evoked-responses of human auditory-cortex may be enhanced by preceding stimuli

Electroencephalography and clinical Neurophysiology, 1989, 74:217-227 Elsevier Scientific Publishers Ireland, Ltd.

217

EEG 02299

Evoked responses of human auditory cortex may be enhanced by preceding stimuli

N. Loveless 1, R. Hari, M. HiLrn iEiinen and J. T'tihonen Low Temperature Laboratory, Helsinki University of Technology, $F-02150 Espoo (Finland)

(Accepted for publication: 22 October 1988)

Summary We report enhancement of the 100 msec deflection Nl00m of the auditory evoked magnetic field in paired.stimulus paradigms. Noise bursts of $0 msee duration were delivered in pairs to the left ear at interpair intervals of 1.2-1.4 sec. Stimulus onset asynchrony (SOA) within the pair was either 70, 150, 230, 300, 370 or $00 msec, all intervals being presented randomly within the same block. Magnetic responses were recorded over the righ: ~temlsphere with a 7-channel tint-order SQUID gradiometer. The mean amplitude of N100m to the second stimulus was maximal at an SOA of about 150 msec, decreasing at longer SOAs to an amplitude about equal to that of the Nl00m evoked by the first stimulus. Similar enhancement effects were elicited by noise bursts, square-wave tones and sinusoidal tones, by pauses in a continuous noise, and when the two stimuli of a pair were led to different ears.

Key words: Evoked magnetic fields; Evoked potentials; Auditory cortex; Recovery cycle; Enhancement; Man

The N100 deflection of the auditory evoked potential is very sensitive to the rate at which stimuli are presented. If short trains of identical stimuli are delivered at inter-stimulus intervals (ISis) of a few seconds with long intervals between trains, the first stimulus of a train evokes an N100 response of very large amplitude which then decreases rapidly over the next few stimuli to an asymptotic level which depends on the ISI. If the train consists of only one pair of stimuli, the response to the second stimulus increases in amplitude with increasing ISI, reaching the amplitude of the first response at ISis of about 10 sec, provided that the inter-pair interval (IPl) is rela- tively long. The function obtained by this paradigm has been described as 'temporal recovery,'

t Permanent address: Department of Psychology, University of Dundee, Dundee DD1 4HN, Scotland, U.K.

Correspondence to: Dr. R. Hari, Low Temperature Labora- tory, Helsinki University of Technology, SF-02150 Espoo (Fin- land).

implying that response decrement can be attributed to a temporary loss of excitability in the neural system generating the evoked potential. Rate effects are to some extent specific to stimulus characteristics, being greatest when successive stimuli are identical, and becoming smaller with decreasing similarity. The N100 deflection is now known to be a complex phenomenon, resulting from a number of overlapping components (NH- t~tnen and Picton 1987). It is therefore difficult to determine how observed rate effects can be attributed to specific components. Neuromagnetic recordings, which provide good spatial resolution, might be helpful here.

N100m, the magnetic counterpart of the electric N100, appears to be generated by a tangential source in supratemporal auditory cortex and can, therefore, be separated from components whose generators are radially oriented and do not contribute significantly to magnetic fields recorded outside the head. Hari et al. (1982, 1987) found that the amplitude of N100m to short tones and to onsets and offsets of noise bursts is near its asymptote at an ISl of 8-10 sec, but decreases

0168-5597/89/$03.50 © 1989 Elsevier Scientific Publishers Ireland, Ltd.

218

sharply as ISI is reduced towards 1 sec. N100m was evoked by a variety of auditory stimuli, in- cluding speech sounds. Kaukoranta et al. (1987), reco:ding responses to fricative-consonant/vowel transitions in simple words, found that N100m responses were elicited by the onset of the vowel as well as by that of the consonant. A similar s~uence of 2 N100m responses was elicited by a ~ ise burst followed by a square-wave tone, sug- gesting that the responses were evoked by general acoustic features rather than by features which were specifically phonetic.

