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Presentation rate and magnitude of stimulus deviance effects on human pre-attentive change detection
ELSEVIER
Neuroscience Letters 193 (1995) 185-188
HlllDitllflCf LEITUlS
Presentation rate and magnitude of stimulus deviance effects on human pre-attentive change detection Erich Schr6ger a,*, Istv~in Winkler b,c alnstitute of Psychology, Ludwig-Maximilians-UniversittitMiinchen. Leopoldstr. 13, D-80802 Munich, Germany blnstitute,for Psychology, Hungarian Academy of Sciences, Budapest, Hungary CCognitive Brain Research Unit, Department of Psychology, Universi~ of Helsinki, Helsinki, Finland
Received 10 May 1995; revisedversion received 31 May 1995; accepted 31 May 1995
Abstract
The present study investigated the effects of the inter-stimulus interval (ISI) and the magnitude of deviance on the mismatch negativity (MMN), an event-related potential index of pre-attentive change detection. The latency of the MMN to infrequent changes in intensity and duration was prolonged by increasing the ISI from 400 ms to 4 s. Results indicate that these features are preserved in sensory memory for several seconds. By increasing the ISI the sharpness of the neural traces decreases, thus prolonging the change detection process. Keywords: Audition; Change detection; Event-related brain potential; Mismatch negativity; Auditory sensory memory; Neural
representation
Pre-attentive detection of biologically significant changes in the environment is crucial for avoiding potential dangers. Such a mechanism was revealed in the auditory modality by the mismatch negativity (MMN) [14] of the event-related brain potentials (ERP). This frontocentrally negative ERP component, usually peaking between 150 and 250 ms from stimulus onset, is elicited by infrequent auditory stimuli deviating from a repetitive standard sound in some physical feature [14]. The MMN reflects pre-attentive change detection because it is elicited even when subjects perform a task that is not related to the auditory stimuli [e.g. 2,18]. There exists a vast body of evidence suggesting that MMN is generated by a process registering the deviation of the incoming stimuli from the trace of the previous reference stimulus [14,15, 27]. Recent research revealed [28] that the traces involved in the mismatch process are stored by the second phase of auditory sensory memory, the synthesized auditory memory [13], which can maintain complex auditory information up to about 20 s [4]. This memory is of special relevance since it creates the informational basis for subse* Corresponding author, Tel.: +49 89 2180 5209; Fax: +49 89 2180 5211; E-mail: schr°ger@mip'paed'uni-muenchen'de"
quent information processing, that is, it lays the foundation for higher-level processes, such as auditory discrimination [10,24-25,27]. The present study investigated effects of the stimulus presentation rate and the magnitude of change in two features, intensity and duration, on the MMN component. Results were expected to clarify important parameters of this pre-attentive change detection process as well as the underlying memory representation. It has been shown previously that the neural traces storing frequency information can last up to about 10 s in young healthy adults [3,23] although this time is reduced in elderly [19] (see, however, Ref. [6]) and in patients with Alzheimer's disease [20]. However, no similar studies have been conducted for other auditory features. Furthermore, the present paradigm enabled one to study the interaction between the effects of the ISI and the amount of the physical separation between the deviant and standard stimulus. Ten paid healthy subjects (ages 22-35 years, mean 29.6 years, 4 male) participated in the experiment. Subjects gave informed consent after the nature of the study was explained to them. The subject was seated in a comfortable chair in an electrically shielded and acoustically
0304-3940/95l$09.50 © 1995 Elsevier Science IrelandLtd. All rights reserved SSDI 0304-3940(95)11696-Q
186
E. SchrOger, 1. Winkler / Neuroscience Letters 193 (1995) 185-188
Table 1 Grand-average MMN amplitudes (,uV) measured at Fz, separately for each deviant and experimental condition
Shoa ISI Long ISI
Intensity Deviant
Duration Deviant
Small
Large
Small
Large
-0.91"* (205) -0.64* (240)
-1.42"** (180) -1.10'*
-0.48* (170) -0.27 (245)
-0.22 (185) -0.75** (250)
(220)
The values in parentheses indicate the grand-average MMN peak latencies (ms) relative to change onset. One-tailed t-test: *P < 0.05; **P < 0.01; ***P < 0.001.
