus, one arrow indi-cates the half-pulse in which the more apical electrodein the apical channel is the cathode, and the other in-dicates the half-pulse where the more apical electrode ofthe basal channel is the anode. It can be seen that, inthis non-inverted condition, the interval between thesetwo half-pulses is longer in the stimulus where the basalchannel is delayed (left-hand column) than when theapical channel is delayed (right-hand column). If thesize of this interval were important then the patternof results would be reversed in the `both-inverted' con-

dition shown in Fig. 3c, where the interval between thetwo half-pulses is longer when the apical channel isdelayed. Analogous arguments would apply if timingbetween di¡erent pairs of half-pulses were important(i.e. those where the more basal electrode in the apicalchannel is the cathode, and where the more basal elec-trode in the basal channel is the anode).

3.2. Results

A comparison of the striped and open bars in Fig. 5shows that performance in the non-inverted and basallyinverted conditions was very similar, thereby providingevidence against any e¡ects of current summation. Thesolid bars show that, for listeners AP and JV, perform-ance was also similar in the both-inverted condition.The results of listener AE do show an e¡ect of pulsepolarity, being worse in the both-inverted than in theother two conditions (P6 0.01 in each case). Even here,however, no reversal in the asymmetry (which wouldhave resulted in a score below 50%) was observed.Once again, the measures for each listener and condi-tion were highly reliable, with a split-half reliability co-e¤cient of 0.947.

The absence of an e¡ect of reversing the polarity onthe basal channel has one further implication, arisingfrom the fact that the polarity reversal is equivalent toadvancing one half of the biphasic pulse by 40 Ws anddelaying the other half by an equal amount. That is, ifthe AN response was dominated by one half of eachpulse, as is sometimes observed physiologically (van denHonert and Stypulkowski, 1987; Parkins, 1989), thenthe results presented here are not a¡ected by a 40 Wsshift in the latency of that response.

4. Experiment 3: Interspersed maskers

4.1. Rationale and method

Even though experiment 2 ruled out explanations in

Fig. 5. Percentage of trials in which the signal (basally delayed stim-ulus for JV and AE, apically delayed for AP) was identi¢ed as suchin the three conditions of experiment 2. The key indicates whichchannels were inverted.

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terms of current summation, it is possible that the stim-ulation of the two target channels excited a commonpopulation of AN ¢bers. To test this, experiment 3presented maskers to channels that were intermediateto the two target channels. In order to reduce confusione¡ects arising from listeners not knowing which chan-nel(s) to listen to, the maskers started 400 ms before the¢rst target stimulus and ended 400 ms after the end ofthe second in each two-interval forced-choice (2IFC)trial. This would have caused them to form a separateauditory stream from the targets (e.g. Dannenbring andBregman, 1978), whilst still exciting activity in neuralpopulations intermediate to the two target sites. A fur-ther quality di¡erence was provided by presenting themaskers at a rate of 1000 pps rather than the 100 ppsused for the signals.

In experiment 3a, the masker was applied to a singlechannel with a position intermediate to the two targetsas measured along the length of the electrode array.This was channel 4 for all listeners except AE, forwhom channel 6 was used. Prior to the main experi-ment, a 400-ms portion of the masker was loudness-balanced twice to each of the two target channels ^once starting with a current level which was judged tobe quieter than the target and once starting with a leveljudged to be louder. The masker level was then set tothe mean of the loudness matches to the two targets. Inthe main part of experiment 3a the timing of the maskerrelative to the target stimuli was not randomized butwas such that listeners could not reliably use intervalsbetween masker and target pulses to perform the task.2

Four listeners were tested at basal and apical delays of1 ms. The remaining listener, AE, was tested with sig-nals which were delayed on the basal channel by 1.0 ms.No feedback was provided.