Mltkellt et al. (1988) found that the 2 N100m responses elicited by noise/square-wave sequences differed in their reactions to a number of parame- ters: in particular, the response to the square-wave was less affected by the interval separating successive noise/square-wave sequences than the response to the noise. The authors noted that the structure of the sequence resembled a forward- masking paradigm, but were unable to decide whether the difference in rate effects was caused by a masking effect of the noise or whether it was due to the paired presentation of the stimuli. The latter possibility is supported by an experiment in which tone-noise and noise-tone pairs were presented at a stimulus onset asynchrony (SOA) of 310 msec and at IPls of 1.2-1.3 sec and 7-8 sec. The effect of IPI was stronger on the fir,~t response of the pair, independent of the stimulus characteristics (Had 1989).

Similar problems of interpretation have arisen in other experiments using paired.stimulus paradigms. Mlikelli et al. (1987) compared intermittent frequency and amplitude modulations (FMs and AMs) of a continuous tone using pairs separated by 500 msec and found that the second response was lar~.er for ~,n-identical than for identical pairs, l~kelli (1988) presented pairs of 50 msec noise l~ursts with SOAs of 310 mscc every 2 see in all 4 possible combinations of contrstateral and ipsila~eral presentations. The amplitude ratios of the f:~t and second ~'.T]00m were larger for pairs with similar ~:han wi~ different stimuli. Surpris- ingly, the largest responses to both contra- and ipsilater~i stimuli were obtained when the stimuli were the second members of the pairs and were preceded by a stimulus to the other ear. This was

N. LOVELESS ET AL.

taken to suggest that an additional mechanism, possibly sensitive to changes in location of sound in space, was triggered in this type of stimulus presentation.

It is, therefore, a general issue how far the responses evoked by a pair of sounds can be accounted for in terms of 'recovery cycles.' The general principles which appear to govern rate effects (Nii~tiinen and Picton 1987) suggest the following: The amplitude of the response to the first stimulus is an increasing function of IPl. The amplitude of the second response should also be an increasing function of IPl, but to an extent limited by the similarity of the 2 stimuli of the pair and the additional time occupied by the SOA. Except perhaps for the special case of identical pairs, it is difficult to predict the relative amplitudes of the 2 responses.

This analysis implies that the amplitude of the second response is an increasing function of SOA. In fact, the form of the temporal recovery function is not well established for intervals less than about 500 msec. When SOA is decreased beyond this point, successive responses begin to overlap and transient responses gradually change into steady-state responses w~ich are not linear sums of the transient responses. In the course of another investigation (Loveless and Hari unpublished) we noted that when pairs of sounds were presented at intervals of less than 500 msec, the N100m responses to the second sound appeared to be enhanced We therefore carried out several experiments on this phenomenon.

Materials and methods

Subjects and experimental conditions Nine members of laboratory personnel and paid

students served as subjects in the main experiment. Additional experiments were carried out on two of them; the methodological details of these experiments are given in Results. The measurements were made in the magnetically shielded room of the Helsinki University of Technology. During the recordings the subject lay on one side, and his head was fixed by a vacuum cast.

F A C I L I T A T I O N O F AEFs • 219

Stimuli Noise bursts of 78-80 dB (SPL rms) were pre-

sented to the left ear through a plastic tube and ear piece. The stimulus led to the electroacoustic" transformer had a flat spectrmn from 0 to 5 kHz, but when measured from the ear piece the spectrum of the stimulus was flat from 0.25 to 3 kHz with no significant power above 4 kHz. Bursts of 50 msec duration were presented in pairs with SOAs of 70, 150, 230, 300, 370, or 500 msec. All these intervals were presented in random order within the same block, with the restriction that no SOA could occur more than 3 times in succession. The IPI varied randomly from 1.2 to 1.4 sec. This procedure allowed responses to be recorded at exactly the same location and in the stone state of ,~igilance for all SOAs. The subject was instructed to read a book and to pay no attention to the stimuli.