attenuated cabin. He/she was instructed to read a selfselected book and to ignore the auditory stimuli presented monaurally to his/her right ear via headphones. Five different stimuli were employed during the experiment (all presented with rise and fall times of 5 ms), the frequent ('standard') stimulus (frequency 700 Hz; intensity 70 dB SPL; duration 250 ms) and four infrequent ('deviant') ones differing from the standard either in intensity or duration (small intensity deviant --4 dB SPL relative to the intensity of the standard; large intensity deviant -10 dB SPL relative to the standard; small duration deviant 210 ms; large duration deviant 160 ms). Within each stimulus block, two different deviants were presented, each occurring with a probability of 0.15, one intensity (either small or large) and one duration deviant (again, either small or large). The standard-stimulus probability was always 0.7. In separate blocks, two different offset-to-onset ISis were tested: 400 ms (Short-ISI Condition) and 4 s (Long-ISI Condition). In the Short-ISI Condition, four blocks of 336 stimuli (each having a different combination of the intensity and duration deviants) were delivered, the Long-ISI Condition consisted of eight blocks with 168 stimuli, each. The order of experimental blocks was balanced across subjects. EEG was measured with Ag-Ag/CI electrodes from 10 scalp locations: Fpz, Fz, Cz, and Pz (10-20 system), both mastoids (1M and rM, respectively), two electrodes placed at 1/3 and 2/3 of the arc connecting Fz to 1M (L1, L2), and another two electrodes positioned symmetrically over the right hemisphere (R1, R2). The horizontal EOG was monitored at the outer canthus of the left eye. EEG and EOG were digitized by NeuroScan Inc. data acquisition unit (digitizing rate 200 Hz; bandpass 0.1-40 Hz) and subsequently filtered from 1 to 25 Hz. Epochs were of 700ms duration (including a lOOms prestimulus baseline). Epochs with a change exceeding 150/xV on any channel were rejected from further analysis. ERPs were averaged, separately for each condition and stimulus type. To estimate the MMN component difference waves were computed by subtracting the ERP to the standard
stimulus from the ERPs elicited by different deviant stimuli. The MMN response to deviation in duration is elicited in temporal relation to the latency at which the standard and deviant stimulus start to differ [8,28]. Therefore, MMN responses to small and large duration deviants were expected to peak, respectively, ca. 210 and 160 ms later than those to intensity deviants. MMN peak latencies to duration deviants were measured with reference to the 'deviation-onset' latency. Since the amplitude and latency of the MMN component are not necessarily correlated [9], both parameters were measured to reveal the effects of the manipulated variables. MMN amplitudes were measured as the mean amplitude in the 50-ms interval around the latency of the MMN peak in the corresponding grand-average response (see Table 1). MMN peak latencies for each subject were visually determined by three independent observers on the basis of the scalp distribution. The presence of the MMN component was tested by one-tailed one-group t-tests of the difference amplitudes recorded from Fz. The MMN amplitudes and peak latencies obtained in the different experimental conditions at Fz were compared by repeated measurement analyses of variances. Factors were ISI (levels: short versus long), Magnitude of Deviation (levels: small versus large), and, in the omnibus ANOVA only, Deviant Feature (levels: intensity versus duration). Fig. la shows the frontal (Fz) ERP responses elicited by standard, small-, and large-intensity-deviant stimuli, separately for the Short- and Long-ISI Conditions. The corresponding 'deviant - standard' difference curves are presented in Fig. lb. Both small and large intensity deviants elicited significant MMNs in both ISI conditions: the mean MMN amplitudes were significantly different from zero (Table 1). No significant ISI or Magnitude of Deviance effect was found on the MMN amplitude to intensity
ERPs . . . . Standard - - D e v i a n t Small Int. Dcv.
Difference Waves
Large Int. Dev.
Small Duc Dcv.
Small Int. Dev,
Largc Dur. eev.
Short ISI
A ~ i
Large lilt. Dev. |
Small Dot. Dev.