In experiment 3b we controlled for the possiblespread of excitation in the other direction around thecochlea by applying a dual masker using the maskerchannel of experiment 3a plus a channel basal to the

basalmost target. This was channel 8 for all listenerstested. The level of the additional masker was loud-ness-balanced to the targets in the same way as in ex-periment 3a, with the level of each masker being set tothe mean of the loudness matches to each of the twotargets. If the targets had been correctly set to equalloudness in the prelude to experiment 1, then themasker should have been adjusted to the same currentlevel (within experimental error) when matching to bothtargets. This was indeed the case: the mean ratio be-tween the higher and lower current levels was only 0.38dB, with a range of 0.05 to 1.27 dB across listeners andelectrodes (Table 1b). In this part of the experiment themore basal masker was always advanced by 0.1 ms rethe apical masker, but the timing between the maskerand target pulses was randomized from presentation topresentation.

The two electrodes used for each masker channel areconnected by dashed lines in the X-ray tracings of Fig.1a. Listener AE could not participate in experiment 3b(with a dual masker) because our use of the basalmostchannel as one of the targets meant that we could notselect a more basal masker. The alternative method ^ ofusing a masker more apical than the apical target(channel 4) ^ was precluded by the facts that channel3 overlapped physically with channel 4 (see Fig. 1b,array type 5.7), that channel 2 could not be stimulatedat a level high enough for its loudness to match that ofthe targets, and that channel 1 was not functioning atall. The other four listeners were tested with signal de-lays on the target channel that had given the best per-formance in experiment 1: this was the basal channelfor JV, DD, and SV, and the apical channel for AP.The signal delay used was selected separately for eachlistener to correspond to one which had led to a highlevel of performance in experiment 1. This was 2 ms forSV and 1 ms for the other three listeners.

Unlike the case in experiments 1, 2, and 3a, each trialin experiment 3b was followed by correct answer feed-back. This made what we expected to be a taxing task(attending to two channels whilst ignoring two others)more acceptable to the listeners, but meant that a com-parison of experiments 1 and 3b would have con-founded the e¡ects of the masker and of feedback.Therefore experiment 3b alternated blocks of 25 trialsin which the dual-channel masker was present with sim-ilar blocks in which it was absent; feedback was pro-vided in both cases. In both parts of experiment 3 allmeasurements were based on a total of 100 trials forlisteners JV, DD, AP and SV, and on 50 trials forlistener AE.

4.2. Results

Fig. 6a shows the results for a signal delay of 1 ms in

2 The shortest time between a masker pulse and a subsequent targetpulse on the non-delayed channel was always 0.3 ms in the ¢rst inter-val of each trial and 0.4 ms in the second, regardless of whether thestimulus was a reference or a signal. Hence only the interval betweenthe masker pulses and those on the delayed channel could possiblyprovide a cue. In most conditions of experiment 3a the delay betweenthe two target channels in the signal interval was 1.0 ms, and, as thiswas equal to the masker period, the time between adjacent maskerand target pulses was the same as in the reference stimulus. For theone condition where a 0.1-ms delay was tested (subject AE) themasker-target delay would have been 0.4 ms for a signal in the ¢rstinterval, the same as that which would occur in the reference intervalof that trial. When the signal occurred in the second interval, themasker-target delay would have been 0.5 ms and the subject couldhave used this cue. However, even if the cue had proved infallible onthis 50% of trials, AE would have had to guess on the other 50%,leading to a maximum possible score of 75%. The results show thatshe performed better than this.

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experiment 3a, in which a single masker was presented(solid bars), together with the data from the corre-sponding condition of experiment 1 (hashed bars). Itcan be seen that the masker did not have a substantiale¡ect on either the overall level of performance or theasymmetry between conditions with basally and api-cally delayed signals. The results obtained with thedual maskers of experiment 3b are shown by the ¢lledbars of Fig. 6b, with the data obtained for those samedelays in the absence of a masker shown by the openbars. Again, it can be seen that the maskers had only amodest e¡ect overall. In addition, a comparison of thenew measures obtained with no masker and those orig-inally measured in experiment 1 (hashed bars) showsthat the introduction of feedback had only a minore¡ect on performance.

The split-half reliability coe¤cients for the data inFigs. 6a and b were 0.974 and 0.808 respectively. Thecoe¤cient for Fig. 6b was lower than that in the other

experiments, but the di¡erence between the means ofthe ¢rst and second half of all responses was small(45.083 vs. 44.583) and not signi¢cant (paired samplest-test, df = 11, t = 0.458, P = 0.656).