Recording Magnetic field outside the head was measured

with a 7-channel first-order SQUID gradiometer whose pick-up coils are mounted in a hexagonal grid on a spherical surface with a radius of 125 mm (Knuutila et al. 1987). The pick-up coils have diameters of 20 mm and are separated by 36.5 ram. Their distance from the scalp is typically 18-20 mm. The sensitivity of the instrument is 5-6 iT/HfH~. All recordings were made over the right hemisphere at the posterior field extremum where the magnetic flux is directed into the skull during the main deflection, N100m, of the evoked response, resulting in a downward deflection in our figures.

Data analysis The recording passband was 0.05-100 Hz (3 dB

points; roll-off 35 dB/decade for the high.pass and 80 dB/decade for the low-pass filter) and the data were digitized at 500 Hz. The first 2 responses of each stimulus block were omitted from the analysis. Further, the vertical electro-oculo- gram (EOG) was recorded during all magnetic measurements and all traces coinciding with EOG deflections exceeding 150/tV were omitted from the analysis. The averaged EOG did not exceed 10

~V. At least 50 responses were averaged for.each SOA. Peak amplitudes and latencies were measured from the channel with the maximal signal. In all recordings standard errors of the means of the averaged responses were also calculated; these values were typically 30-35 fT and were used in testing whether effects seen in single subjects were statistically significant and whether field patterns obtained from the 7-channel measurements differed from each other at different latencies.

Results

Main experiment Fig. 1 shows the responses of I subject to pairs

of noise bursts at each of the 6 SOAs. The superimposed traces demonstrate the reproducibility of the responses. The most promi~ent feature of the r~sponse to the first stimulus is an N100m deflec- tk~n at a latency of about 100 msec, usually preceded by a smaller deflection, P40m, and followed by another deflection, P200m, both of opposite polarity to N100m. P200m appears to be pro- longed at the longer SOAs, when it is not ob- scured by the response to the second stimulus. This second response has generally the same form as the first. However, a part of its apparent amplitude variation is due to superimposition upon the P200m response to the previous stimulus. At the shortest SOA (70 msec) the overlap was so severe that in some subjects it was difficult to discern N100m at all.

In order to differentiate the response to the second stimulus of a pair we subtracted the responses at the longest SOA (500 msec) from those at shorter SOAs. Fig. 2 shows data from 3 subjects before and after the subtraction. The difference

• curves bring out clearly the N100m response at the shortest SOA and appear to provide a stable baseline. Amplitudes of P40m and N100m were measured from the mean value of this baseline over a period of 100 msec before the stimulus. Response wave forms are similar for all SOAs. Note that in subject 2 the second stimulus evoked at the shortest SOA a very large response, superimposed upon the first.

N. LOVELESS El" AL. 220

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FACILITATION OF AEFs 221

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pairs and are averages of Nl00m to all 6 pairs.

All 9 subjects showed enhancement of the second response at short SOAs. Fig. 3 shows the mean peak amplitudes and latencies of the P40m and N100m deflections for the first and for the second stimulus as a function of SOA. The amplitude of N100m to the second stimulus is signifi- candy larger (P < 0.02, binomial tes0 at SOAs of 70, 150 and 230 msec than at 500 msec, when it reaches the same level as N100m to the first stimulus; the largest mean increase of N100m amplitude is 80% as compared with the response

to the first stimulus. The latencies of P40m and N100m to the second stimulus are longer than those to the first by 10-15 msec and 15-20 msec, respectively; the differences are significant for N100m at SOAs of 300 and 370 msec ~nd for P40m at SOAs of 150 and 230 msec (P < 0.02, 2-tailed t test for group means). From the similar- ities of the latency variations of P40m and N100m we think it likely that the P40m response as measured is strongly influenced by the leading edge of the N100m deflection. This suggests that variations in SOA affect the generation of N100m to the second stimulus as early as 40-50 msec. The amplitude of N100m increases as SOA decreases, peaking on average at SOA of 150 msec. At the 70 msec SOA, the mean response is slightly smaller, but there are appreciable individual differences at this point. Subject 2, who showed the most prominent incremental responses, produced the maxi- mum response at a SOA of 70 msec and so did several others, but about half of our subjects had smaller responses at 70 msec than at 150 msec. Estimation of amplitude is quite difficult at this point.

