Acta Oto-Laryngologica
ISSN: 0001-6489 (Print) 1651-2251 (Online) Journal homepage: http://www.tandfonline.com/loi/ioto20
Attention Effects on the Auditory Event-related Potential R. Nä;ätänen & W. Teder To cite this article: R. Nä;ätänen & W. Teder (1991) Attention Effects on the Auditory Event-related Potential, Acta Oto-Laryngologica, 111:sup491, 161-167, DOI: 10.3109/00016489109136794 To link to this article: http://dx.doi.org/10.3109/00016489109136794
Published online: 08 Jul 2009.
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Acta Otolaryngol (Stockh) 1991; Suppl. 491: 161-167
Attention Effects on the Auditory Event-related Potential R. NUTANEN and W. TEDER From the Department of Psychology, University of Helsinki, Finland
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R. Naatanen, W. Teder. Attention effects on the auditory event-related potential. Acta Otolaryngol (Stockh) 1991; Suppl 491: 161-167. Studies on selective-attention effects on the auditory event-related brain potential (ERP) are reviewed. Brainstem components of the ERP have not been shown to be sensitive to attention. On the other hand, attention effects in the middle-latency range ( 1 2-50 ms from stimulus onset) appear to occur under some conditions but it is not clear whether these effects are exogenous or endogenous. The predominant attention effect on the auditory ERP is the processing negativity, a slow endogenous negativity which often commences well before the exogenous (supratemporal) NI component peaks (at about 100 ms post-stimulus), therefore giving the impression that this exogenous component is attention-sensitive. It is not yet settled, however, whether even these exogenous processes under some conditions might be modulated by selective attention. Key words: selective aiteniion. NI,processing negativity.
INTRODUCTION Event-related potentials (ERP) might give us some indication as to how the brain selects desired sensory information in audition, i.e., what is selective attention and how is processing of sensory input modified by it. ERP findings claimed to indicate auditory stimulus selection can be classified into three categories: 1) very early effects; 2) enhancement of some exogenous component of the N1 wave; 3) the processing negativity (PN).
VERY EARLY EFFECTS OF AUDITORY SELECTIVE ATTENTION A number of studies (1-6) have explored the possibility that selective attention enhances auditory brainstem responses elicited by attended stimuli and/or attenuates these responses to ignored stimuli. The majority of these studies concluded that brainstem responses are not modified by attention. Lukas (3, 4), however, reported that some part of the brainstem response was larger when the subject attended to auditory stimuli than to visual stimuli. There are, however, some serious problems (see 7, 8) in interpreting these data in this way. In conclusion, it appears, in the light of the evidence available, that selective attention does not modulate auditory brainstem responses. Studies on polysynaptic eye-blink reflexes (see 9) suggest, however, that selective attention might modulate quite early phases of auditory information processing (10, 1 1). On the basis of their quite recent results obtained by combining reflex and ERP measurements, Hackley et al. (12) suggested that whereas evoked auditory activity in the lower brainstem is not modified by attention, later activity mediated in the upper brainstem can be attention-modulated. Puel et al. (13), in a recent study on cochlear echo amplitudes for sound stimuli, concluded that the auditory efferent system might be able to selectively modulate the cochlear response to sound according to the direction of attention. These very interesting results demonstrating an attenuation of the sound-emitted echo amplitude in the closed ear canal when a task demanding visual attention is introduced to a resting subject cannot, however, be regarded as providing a conclusive demonstration for selective modulation. It was not tested whether the echo amplitude might also be reduced compared with resting-state levels during an auditory task as it was during a visual task. To this end, their effect might well have been nonspecific, 11-918418
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162 R. Naatanen and W. Teder i.e., caused by increased nonspecific arousal accompanying task performance. This criticism is similar to that directed to the reduction of the cochlear response to clicks observed by HernAndez-Peon et al. (14) when the cat’s attention was elicited by the appearance of an interesting stimulus (mice in a glass jar) in its visual field (15). The earliest ERP effects of selective attention in audition might occur in the middle-latency range (1 2-50 ms from stimulus onset; (16)). McCallum et al. ( 1 7) observed an early attention effect commencing at a latency of 26 ms in their free-field listening situation. (There was a possible effect even at an onset latency of 15 ms, but this needs to be replicated; see 17). Their effect emerged as a slow negative displacement of the ERP to attended stimuli relative to that to unattended stimuli, suggesting an emergence of an endogenous component