~
"1
--v"
" ~
Large Dttr. Dev
7
'
"v-
•
Long ISl .... t
~_
. ~Om'
.t
r~
+
c~0ms
Fig. 1. Frontal (Fz) ERPs elicited by the standards and by the different deviants (a,c) as well as the corresponding difference waves (b,d). ERPs are plotted in the interval from -100 to 600 ms relative to stimulus onset. MMN peak latencies (relative to stimulus onset) are indicated by black arrows.
I
E. SchrOger, L Winkler I Neuroscience Letters 193 (1995) 185-188
deviants. However, both of these factors independently affected the MMN peak latencies. Mean individual MMN peak latencies were 202 and 229 ms for the small- and 179 and 201 ms for the large-intensity-deviants in the Short- and Long-ISI Conditions, respectively. The corresponding ANOVA yielded a main effect of the ISI (El, 9 = 20.12, P < 0.01) and the Magnitude of Deviation (F1,9 = 37.73, P < 0.001). The ISI main effect was due to prolonged MMN latencies in the Long- compared with the Short-ISI Condition. Shorter MMN peak latencies were obtained for large than for small intensity deviants (Magnitude of Deviation effect). Fig. lc shows the frontal (Fz) ERP responses elicited by standard, small-, and large-duration-deviant stimuli, separately for the Short- and Long-ISI Conditions. The corresponding 'deviant - standard' difference curves are presented in Fig. ld. Variation in the MMN latency, due to different latencies for standard and deviant offset responses and sustained potentials [21], prevented two of the four MMN responses to reach significance when amplitudes were measured in fixed intervals around the grand-average peak (Table 1). Nevertheless, a MMN could be identified for each condition/magnitude of deviance. Again, no significant ISI or Magnitude of Deviation effect was found for the MMN amplitudes, but the ISI significantly affected the MMN peak latencies. Mean individual MMN peak latencies were 163 and 244 ms for small and 172 and 242 ms for large duration deviants in the Short- and Long-ISI Conditions, respectively. The MMN peak latency was longer for the Long- than for Short-ISI Condition (El, 9 = 124.80, P < 0 . 0 0 1 ) . l The omnibus-ANOVA of the latency measurements (comparing the two kinds of deviance) yielded an ISI x Deviant Feature interaction (F1, 9 = 20.90, P < 0.001) resulting from the larger ISI-related prolongation of the duration-MMN than of the intensity-MMN peak latency. The elicitation of MMNs both by intensity and duration deviants in the Long-ISI Condition demonstrated that, like the pitch information [3,23], stimulus intensity and duration are preserved for at least 4 s in the auditory sensory memory. The shorter MMN peak latency for large than small intensity deviants was anticipated on the basis of similar results for stimulus frequency [e.g. 17,25, 26]. The present experiment revealed that MMN peak latency, rather than the MMN amplitude correlated with the prolongation of the ISI. Two aspects of the ISI effect on the mismatch process can be considered: (1) increasing 1 The mismatchprocessis based upon comparingtwo memorytraces. Thus the process of encoding the deviant-stimulus duration is part of the measured MMN peak latency. Because the period of the encoding process might vary with the duration of the stimulus, the comparison between MMN peak latencies to different duration-deviants might be distorted. Therefore,the effects of the Magnitude of Deviation could not be estimated on the basis of the MMNs elicited by the present duration deviants.