Field maps were not constructed in this study. We have, however, good reasons to think that the observed enhancement of responses was due to changes in source strength, rather than in source location; First, in 7-channel measurement (cf., Fig. 1) distribution of the first and second responses did not differ significantly at the 95% confidence level (for testing of differences between 2 field patterns, see Kaukor~nta et al. 1986). Second, in another study (Loveless and Had unpublished) the duration of the first noise burst was varied between 100, 240 and 400 msec and the second stimulus (duration 50 msec) always started at 420 msec. Enhancement of the second stimulus was evident for the 240 msec noise bursts. The field map of this enhanced second response did not differ from that of the other two second responses.

It thus appears that as the interval between a pair of identical sounds decreases, the amplitude of N100m decreases down to intervals of about 500 msec, but then increases again below intervals of about 300 msec. In order to characterize this phenomenon further, we report 3 additional experiments.

222

Additional experiments Effect of dichotic presentation. Since enhance-

ment of evoked responses depends on the interval between 2 sensory inputs, it is of interest to determine the cerebral level at which these inputs interact. We tested 2 subjects under the original condition in which 2 ~cise bursts were presented monaurally to the contr~ateral ear, and 2 additional dichotic conditions in which the first stimulus was contralateral and the second ipsilateral and vice versa.

In the dichotic series, N100m to the first stimulus was larger (Fig. 4) and about 10 msec shorter in peak latency for the contralateral ear than for the ipsilateral. The contralateral first response was smaller in identical pairs than when mixed with ipsilateral responses; the ipsilateral first response was the smallest. In all stimulus combinations the second response was enhanced, both in comparison with the amplitude of the first response, and more clearly in comparison with the amplitude of the second response at SOA of 500 msec. These differences were highly significant (P < 0.005; 2-tailed t test for group means). The latency changes (increases of 15-20 msec during enhancement) were qualitatively similar for all conditions.

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pairs vice versa.

N. LOVELESS ET AL.

Effect of stimulus quality. We also observed that the enhancement effect applies to a wider range of stimuli and to pairs which are not physically identical. We tested 1 subject with pairs of 50 msec tones of the same (1 kHz) or different (1 kHz, 1.5 kHz) frequency. Both square-wave and sinusoidal tones were used. Significant enhancement effects were observed with both types of stimuli independently of whether the stimuli of the pair were physically identical or not: the amplitudes of N100m were 56-120% higher at the SOA of 150 msec than of 500 msec (P < 0.001 for 3 stimulus combinations and P < 0.05 for 1). The latency increase (30-40 msec) during enhancement was also very similar in all conditions.

Responses to offsets. All the above findings may be explained by neural processes triggered by stimulus onsets. We therefore compared, in 1 subject, responses to noise onsets with responses to offsets, i.e., to pause onsets in continuous noise. This was done both for wide-band (0-4 kHz, 94 dB SPL rms) noise as before and also for narrow- band noise of low frequency (0-250 Hz, 77 dB SPL rms).

For wide-band noise, offset responses are larger in amplitude than responses to onsets; for the lower-intensity narrow-band noise no such difference exists (Fig. 5). Offset responses show a very clear enhancement effect; at SOAs of 150-300 msec the amplitudes are significantly larger than at the SOA of 500 msec (P < 0.005). N100m to the first offset is larger and more stable than N100m to the onset. The latency is about 10 msec longer to the offset than to the onset. The latency of N100m to the second offset is clearly longer (up to 70 msec) at short SOAs; at longer SOAs the latencies are about the same as to the first stimulus. A prominent P200m is seen after the first offset of wide-band noise; *his finding contrasts with those of Hari et al. (1987) ~ith longer ISis.

Discussion

The present data indicate that auditory evoked magnetic responses, which reflect activity of the supratemporal auditory cortex, may be enhanced in paired stimulus paradigms. On average, the


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function of SOA in different conditions.