The results of experiment 3 make it unlikely that, inexperiment 1, listeners were detecting across-channeltiming di¡erences by attending to auditory nerve ¢berswith CFs between those of the BM regions occupied bythe target electrodes. This conclusion rests, however, onthe assumption that the masker channels excited AN¢bers with CFs between those excited by the targets.This assumption was tested in experiment 4.

5. Experiment 4: Pitch judgements

5.1. Method

In experiment 4 listeners compared the pitch of two

Fig. 6. (a) Data from experiment 3 in the absence (hashed bars) or presence (¢lled bars) of a masker on a single channel. (b) Open and ¢lledbars show performance obtained in the absence and presence of a dual masker in experiment 3b, in which feedback was provided. The signalwas delayed by 1 ms on the basal channel for listeners JV and DD, by 1 ms on the apical channel for AP, and by 2 ms on the basal channelfor SV. The hashed bars show data from the corresponding conditions of experiment 1 in which there was no masker and no feedback. Notethat although the ordinate is labelled `% correct' in both parts of the ¢gure, any deviation from chance performance (50%) indicates that listen-ers could discriminate between the standard and signal.

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400-ms pulse trains presented sequentially to two di¡er-ent channels. The two channels were selected from themasker and target channels used in experiment 3, andall possible combinations were tested. The two channelswere presented in random order, separated by a 500-mspause. The listener was asked to identify the intervalcontaining the higher pitch. No feedback was given.The results are based on 40 judgements per pair forlisteners AP, DD, and JV, on 20 judgements per pairfor SV, and on 50 judgements per pair for AE.

Because pulse rate a¡ects pitch (e.g. Eddington et al.,1978; Shannon, 1983a; Pijl and Schwarz, 1995) we pre-sented all stimuli at the same rate. We chose the rate of1000 pps that was used for the masker channels in ex-periment 3. The alternative approach, of using a rate of100 pps for all channels, was not adopted because itwas not always possible to generate a su¤ciently loudpercept on both masker channels at that rate. As thepulses on the target channels had been presented at arate of 100 pps in previous experiments, the levels onthose channels at a rate of 1000 pps had to be re-bal-anced against the stimuli on the masker channels. Todo this, each target channel was adjusted twice to eachmasker channel : once starting from a quieter level andonce from a louder level.

5.2. Results

Table 3 shows the percentage of trials on which themore basal channel in each comparison was judged tohave the higher pitch, with the data for each listenerbeing shown in a separate matrix. It can be seen thatthis value exceeded 50% for all listeners and all compar-isons, with only one exception (listener DD comparingchannels 6 and 8). In all but four of the 27 comparisonslisteners scored at least 85%, indicating that the electro-des were not only arranged tonotopically but wereeasily discriminable. Note also that two out of thefour exceptions occurred for listener DD, who, overall,performed worse than the other four listeners at thispitch discrimination task. If this re£ected greater chan-nel interaction, and if such interaction were responsiblefor the ability of some listeners in experiment 1 to de-tect 0.1-ms timing di¡erences between channels, thenone might expect DD to have performed well at thattask. Inspection of Fig. 4 shows that, in contrast, hewas relatively poor at discriminating between 0.1-msbasal and apical delays.

One possible limitation in generalizing from the re-sults of experiment 4 to those of experiment 3 comesfrom the di¡erence in pulse rate (1000 vs. 100 pps)applied to the `masker' channels in the two experiments.It is possible that the spatial pattern of activation eli-cited by the masker channels di¡ered between the twoexperiments, either as a result of the rate di¡erence per

se, or of the change in current resulting from the loud-ness-balancing procedure (this di¡erence had a meanvalue of 2.5 dB, with a range of 0.9 to 5.4 dB acrosslisteners and electrodes). However, it seems unlikelythat such di¡erences would have reversed the e¡ectiveordering of channels along the neural array, particu-larly given evidence that for loudness-balanced stimulithe perceptual dimensions corresponding to rate andplace are orthogonal (Tong et al., 1983).