187
the ISI decreases the frequency of MMN elicitation and (2) increasing the ISI results in increased decay of the standard-stimulus trace between two stimulus presentations. Contrary to the present findings, the first effect should result in more vigorous MMN responses due to decreased refractoriness of the MMN generator neurons (however, considerable MMN can be elicited even with very fast rates of stimulus presentations resulting in short inter-deviant intervals [16] showing that MMN generation is quite insensitive to refractoriness effects). The second possible consequence of increasing the ISI, the decreased standard-stimulus trace strength, was previously assumed to affect the MMN amplitude [e.g. 22,27]. However, no previous study manipulating the pre-deviant interval has shown a decrease of the MMN amplitude [3,6,12,16,23] (in some studies, no MMN was elicited with prolonged ISis [5,12,23]). It is possible that trace decay (loss of specificity or sharpness of the trace) can be considered analogous to decreasing the magnitude of stimulus separation (also resulting in prolonged MMN peak latencies [17,25], see the present intensity results). Thus the MMN peak latency could reflect the duration of the mismatch process detecting the deviance of the incoming stimulus from the standard-stimulus trace. This process lasts longer for small stimulus separations as well as when the trace became less sharp due to decay. Corroborating evidence was reported by Alain et al. [1]. These authors found that the MMN to infrequent breaks in a tone sequence consisting of two alternating tones was delayed by increasing the ISI between successive tones. Finally, varying the ISI affected the peak latency of the duration-MMN more than that of the intensity-MMN. This divergence between the intensity-, the duration-, and perhaps also the frequency-MMN, since no latency effect was reported in a previous study using comparable ISI [16], complements previous findings revealing different locations for MMN generators responding to deviances in different features [7,11]. The present finding suggests that the different generator locations are accompanied by functional differences between the neural traces of different features underlying the MMN [24]. In summary, the present study revealed pre-attentive detection of infrequent changes in intensity and duration even when stimuli were presented with relatively long ISis (4 s). Lower rates of stimulus presentation prolonged the time needed for change detection, whereas larger changes resulted in earlier detection. Differences in the storage of different stimulus features also affected the pre-attentive change detection process. This research was supported by the Max-PlanckInstitute of Psychological Research, Munich and the Hungarian National Scientific Fund (OTKA 006967). The authors thank to Martin Eimer for his valuable comments, and Christian Wolff, Renate Tschakert, and Angela Kallo for their help in data acquisition.
188
E. Schri~ger, L Winkler / Neuroscience Letters 193 (1995) 185-188
[1] Alain, C., Woods, D.L. and Ogawa, K.H., Brain indices of automatic pattern processing, NeuroReport, 6 (1994) 140-144. [2] Alho, K., Woods, D.L. and Algazi, A., Processing of auditory stimuli during auditory and visual attention as revealed by eventrelated potentials, Psychophysiol., 31 (1994) 469-479. [3] Brttcher-Gandor, C. and Ullsperger, P., Mismatch negativity in event-related potentials to auditory stimuli as a function of varying interstimulus interval, Psychophysiology, 29 (1992) 546-550. [4] Cowan, N., On short and long auditory stores, Psychol. Bull., 96 (1984) 341-370. [5] Cowan, N., Winkler, I., Teder, W, and N/i~it/inen, R., Memory prerequisites of mismatch negativity in the auditory event-related potentials (ERP), J. Exp. Psychol.: Learning, Memory, Cognition, 19 (1993) 909-921. [6] Czigler, I., Csibra, G. and Csontos, A., Age and inter-stimulus interval effects on event-related potentials to frequent and infrequent auditory stimuli, Biol. Psychol., 33 (1992) 195-206. [7] Giard, M.H., Lavikainen, J., Reinikainen, K., Perrin, F., Bertrand, O., Pernier, J. and N/itit~inen, R., Separate representations of stimulus frequency, intensity, and duration in auditory sensory memory, J. Cognitive Neurosci., (1995) in press. [8] Gomes, H., Ritter, W. and Vaughan, Jr., H.G., The nature of preattentive storage in the auditory system, J. Cognitive Neurosci., 7 (1995) 81-94. [9] Lang, A.H., Eerola, O., Korpilati, P., Holopainen, 1., Salo, S. and Aaltonen, O., Practical issues in the clinical application of the mismatch negativity, Ear Hear. (1995) 118-130. [10] Lang, A.H., Nyrke, T., Ek, M., Aaltonen, O., Raimo, I. and Niiiittinen, R., Pitch discrimination performance and auditory event-related potentials. In C.H.M. Brunia, A.W.K. Gaillard, A. Kok, G. Mulder and M.N. Verbaten (Eds.), Psychophysiological Brain Research, Tilburg University Press, 1990, pp. 294-298. [11] Lev/inen, S., Haft, R., McEvoy, L. and Sams, M., Responses of the human auditory cortex to changes in one vs. two stimulus features, Exp. Brain Res., 97 (1993) 177-183. [12] M~intysalo, S. and Nii/it/inen, R., The duration of a neuronal trace of an auditory stimulus as indicated by event-related potentials, Biol. Psychol., 24 (1987) 183-195. [13] Massaro, D.W., Experimental Psychology and Information Processing, Rand McNally, Chicago, 1975. [14] N~iiittinen, R., Attention and Brain Function, Erlbaum, Hillsdale, NJ, 1992.