224

increment is maximal at SOA of about 150 msec and fades out after 300 msec. Enhancement of auditory evoked cortical responses, either electric or magnetic, has not to our knowledge been re- ported before. At the brain-stem level, however, enhancement of evoked responses at short intervals has been observed. Ananthanaryan and Gerken (1983) presented pairs of tones, a masker and a probe, of equal frequency and suprathresh- old intensity at an IPl of 500 msec. Wave V of the auditory evoked potential showed an amplitude increment which was maximal at intervals between masker offset and probe onset of 15 and 45 msec. This enhancement was interpreted as a central process concerned with the timing of sound sequences.

The results of our dichotic presentation suggest that the enhancement of cortical late responses is also due to a central process. N100m evoked by the first stimulus of a pair showed ear specificity, thereby agreeing with results from both electrical potential studies (Butler et al. 1969; Picton et al. 1985) and magnetic recordings (Mlikellt 1988). Thus the mechanism of response enhancement seems to be non-cochlear, located in proximal brain-stem or in central auditory pathways where the inputs from the 2 ears can interact. The similar functions for stimuli of both ears support the idea that the enhancement effect is non.specific in that it depends on the time since the last stimulus without regard to the ear of presentation.

Enhancement can apparently be triggered by a wide variety of stimuli, by offsets as well as onsets, and is not limited to repetitions of identical sounds. It thus appears to be a rather general effect upon the second of a pair of stimuli. We have accord- ingly to consider how such incremental effects are to be acco~mnodated with existing views of rate effects. It would be possible to revise the concept of 'excitability cycle' so that as the interval between stimuli decreases, excitability reaches a lower limit at about 500 msec and then shows an increase. However, it seems implausible to see this increment as part of the mechanism which is responsible for decrements, whatever that may be. One might rather be dealing with a 'dual-process' phenomenon, analogous to the dual-process theory of habituation (Thompson et al. 1979) which

N. LOVELESS ET AL.

states that repeated stimulation results in the development of 2 separate processes, habituation and sensitization.

Physiological considerations The physiological mechanisms underlying rate

effects are not well understood. The decrement of response amplitude as ISI decreases to about 500 msec is linked with increased specificity in that it depends on the similarity of the 2 stimuli; indeed recent evidence suggests that specificity at 460 msec is very sharp (Niiitiinen et al. 1988). Butler et al. (1969), who suggested that specificity could be explained by the activation of overlapping populations of neural units, attributed the response decrement to habituation. 'Refractoriness' was invoked (Ritter et al. 1968) because dis- habituation had not been demonstrated, but its nature is unclear: real postsynaptic refractory effects are improbable because axons can transmit action potentials at frequencies of hundreds of hertz and postsynaptic potentials are not followed by refractory periods at all. On the other hand, repeated stimulation can decrease presynaptic transmitter release in simple animal preparations (Thompson et al. 1979). Webster and Aitidn (19"/1) attempted to show that decrement was due to an inhibitory process in specific pathways.

In the auditory cortex of anesthetized cats, Hocherman and Gilat (1981) found cells whose unit activity was facilitated when ISI was decreased from 900 to 550 msec. These neurons consisted of less than 10~ of all cells, the majority of which showed response suppression. These data indicate that a decrease of ISI does not necessarily imply a decrease of excitability, as would be suggested by the refractoriness concept.

A disinhibition hypothesis for response facilitation has been suggested by Mitzdorf (1987) on the basis of current source density analysis in the visual cortex of anesthetized cats. When 2 identical abrupt visual stimuli were presented in close succession, the response to the second was larger and more coherent. This facilitation lasted for about 600 msec, being strongest when the stimuli were separated by 200-300 msec and being weak when general excitability was either high or very low. Facilitated responses had strikingly longer


(about 30 msec) onset latencies; this was attributed to delayed afferent input to the cortex. According to Mitzdorf, response facilitation is based on subtle interactions between distant cells or modules.