rather than a modulation of an exogenous (middle-latency) component. On the other hand, the “P20-50” effect on Woldorff et al. (2) might be of either exogenous (then possibly involving, according to the authors, the Pa component) or endogenous nature, as also suggested by the authors themselves. This effect, obtained in selective listening to dichotic stimuli presented with very short interstimulus intervals (ISI), emerged as a positive ERP displacement commencing at about 20 ms post-stimulus and continuing for some 20-30 ms. On the other hand, Linden et al. (18), using a somewhat different paradigm, found no selective-attentional modulation of the middle-latency components. ATTENTIONAL ENHANCEMENT OF SOME EXOGENOUS COMPONENT OF THE AUDITORY N 1 WAVE In their now classic paper from 1973, Hillyard, Hink, Schwent & Picton (19) were the first to demonstrate an attentional enhancement of the N1 wave so that this could not be questioned on methodological grounds (for a review, see 20). The authors interpreted this finding in terms of an enhancement of an exogenous N1 component, i.e., of some exogenous generator process contributing to the N l wave. (For a definition of an ERP component, see 21.) In 1978, an endogenous attention effect termed the processing negativity (PN) was, however, described by Naatanen et al. (22). This protracted negativity commenced after the N1 peak and lasted for several hundreds of milliseconds; therefore an exogenous N 1 process could not, presumably, be involved. The authors further suggested that even Hillyard et al.’s (19) effect might have been caused by a PN rather than an enhancement of an exogenous N1 component. According to them, Hillyard and colleagues’ very fast stimulus rate might have caused PN to commence early enough to overlap the “exogenous N1 component”. A number of further studies (for a review, see 23) showed that PN is the main, perhaps the only, effect of selective attention at the N1 latency range. Meanwhile it had become increasingly clear that there are at least three exogenous components in the N1 wave (for a review, see 21) and, further, that if attention indeed enhances some exogenous N l component, then that probably is, judging from similarities in latency and topography, the supratemporal N 1 component (see 8). Quite recent studies (2, 12) from Hillyard’s laboratory, however, demonstrated an attention effect with a time course which very closely paralleled that of the supratemporal N1 component. These results were obtained under heavy-load dichotic conditions requiring a very strong attentional focus, with the most essential aspect of this design being the use of very short ISIs. Therefore the authors proposed that under such conditions, some exogenous N1 generator process might be modulated by selective attention. Teder et al. (24) wished to demonstrate that the selective-attention effect obtained even with very short ISIs is due to a PN rather than to an enhancement of some exogenous N1 process. These authors compared attention effects with four different IS1 (random, rectangular distribution) conditions: (A) 60-100 ms; (B) 120-200 ms; (C) 360-600 ms; (D) 600-1000 ms.
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ISI: 60- 100 rns
Difference waves: attend-unattend (Nd) -4pv
Random ISls: 60-100 ms - 120-200 ms 360.600 ms 600-loo0 ms .....
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Fig. 1. Top: Grand-average vertex (Cz) ERPs to unattended and attended tones for left-ear stimuli from four random-IS1 conditions (60-100 ms, 120-200 ms, 360-600 ms, 600-1 000 ms). S=stimulus onset. Bottom: Superimposition of difference waves obtained by subtracting ERPs to unattended stimuli from those to attended stimuli separately for each IS1 condition shown above.
Standard stimuli (96%) were tones of 300 Hz,deviant stimuli (4%) tones of 330 Hz.The ear of entry was random. The subject’s task was to press a button each time a deviant stimulus (a “target”) appeared within the input stream to a designated ear. Fig. 1 (two top rows) presents grand-average (10 subjects) vertex ERPs for attended and ignored stimuli separately for each IS1 condition. The difference waves (Nd) obtained by subtracting unattend ERPs from the respective attend ERPs are shown in the bottom of the figure. A comparison of the Nds from the two “short-ISI” conditions with those from the two “long-ISI” conditions shows a slight prolongation of the peak of the early Nd phase with IS1 prolongation. This pattern of data, therefore, seems to suggest that the peak latency of the early Nd might, within a certain range, be a rather continuous function of the mean ISI. This supports the interpretation that even with very short ISIs, the ERP attention effect is due to PN rather than to an enhancement of a n exogenous N1 component. Further evidence for this interpretation was provided by the very recent results of Naatanen et al. (25). These authors presented tones of 300 Hz to the subject’s left ear and those of 6000 Hz to the right ear in random order and with ISIs randomly varying from 60 ms to 200 ms. The subject was instructed to count occasional slightly higher tones within a designated input stream.