[15] Nii~it~inen, R., Paavilainen, P., Alho, K., Reinikainen, K. and Sams, M. Do event-related potentials reveal the mechanism of the auditory sensory memory in the human brain? Neurosci. Lett., 98 (1989) 217-221. [16] Nii~it/inen, R., Paavilainen, P., Alho, K., Reinikainen, K. and Sams, M., Inter-stimulus interval and the mismatch negativity. In C. Barber and T. Blum (Eds.), Evoked Potentials III, Butterworths, London, 1987, pp. 392-397. [17] N~tiinen, R., Simpson, M. and Loveless, N.E., Stimulus deviance and evoked potentials, Biol. Psychol., 14 (1982) 53-98. [18] Paavilainen, P., Tiitinen, H., Alho, K. and Niiiit'~nen, R., Mismatch negativity to slight pitch changes outside strong attentional focus, Biol. Psychol., 37 (1993) 32-41. [19] Pekkonen, E., Jousmiiki, V., Partanen, J. and Karhu, J., Mismatch negativity area and age-related auditory memory, Electroencephalogr. Clin. Neurophysiol., 87 (1993) 321-325. [20] Pekkonen, E., Jousm/iki, V., Krnrnen, M., Reinikainen, K. and Partanen, J., Auditory sensory memory impairment in Alzheimer's disease: an event-related potential study, NeuroReport, 5 (1994) 2537-2540. [21] Picton, T.W., Woods, D.L. and Proulx, G.B., Human auditory sustained potentials. I. The nature of the response, Electroencephalogr. Clin. Neurophysiol., 45 (1978) 186--197. [22] Sams, M., Alho, K. and Niiiittinen, R., Short-term habituation and dishabituation of the mismatch negativity of the ERP, Psychophysiology, 21 (1984) 434-441. [23] Sams, M., Haft, R., Rif, J. and Knuutila, J., The human auditory sensory memory trace persists about 10 sec: neuromagnetic evidence, J. Cognitive Neurosci., 5 (1993) 363-370. [24] Schrrger, E., Processing of auditory deviants with changes in one vs. two stimulus dimensions, Psychophysiology 32 (1995) 55-65. [25] Tiitinen, H., May, P., Reinikainen, K. and Nii/St~en, R., Attentive novelty detection in humans is governed by pre-attentive sensory memory, Nature, 372 (1994) 90-92. [26] Winkler, I., Paavilainen, P. and Ntitit/inen, R., Can echoic memory store two traces simultaneously? A study of event-related brain potentials, Psychophysiology, 29 (1992) 337-349. [27] Winkler, I., Reinikainen, K. and Niitittinen, R., Event-related brain potentials reflect traces of echoic memory in humans, Percept. Psychophys., 53 (1993)443-449. [28] Winkler, I. and Schrrger, E., Neural representation for the temporal structure of sound patterns, NeuroReport, 6 (1995) 690--694.