6. Experiment 5: Discriminating between 2-ms basal andapical delays

6.1. Rationale and method

In Section 1 we suggested that the detection ofacross-channel timing di¡erences might require a refer-ence stimulus in which the pulses on the two channelswere either synchronous or very nearly so. However,the results of listener SV in experiment 1 suggest thatthis may not always be the case. As with the otherlisteners he showed an asymmetry, being better at dis-criminating basally delayed than apically delayed sig-nals from the reference stimuli. Unlike that of the otherlisteners, however, his asymmetry could not be attrib-uted to the di¡erent reference stimuli used in the two

Table 3Results of experiment 4

JV 4 7 8

2 98 98 1004 100 937 53

AE 6 8

4 100 1006 98

DD 4 6 8

3 60 100 904 95 886 40

AP 4 7 8

2 85 98 1004 95 1007 65

SV 4 6 8

2 95 100 1004 85 1006 100

Each part of the table shows a matrix indicating the percentage oftrials in which one listener identi¢ed the more basal channel as hav-ing the higher pitch, for various pairs of channels. Channels, whichwere used as targets in experiments 1^3, are shown in bold type inthe column and row labels; those used as maskers in experiment 3are shown in italics.

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conditions, as these were indiscriminable (evidenced byhis chance performance at the two 0.1-ms delays). Thisled us to expect that he would be able to discriminatebetween a basal delay of 2.0 ms (which he had reliablylabelled as a `signal' in experiment 1) and an identicalapical delay (which he had not). Experiment 5 meas-ured the discrimination between 2.0-ms apical and basaldelays for all listeners, both in the presence and absenceof a masker on one (listener AE) or two (JV, DD, AP,SV) channels. These maskers were the same as in ex-periment 3, with the minor exception that the startingphase of listener AE's single-channel masker wasrandomized from presentation to presentation. Blocksof 25 trials with and without a masker were alternateduntil 100 trials of each had been collected for everylistener. Feedback was given, with the `correct answer'stimulus being de¢ned as that signal which had beenconsistently labelled as such in experiment 1 (basal de-lay for all except AP).

6.2. Results

Fig. 7 shows that in the absence of a masker listenersAE and, as predicted, SV could perform the task reli-ably. Hence for these two listeners the detection ofacross-channel timing di¡erences was possible evenwhen the stimulation to the two channels always con-tained an asynchrony as large as 2 ms. However, thiswas not the case for the other three listeners. On aver-age, the maskers had at most a small e¡ect.

Experiment 5 is similar to one condition in the studyby McKay and McDermott (1996), in that the signaland reference di¡ered only in the order of stimulationon the two channels. They presented amplitude-modu-lated pulse trains to each of two channels, with eachtrain consisting of one large and four small pulses re-peated with a period of 10 ms. The `channel reversal'comparison occurred when the delay between the large

pulses on the two channels was 9 ms in the signal in-terval and 1 ms in the reference interval. One of theirlisteners could perform this task at a channel separationof 3.75 mm when the current applied to the two chan-nels was constant throughout a block of trials, butperformance dropped to chance when the currentwas randomized from presentation to presentation. Aswas the case with three of our ¢ve listeners, the otherfour of McKay and McDermott's participants couldnot do the task even in the absence of current random-ization.

7. Discussion

7.1. Comparison with previous measures ofacross-channel timing sensitivity

All ¢ve listeners in the present study could reliablydetect di¡erences between the timing of pulses appliedto widely separated channels of their cochlear implants.This di¡ers from the results of previous studies (Tongand Clark, 1986; McKay and McDermott, 1996),where, except at small (6 3 mm) channel separations,listeners performed at chance. One possible explanationfor the discrepancy, described in Section 1, is that thepresent study was the only one to include inter-channeldelays of less than 1 ms. Consistent with this explana-tion, the good performance of four listeners was largelydue to one stimulus, having an inter-channel delay of0.1 ms, sounding di¡erent from all other stimuli used inthe experiment. Additionally, three out of ¢ve listenerscould not discriminate between two stimuli with equaland opposite delays of 2.0 ms on the two target chan-nels. However, this does not explain the whole patternof results, as two listeners (SV and AE) could performsuch a comparison, and three could detect di¡erencesbetween pairs of stimuli that did not include the onethat sounded `special'.