164 R. Naatanen and W. Teder
Left, 300 Hz
Right, 6000 Hz
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(Nd)
Fig. 2. Grand-average vertex (Cz)ERPs to attended and unattended tones (foprow) and respective difference waves (attend minus unattend) for left-ear (300 Hz)and right-ear stimuli (6000 Hz). ISI: random 60-200 ms. S=stimulus onset.
Grand-average (9 subjects) vertex data are shown in Fig. 2. The top row of this figure shows that ERPs both to unattended and attended stimuli are much larger for the low than high tones (see 21). On the other hand, Nds for the two tones are very similar. This pattern of data suggests that mechanisms of exogenous N1 generation and those of the attention effect are different for one would expect the attention effect to be proportional t o the strength of the generator response elicited in the a b s e v e of attention. Consequently, it appers that the supratemporal component of the exogenous N1 is not modulated by selective attention. Giard et al. (26), however, have obtained an interesting attention effect which may or may not express an attentional enhancement of some exogenous type of neuronal population on the supratemporal cortex. This effect emerged as a small negativity which preceded the early phase of the typical Nd and showed a pitch-specific distribution. Finally, two recent studies (27,28) suggest that when irrelevant stimuli are visual, attending t o auditory stimuli causes an enhancement of the negative component belonging to the Tcomplex (see 29). PROCESSING NEGATIVITIES Processing negativities (PN) were already illustrated in the afore-going (Figs. 1 and 2). The early, sensory-specific component of the P N was suggested by Naatanen (8, 23) to be generated by an on-line matching process by which the brain rapidly chooses relevant stimuli among irrelevant stimuIi for further processing or response. This matching process occurs, on this hypothesis, between a sensory input and a voluntarily maintained neural representation, “the attentional trace”, where sensory information essential for selecting relevant stimuli among irrelevant stimuli is stored. This theory predicts that even irrelevant stimuli elicit some P N and, further, that this P N is larger and longer, the more similar an irrelevant stimulus is to the relevant. These and some other predictions of the attentional-trace theory were confirmed in a series of studies by Alho et al. (e.g., 30; for a review, see 8). Thus the negative difference wave (Nd) does not reveal the PN but rather the difference between PNs t o relevant and irrelevant stimuli (23, 30). P N also has a later, frontal component (31, see also 20) but its functional significance is still an open question. This component might reflect further processing of stimuli selected in initial
Attention effects on the auditory event related potential 165 attentional-trace selection or rehearsal activity maintaining the attentional trace (23, see also 32). Naatanen & Picton (21) proposed, in line with the latter interpretation, that this component might be generated by a central “executive” mechanism which initiates and controls the selective-attention state, more specifically, the sensory-specific mechanism of stimulus selection, the attentional trace.
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CONCLUDING SUMMARY The earliest selective-attention effects on the auditory ERP are not yet settled. Whereas it is quite clear that brainstem respones are not modulated by attention, effects at the middlelatency range under certain conditions seem to be quite firmly established. On the other hand, it is unclear whether they are of exogenous or endogenous nature although in the light of the available evidence, the latter alternative appears more likely. Puel et al.’s (13) data tentatively suggest that even the cochlear response might be sensitive to selective attention but an alternative interpretation in terms of a nonspecific effect should be ruled out. PN appears to be the predominant, in many conditions even the only, effect of selective attention on auditory ERPs. However, the long controversy involving a possible selectiveattention effect on some exogenous N1 component is not yet settled. Tentatively, it appears that the supratemporal N1 component is insensitive to attention (unless Giard et al.’s ( 2 5 ) effect originate as from an attentionally sensitive subpopulation of neurons generating this component). On the other hand, the negative component of the T-complex (maximal over the temporal sites) might be sensitive to intermodal selective attention.
ACKNOWLEDGEMENTS This study was supported by The Academy of Finland and by The Signe and Ane Gyllenberg Foundation (Helsinki, Finland).