Neuroscience Letters 193 (1995) 185-188
HlllDitllflCf LEITUlS
Presentation rate and magnitude of stimulus deviance effects on human pre-attentive change detection Erich Schr6ger a,*, Istv~in Winkler b,c alnstitute of Psychology, Ludwig-Maximilians-UniversittitMiinchen. Leopoldstr. 13, D-80802 Munich, Germany blnstitute,for Psychology, Hungarian Academy of Sciences, Budapest, Hungary CCognitive Brain Research Unit, Department of Psychology, Universi~ of Helsinki, Helsinki, Finland
Received 10 May 1995; revisedversion received 31 May 1995; accepted 31 May 1995
Abstract
The present study investigated the effects of the inter-stimulus interval (ISI) and the magnitude of deviance on the mismatch negativity (MMN), an event-related potential index of pre-attentive change detection. The latency of the MMN to infrequent changes in intensity and duration was prolonged by increasing the ISI from 400 ms to 4 s. Results indicate that these features are preserved in sensory memory for several seconds. By increasing the ISI the sharpness of the neural traces decreases, thus prolonging the change detection process. Keywords: Audition; Change detection; Event-related brain potential; Mismatch negativity; Auditory sensory memory; Neural
representation
Pre-attentive detection of biologically significant changes in the environment is crucial for avoiding potential dangers. Such a mechanism was revealed in the auditory modality by the mismatch negativity (MMN) [14] of the event-related brain potentials (ERP). This frontocentrally negative ERP component, usually peaking between 150 and 250 ms from stimulus onset, is elicited by infrequent auditory stimuli deviating from a repetitive standard sound in some physical feature [14]. The MMN reflects pre-attentive change detection because it is elicited even when subjects perform a task that is not related to the auditory stimuli [e.g. 2,18]. There exists a vast body of evidence suggesting that MMN is generated by a process registering the deviation of the incoming stimuli from the trace of the previous reference stimulus [14,15, 27]. Recent research revealed [28] that the traces involved in the mismatch process are stored by the second phase of auditory sensory memory, the synthesized auditory memory [13], which can maintain complex auditory information up to about 20 s [4]. This memory is of special relevance since it creates the informational basis for subse* Corresponding author, Tel.: +49 89 2180 5209; Fax: +49 89 2180 5211; E-mail: schr°ger@mip'paed'uni-muenchen'de"
quent information processing, that is, it lays the foundation for higher-level processes, such as auditory discrimination [10,24-25,27]. The present study investigated effects of the stimulus presentation rate and the magnitude of change in two features, intensity and duration, on the MMN component. Results were expected to clarify important parameters of this pre-attentive change detection process as well as the underlying memory representation. It has been shown previously that the neural traces storing frequency information can last up to about 10 s in young healthy adults [3,23] although this time is reduced in elderly [19] (see, however, Ref. [6]) and in patients with Alzheimer's disease [20]. However, no similar studies have been conducted for other auditory features. Furthermore, the present paradigm enabled one to study the interaction between the effects of the ISI and the amount of the physical separation between the deviant and standard stimulus. Ten paid healthy subjects (ages 22-35 years, mean 29.6 years, 4 male) participated in the experiment. Subjects gave informed consent after the nature of the study was explained to them. The subject was seated in a comfortable chair in an electrically shielded and acoustically
0304-3940/95l$09.50 © 1995 Elsevier Science IrelandLtd. All rights reserved SSDI 0304-3940(95)11696-Q
186
E. SchrOger, 1. Winkler / Neuroscience Letters 193 (1995) 185-188
Table 1 Grand-average MMN amplitudes (,uV) measured at Fz, separately for each deviant and experimental condition
Shoa ISI Long ISI
Intensity Deviant
Duration Deviant
Small
Large
Small
Large
-0.91"* (205) -0.64* (240)
-1.42"** (180) -1.10'*
-0.48* (170) -0.27 (245)
-0.22 (185) -0.75** (250)
(220)
The values in parentheses indicate the grand-average MMN peak latencies (ms) relative to change onset. One-tailed t-test: *P < 0.05; **P < 0.01; ***P < 0.001.