Four further di¡erences between our study and thoseof Tong and Clark (1986) and of McKay and McDer-mott (1996) come from the method of stimulation. Themost obvious of these is that our listeners were im-planted with the LAURA device, whereas those partic-ipating in the earlier studies were users of the Nucleus-22 implant. If our results were due to interactions at thelevel of the auditory nerve, then this might be attributedto poorer spatial selectivity in the LAURA device. Dif-ferences between the devices are hard to evaluate, be-cause extensive psychophysical measurements of theLAURA implant's spatial selectivity have not beenmade, and, even if they had, the large inter-listenerdi¡erences commonly observed within the same device(e.g. Shannon, 1983b; Chatterjee and Shannon, 1998)would hinder a comparison. However, the ine¡ective-

Fig. 7. Percentage of trials on which listeners correctly identi¢ed thestimulus with a 2.0-ms apical (listener AP) or basal (other listeners)delay as being the signal in experiment 5. Solid bars indicate thecondition with a masker present; hashed bars are for the conditionwith no masker. Note that, although the ordinate is labelled `% cor-rect', any deviation from chance performance (50%) indicates thatlisteners could discriminate between the standard and signal.

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ness of interspersed maskers in experiment 3, combinedwith the ¢nding in experiment 4 that the channels werearranged tonotopically, argues against an explanationof our results in terms of poor spatial selectivity. Fur-ther arguments against this explanation come from thehigh discriminability of the two targets in experiment 4,and the fact that the listener showing the worst discrim-ination between channels in that experiment did notperform well at the across-frequency comparisons inexperiment 1.

The second di¡erence in stimulation is that we used apulse duration of 40 Ws/phase, compared to the 100 Wsused by Tong and Clark (1986) and for most of McKayand McDermott's (1996) listeners. There is psychophys-ical evidence that pulse duration a¡ects the slope of thetemporal integration function (P¢ngst et al., 1991), a¢nding which may re£ect an e¡ect on the temporalpattern of neural activity evoked. It is conceivablethat this, in turn, might a¡ect the ability of listenersto compare ¢ring patterns between di¡erent popula-tions of AN ¢bers. However, the slope of the integra-tion function is constant for durations between 50 and500 Ws/phase (P¢ngst et al., 1991), and so it is unlikelythat such di¡erences could account for the discrepancybetween our results and those obtained previously witha pulse duration of 100 Ws/phase. Alternatively, onecould argue that the shorter pulse durations used herenecessitated higher current levels, and that this resultedin a reduction of spatial selectivity. This seems unlikely,given not only the arguments against a `spatial selectiv-ity' interpretation described above, but also McKayand McDermott's (1999) recent experiments on the ef-fect of pulse duration on the detection of across-chan-nel timing di¡erences. They reported that the spatialseparation beyond which performance deterioratedwas smaller at a pulse duration of 50 or 100 Ws thanat 266 Ws, suggesting that spatial selectivity is best atshort pulse durations. This conclusion held even thoughthe pulses of di¡erent durations were matched for loud-ness, so that the current level increased with decreasingpulse duration.

A third di¡erence arises from the fact that, unlike theabrupt gating used in the other two studies, our stimuliwere turned on and o¡ with 50-ms ramps. We can thinkof no reason why this would have resulted in a markedimprovement in performance. A fourth, perhaps moreplausible, reason for the di¡erence between our resultsand those of McKay and McDermott (1996) is thatthey randomized the current applied to the two chan-nels from presentation to presentation whereas we didnot. Our decision not to randomize the current levelwas based on two considerations. First, if the two chan-nels did excite a common population of AN ¢bers, thenwe would expect their relative timing to a¡ect primarilya percept of `roughness' or pitch (Tong and Clark,

1986), rather than in£uencing loudness.3 We thereforechose to control for such cues using interspersedmaskers rather than by roving the level. Second, asMcKay and McDermott (1996) have pointed out, onemight expect a randomization of current level to de-grade performance even if the cue being used werenot loudness. As it turned out, the label (`zachter')used by some of our subjects to describe the signalssuggests that they may have sounded quieter than thereference stimuli, and so loudness randomization couldwell have caused a substantial degradation in perform-ance. However, we should stress that, although listen-ers' perceptual descriptions are informative, the crucialissue is whether the di¡erent percepts used to performthe task arose from interaction at the level of the AN,or whether they re£ect the operation of more centralprocesses. The results of our control experiments pointto the latter interpretation.