The polarity of N100m can be accounted for by the direction of intracellular currents associated with EPSPs in apical dendrites of the supratemporal cortex. The disinhibition hypothesis would attribute N100m enhancement either to an increase of the absolute amount of EPSPs or to loss of inhibitory currents. However, a parallel effect may be caused by increased simultaneous inhibitory activity in deep cortical layers: deep lPSPs and superficial EPSPs produce currents in the same direction (from superficial to deep layers in the intracellular space) and their resultant activity is responsible for the measured cerebral magnetic fields. Inhibitory influences are abundant in the cortex and, although often neglected, certainly have an important role in the generation of evoked responses. For example, excitatory afferent input is, in general, followed disynaptically by inhibition (Creutzfeldt 1977). Because inhibitory synapses are mainly concentrated near or at the somas of pyramidal cells, their contribution to external magnetic fields tends to parallel that of excitatory currents in apical dendrites. Present data do not allow us to differentiate this possibility from the disinhibition hypothesis.

In summary, rate effects on evoked responses might be explained in a way analogous to the dual-process theory of habituation (Thompson et al. 1979) by proposing 2 mechanisms: one affecting tl/e number of cellular elements c~ntributing to the response, and the other affecting their reac- tivity. According to this interpretation, several synchronously activated neuronal populations contribute to the responses at long ISis, so that the responses are large in amplitude. Stimulus repetition results in suppressic~n of some of these populations by active inhibition; the suppression continues up to ISis of about 0.5 sec. At still shorter ISis the response is mainly determined by activation of stimulus-specific neurons, the reac- tivity of which depends on the spontaneous activity and on acti,~ity triggered by preceding stimuli.

Psychoacoustic parallels A number of psychoacoustic phenomena show

some kind of enhancement over a period of a few hundred milliseconds. In some studies of forward masking, a masker of moderate intensity has been found to lower the threshold for a signal of similar spectrum (Zwislocki et al. 1959; Rubin 1960). This effect has been termed 'facilitation.' M~ore and Welsh (1970) examined the threshold for one click as a function of another, over a range of intervals up to 600 msec. A first sound of low intensity (3 dB SL) produced facilitation throughout 600 msec, peaking at about 80 and 160 msec. As the intensity of the first sound increased to 20-40 dB, it began to produce masking at the shorter intervals, changing to facilitation from 160 to 600 msec. Facilitation was found only for monaural presentation.

Enhancement has also been found at supra- threshold levels in studies of 'loudness enhancement.' When a pair of sounds is presented to one ear, the second sound appears to be about 5 dB louder than the first when they are actually of equal intensity. The enhancement of the second sound increases still further as its intensity becomes less than that of the first. The enhancement decays over a period of 50-150 msec (Irwin and Zwislocki 1971; Zwislocki and Sokolich 1974; Zwislocki et al. 1974). Loudness enhancement also occurs when the second sound is presented to the ear contralateral to the first, although Elmasian and Galambos (1975) found that monaural presentation produces more enhancement and less variability than dichotic presentation. They observed that 'loudness enhancement' differs from 'facilitation' in being maximal immediately after the first stimulus and increasing with its intensity.

Our findings resemble the loudness enhancement studies in that they can be produced dichoti- cally. Moreover, informal observations support the view that sounds presented at these short intervals tend to form perceptual groups with subjective accentuation (cf., Plomp 1964), though when the pairs are not identical, grouping may be affected by the presence of the same sound in the previous pair.

It is difficult to find a psychoacoustic parallel

226

for the effectiveness of offsets, but there is good evidence of their importance in the perception of temporal patterns. The subjective grouping of repetitive sequences of two elements may be power- fully altered by the introduction of pauses (Royer and Garner 1966, 1970; Handel 1973).

Thus, the time course of evoked response enhancement seems to parallel some psychoacoustic findings. It is not clear whether this parallelism indicates any functional connection between evoked responses and psychoacoustical perfor- mance. Evoked response amplitudes and sensa- tions are known to be dissociated in some cir- cumstances (cf., Nltlttlinen and Picton 1987; Hari and Mltkelli 1988).

This study has been financially supported by the Academy of Finland and by an Award for the Advancement of European Science by the KSrber Foundation. We thank S.-L. Joutsiniemi for help in the measurements.

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evoked-responses of human auditory-cortex may be enhanced by preceding stimuli

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