attenuated cabin. He/she was instructed to read a selfselected book and to ignore the auditory stimuli presented monaurally to his/her right ear via headphones. Five different stimuli were employed during the experiment (all presented with rise and fall times of 5 ms), the frequent ('standard') stimulus (frequency 700 Hz; intensity 70 dB SPL; duration 250 ms) and four infrequent ('deviant') ones differing from the standard either in intensity or duration (small intensity deviant --4 dB SPL relative to the intensity of the standard; large intensity deviant -10 dB SPL relative to the standard; small duration deviant 210 ms; large duration deviant 160 ms). Within each stimulus block, two different deviants were presented, each occurring with a probability of 0.15, one intensity (either small or large) and one duration deviant (again, either small or large). The standard-stimulus probability was always 0.7. In separate blocks, two different offset-to-onset ISis were tested: 400 ms (Short-ISI Condition) and 4 s (Long-ISI Condition). In the Short-ISI Condition, four blocks of 336 stimuli (each having a different combination of the intensity and duration deviants) were delivered, the Long-ISI Condition consisted of eight blocks with 168 stimuli, each. The order of experimental blocks was balanced across subjects. EEG was measured with Ag-Ag/CI electrodes from 10 scalp locations: Fpz, Fz, Cz, and Pz (10-20 system), both mastoids (1M and rM, respectively), two electrodes placed at 1/3 and 2/3 of the arc connecting Fz to 1M (L1, L2), and another two electrodes positioned symmetrically over the right hemisphere (R1, R2). The horizontal EOG was monitored at the outer canthus of the left eye. EEG and EOG were digitized by NeuroScan Inc. data acquisition unit (digitizing rate 200 Hz; bandpass 0.1-40 Hz) and subsequently filtered from 1 to 25 Hz. Epochs were of 700ms duration (including a lOOms prestimulus baseline). Epochs with a change exceeding 150/xV on any channel were rejected from further analysis. ERPs were averaged, separately for each condition and stimulus type. To estimate the MMN component difference waves were computed by subtracting the ERP to the standard
stimulus from the ERPs elicited by different deviant stimuli. The MMN response to deviation in duration is elicited in temporal relation to the latency at which the standard and deviant stimulus start to differ [8,28]. Therefore, MMN responses to small and large duration deviants were expected to peak, respectively, ca. 210 and 160 ms later than those to intensity deviants. MMN peak latencies to duration deviants were measured with reference to the 'deviation-onset' latency. Since the amplitude and latency of the MMN component are not necessarily correlated [9], both parameters were measured to reveal the effects of the manipulated variables. MMN amplitudes were measured as the mean amplitude in the 50-ms interval around the latency of the MMN peak in the corresponding grand-average response (see Table 1). MMN peak latencies for each subject were visually determined by three independent observers on the basis of the scalp distribution. The presence of the MMN component was tested by one-tailed one-group t-tests of the difference amplitudes recorded from Fz. The MMN amplitudes and peak latencies obtained in the different experimental conditions at Fz were compared by repeated measurement analyses of variances. Factors were ISI (levels: short versus long), Magnitude of Deviation (levels: small versus large), and, in the omnibus ANOVA only, Deviant Feature (levels: intensity versus duration). Fig. la shows the frontal (Fz) ERP responses elicited by standard, small-, and large-intensity-deviant stimuli, separately for the Short- and Long-ISI Conditions. The corresponding 'deviant - standard' difference curves are presented in Fig. lb. Both small and large intensity deviants elicited significant MMNs in both ISI conditions: the mean MMN amplitudes were significantly different from zero (Table 1). No significant ISI or Magnitude of Deviance effect was found on the MMN amplitude to intensity
ERPs . . . . Standard - - D e v i a n t Small Int. Dcv.
Difference Waves
Large Int. Dev.
Small Duc Dcv.
Small Int. Dev,
Largc Dur. eev.
Short ISI
A ~ i
Large lilt. Dev. |
Small Dot. Dev.
~
"1
--v"
" ~
Large Dttr. Dev
7
'
"v-
•
Long ISl .... t
~_
. ~Om'
.t
r~
+
c~0ms
Fig. 1. Frontal (Fz) ERPs elicited by the standards and by the different deviants (a,c) as well as the corresponding difference waves (b,d). ERPs are plotted in the interval from -100 to 600 ms relative to stimulus onset. MMN peak latencies (relative to stimulus onset) are indicated by black arrows.