7.2. Comparison with sensitivity to timing di¡erencesbetween ears

The results presented here show that the timing ofelectric pulses is well-preserved in the auditory periph-ery, and we have argued that mechanisms central to theAN can process timing di¡erences between channels. Ifthis is so, then, given the extremely ¢ne sensitivity ofbinaural mechanisms to timing di¡erences betweenacoustic stimuli presented to opposite ears, we mightexpect a similar acuity to electric interaural timing dif-ferences (ITDs). Early evidence against this predictioncomes from a study by van Hoesel and Clark (1997),who showed that even when the electrodes in the twoears stimulated similar regions of the cochlea, thethreshold ITD was 0.5 ms for one of their two listenersand 2.0 ms for the other. However, more recently, Law-son et al. (1999) have reported much better sensitivityfor two of the three listeners tested. One could detectITDs of 50 Ws between two pitch-matched electrodes inopposite ears, with thresholds of about 200 Ws for twoother pairs of pitch-matched electrodes. The secondcould detect di¡erences of about 200 Ws on all threepitch-matched pairs tested, whereas the third listenershowed very poor sensitivity and a rather erratic pat-tern of results. The thresholds for the ¢rst two listeners,although greater than the 10 Ws observed for analogousacoustic stimuli in normal listeners (Hafter and Dye,1983), reveals a sensitivity of the same order as reportedhere. Unfortunately, the very small number of patientsimplanted binaurally, combined with the large inter-lis-

3 An exception to this would occur if the charges applied to the twochannels summed, as a result of direct electrical interaction; this pos-sibility was ruled out by the lack of an e¡ect of polarity reversal inexperiment 2.

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tener di¡erences commonly observed in implant psy-chophysics, makes it impossible to decide on a `typical'result for the detection of electric ITDs. However, it isperhaps worth noting that, acoustically, thresholds fordetecting a di¡erence in ITD between two sounds islowest when one of the sounds is diotic, and increaseswhen both stimuli have non-zero ITDs (Yost, 1974).This means that if the latency of the AN response toelectrical stimulation di¡ers between the two ears, thenthe threshold ITD will be an overestimate of the mini-mum interaural asynchrony that the listener is capableof detecting. One possible source of such a latency dif-ference would occur if the integrity of AN dendritesdi¡ered between the two ears, leading to di¡erences inthe site of activation and hence in latency (for a dis-cussion, see Shepherd and Javel, 1997). Another possi-ble source of latency di¡erence may arise from smalldi¡erences in the level of current applied to the twoears, as discussed below. In either case, variations inthe size of these latency di¡erences across listenersmight account for some of the variability in ITD sensi-tivity that has been reported in the literature.

7.3. Possible mechanisms

Although the present results show that listeners aresensitive to across-channel timing di¡erences, they donot demonstrate a pattern of gradually increasing sen-sitivity with increases in temporal asynchrony. Thismakes it particularly important to rule out artefactsbased on current summation or channel interaction.Our control experiments show that the existence anduse of such artefactual cues would have to survive po-larity reversals and the presence of interspersedmaskers, and would have to depend on which of twochannels was delayed in a manner which di¡ers acrosslisteners. It is therefore worth considering how the op-eration of a neural mechanism or mechanisms at a sitecentral to the AN could account for our results. Anysuch mechanism(s) would have to sum inputs from AN¢bers having widely di¡ering CFs, and to do so in away which was sensitive to timing di¡erences betweenthe AN spikes of di¡erent channels.

The search for a physiological substrate for our ¢nd-ings is hampered by the fact that no in vivo measure-ments have been made of the sensitivity of cochlearnucleus or more central neurons to the temporal syn-chrony between electric pulses applied to discrete pop-ulations of AN ¢bers. There is, however, evidence fromin vitro recordings that octopus cells in the postero-ventral cochlear nucleus, which receive inputs fromAN ¢bers having a wide range of CFs (Godfrey etal., 1975), are exquisitely sensitive to such timing di¡er-ences. Golding et al. (1995) measured the excitatorypost-synaptic potentials (EPSPs) of mouse octopus cells

in response to 100-Ws electric pulses applied to the AN.They found that EPSP amplitude increased monotoni-cally with increases in the stimulating voltage, a ¢ndingthey attributed to the octopus cells summing inputsacross AN ¢bers, and to more AN ¢bers being stimu-lated at higher voltages. More importantly, the stand-ard deviation of the EPSP latency was only 20 Ws, andGolding et al. concluded that octopus cells detectedcoincident ¢ring of AN ¢bers with high temporal pre-cision. One way in which this type of mechanism couldbe consistent with the asymmetries present in our datawould be if the delay between electrical stimulation ofthe cochlea and the post-synaptic e¡ects of the resultingAN activity in the cochlear nucleus di¡ered across elec-trode channels. Given that in deafened squirrel mon-keys AN spike latency can di¡er by 350 Ws over a 2-dB level range (Parkins, 1989), it would only take asmall di¡erence in `e¡ective current level'4 between thetwo target channels to produce asymmetries of the typeseen here. An additional potential source of di¡erencesbetween channel latencies is suggested by Liberman andOliver's (1984) ¢nding that the length of AN ¢bers,measured from the organ of Corti to the border ofthe CN, varies non-monotonically with CF.

It would clearly be premature to conclude that octo-pus cells, or indeed any other speci¢c neural mecha-nism, provide the neural basis for the results observedhere. In the absence of comprehensive in vivo measure-ments obtained with electrical stimulation, it is notknown whether such cells are capable of respondingdi¡erently to apical and basal delays of 0.1 ms, orwhether they can re£ect temporal synchrony on twochannels when maskers such as those used here arepresent. However, the results of Golding et al. doshow that it is possible for more central neurons toexhibit a sensitivity to temporal synchrony betweenAN ¢bers that is at least as acute as that suggestedby our results. It is also worth noting that the temporalprecision revealed by both studies is much ¢ner thanwould normally be needed to detect temporal syn-chrony between two acoustic stimuli occupying di¡erentfrequency regions, as such synchrony would be compro-

4 The term `e¡ective current level' is used because the response of theAN will presumably be determined not only by the current as meas-ured with the test implant, but also by factors such as the distancebetween the electrode and the nerve endings. Note that equating twochannels for loudness may not always equate the two `e¡ective levels',as loudness will presumably be in£uenced by the number of neuronsactivated, which will in turn be a¡ected by the number of survivingneurons in the vicinity of that channel. Note also that Parkins' ¢ndingdi¡ers from that of van den Honert and Stypulkowski (1987), whoreported that in cats the latency to electrical stimulation did not varymonotonically with current level. Possible reasons for the di¡erencesbetween the two studies include the species tested and the pharmaco-logical (Parkins) vs. mechanical (van den Honert and Stypulkowski)deafening of the animals.

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mised by di¡erences in basilar membrane ringing and intravelling-wave delays. Hence electrical stimulation canreveal, both in neural and in behavioral responses, asensitivity to timing di¡erences which are smaller thanthose which would occur naturally. Although this lackof an ecological basis makes it unlikely that a neuralmechanism evolved speci¢cally to process the 0.1-msasynchronies which our listeners can detect, it appearsthat mechanisms central to the AN can neverthelessrespond di¡erentially to those asynchronies.

Acknowledgements

We thank Drs. Philip Joris and Ian Winter for help-ful comments on a draft version of this article, Dr. P.Govaerts for supplying the X-ray information, Dr. As-trid van Wieringen for running part of the experiments,and our subjects for their tireless participation. The im-plant operations were performed at the St. Augustinushospital, Antwerp, by Prof. Dr. E. O¡eciers, whom wealso thank.

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