I
E. SchrOger, L Winkler I Neuroscience Letters 193 (1995) 185-188
deviants. However, both of these factors independently affected the MMN peak latencies. Mean individual MMN peak latencies were 202 and 229 ms for the small- and 179 and 201 ms for the large-intensity-deviants in the Short- and Long-ISI Conditions, respectively. The corresponding ANOVA yielded a main effect of the ISI (El, 9 = 20.12, P < 0.01) and the Magnitude of Deviation (F1,9 = 37.73, P < 0.001). The ISI main effect was due to prolonged MMN latencies in the Long- compared with the Short-ISI Condition. Shorter MMN peak latencies were obtained for large than for small intensity deviants (Magnitude of Deviation effect). Fig. lc shows the frontal (Fz) ERP responses elicited by standard, small-, and large-duration-deviant stimuli, separately for the Short- and Long-ISI Conditions. The corresponding 'deviant - standard' difference curves are presented in Fig. ld. Variation in the MMN latency, due to different latencies for standard and deviant offset responses and sustained potentials [21], prevented two of the four MMN responses to reach significance when amplitudes were measured in fixed intervals around the grand-average peak (Table 1). Nevertheless, a MMN could be identified for each condition/magnitude of deviance. Again, no significant ISI or Magnitude of Deviation effect was found for the MMN amplitudes, but the ISI significantly affected the MMN peak latencies. Mean individual MMN peak latencies were 163 and 244 ms for small and 172 and 242 ms for large duration deviants in the Short- and Long-ISI Conditions, respectively. The MMN peak latency was longer for the Long- than for Short-ISI Condition (El, 9 = 124.80, P < 0 . 0 0 1 ) . l The omnibus-ANOVA of the latency measurements (comparing the two kinds of deviance) yielded an ISI x Deviant Feature interaction (F1, 9 = 20.90, P < 0.001) resulting from the larger ISI-related prolongation of the duration-MMN than of the intensity-MMN peak latency. The elicitation of MMNs both by intensity and duration deviants in the Long-ISI Condition demonstrated that, like the pitch information [3,23], stimulus intensity and duration are preserved for at least 4 s in the auditory sensory memory. The shorter MMN peak latency for large than small intensity deviants was anticipated on the basis of similar results for stimulus frequency [e.g. 17,25, 26]. The present experiment revealed that MMN peak latency, rather than the MMN amplitude correlated with the prolongation of the ISI. Two aspects of the ISI effect on the mismatch process can be considered: (1) increasing 1 The mismatchprocessis based upon comparingtwo memorytraces. Thus the process of encoding the deviant-stimulus duration is part of the measured MMN peak latency. Because the period of the encoding process might vary with the duration of the stimulus, the comparison between MMN peak latencies to different duration-deviants might be distorted. Therefore,the effects of the Magnitude of Deviation could not be estimated on the basis of the MMNs elicited by the present duration deviants.
187
the ISI decreases the frequency of MMN elicitation and (2) increasing the ISI results in increased decay of the standard-stimulus trace between two stimulus presentations. Contrary to the present findings, the first effect should result in more vigorous MMN responses due to decreased refractoriness of the MMN generator neurons (however, considerable MMN can be elicited even with very fast rates of stimulus presentations resulting in short inter-deviant intervals [16] showing that MMN generation is quite insensitive to refractoriness effects). The second possible consequence of increasing the ISI, the decreased standard-stimulus trace strength, was previously assumed to affect the MMN amplitude [e.g. 22,27]. However, no previous study manipulating the pre-deviant interval has shown a decrease of the MMN amplitude [3,6,12,16,23] (in some studies, no MMN was elicited with prolonged ISis [5,12,23]). It is possible that trace decay (loss of specificity or sharpness of the trace) can be considered analogous to decreasing the magnitude of stimulus separation (also resulting in prolonged MMN peak latencies [17,25], see the present intensity results). Thus the MMN peak latency could reflect the duration of the mismatch process detecting the deviance of the incoming stimulus from the standard-stimulus trace. This process lasts longer for small stimulus separations as well as when the trace became less sharp due to decay. Corroborating evidence was reported by Alain et al. [1]. These authors found that the MMN to infrequent breaks in a tone sequence consisting of two alternating tones was delayed by increasing the ISI between successive tones. Finally, varying the ISI affected the peak latency of the duration-MMN more than that of the intensity-MMN. This divergence between the intensity-, the duration-, and perhaps also the frequency-MMN, since no latency effect was reported in a previous study using comparable ISI [16], complements previous findings revealing different locations for MMN generators responding to deviances in different features [7,11]. The present finding suggests that the different generator locations are accompanied by functional differences between the neural traces of different features underlying the MMN [24]. In summary, the present study revealed pre-attentive detection of infrequent changes in intensity and duration even when stimuli were presented with relatively long ISis (4 s). Lower rates of stimulus presentation prolonged the time needed for change detection, whereas larger changes resulted in earlier detection. Differences in the storage of different stimulus features also affected the pre-attentive change detection process. This research was supported by the Max-PlanckInstitute of Psychological Research, Munich and the Hungarian National Scientific Fund (OTKA 006967). The authors thank to Martin Eimer for his valuable comments, and Christian Wolff, Renate Tschakert, and Angela Kallo for their help in data acquisition.
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