REFERENCES I . Hillyard SA, Woldorff M, Mangun GR, Hansen JC. Mechanisms of early selective attention in auditory and visual modalities. In: Ellingson RJ, Murray NMF, Halliday AM, eds. The London symposia (EEG Supplement 39). Amsterdam: Elsevier, 1987: 3 17-24. 2. Woldorff M, Hansen JC, Hillyard SA. Evidence for effects of selective attention in the mid-latency range of the human auditory event-related potential. In: Johnson R Jr, Rohrbaugh JW, Parasuraman R, eds. Current trends in event-related potential research. (EEG Supplement 40.) Amsterdam: Elsevier, 1987: 146-54. 3. Lukas JH. Human auditory attention: The olivocochlear bundle may function as a peripheral filter. Psychophysiology 1980; 17: 444-52. 4. Lukas JH. The role of efferent inhibition in human auditory attention. An examination of the auditory brainstem potentials. Int J Neurosci 198 1; 12: 137-45. 5. Connolly JF, Aubry K, McGillivary N. Human brainstem responses fail to provide evidence of efferent modulation of auditory input during dual modal focused attention. Psychophysiology 1989; 26: 292-303. 6. Picton TW, Stapells DR, Campbell KB. Auditory evoked potentials from the human cochlea and brainstem. J Otolaryngol 1981; 10: 1-41. 7. Donald MW. Neural selectivity in auditory attention: Sketch of a theory. In: Gaillard AWK, Ritter W, eds. Tutorials in ERP Research: Endogenous components. Amsterdam: NorthHolland, 1983: 37-77. 8. Naatanen R. The role of attention in auditory information processing as revealed by event-related potentials and other brain measures of cognitive function. Behav Brain Sci 1990; 13: 201-288. 9. Graham FK. The more or less startling effects of weak prestimulation. Psychophysiology 1975; 12: 238-48. 10. Hackley SA, Graham FK. Early selective attention effects on cutaneous and acoustic blink reflexes. Physiological Psycho1 1984; 1 1: 235-42.
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166 R. Naatanen and W. Teder 1 1 . Hackley SA, Graham FK. Effects of attending selectively to the spatial position of reflex-eliciting and reflexmodulating stimuli. J Exp Psychol 1987; 13: 41 1-24. 12. Hackley SA, Woldorff M, Hillyard SA. Combined use of microreflexes and event-related brain potentials as measures of auditory selective attention. Psychophysiology 1987; 24: 632-47. 13. Puel J, Bonfils P, Pujol R. Selective attention modifies the active micromechanical properties of the cochlea. Brain Res 1988; 447: 380-3. 14. Hernlndez-Peon R, Schemer H, Jouvet M. Modification of electrical activity in the cochlear nucleus during attention in anaesthetized cats. Science 1956; 123: 331-2. 15. Naatanen R. Selective attention and evoked potentials. Annales Academia Scientiarum Fennicae B, 151: 1-226. 16. Starr A, Don M. Brain potentials evoked by acoustic stimuli. In: Picton TW, ed. Human event-related potentials. EEG Handbook (revised series vol. 3). Amsterdam: Elsevier, 1988: 97-1 57. 17. McCallum WC, Curry SH, Cooper R, Pocock PV, Papakostopoulos D. Brain event-related potentials as indicators of early selective processes in auditory target localization. Psychophysiology 1983; 20: 1-1 7. 18. Linden RD, Picton TW, Hamel G , Campbell KB. Human auditory steady-state evoked potentials during selective attention. Electroencephalogr Clin Neurophysiol 1987; 66: 145-59. 19. Hillyard SA, Hink RF, Schwent VL, Picton TW. Electrical signs of selective attention in the human brain. Science 1973; 182: 177-80. 20. Naatanen R, Michie PT. Early selective attention effects o n the evoked potential. A critical review and reinterpretation. Biol Psychol 1979; 8: 81-1 36. 21. Naatanen R, Picton TW. The NI wave of the human electric and magnetic response to sound: A review and an analysis of the component structure. Psychophysiology 1987; 24: 375-425. 22. Naatanen R, Gaillard AWK, Mantysalo S. Early selective attention effect on evoked potential reinterpreted. Acta Psychol 1978; 42: 31-29. 23. Naatanen R. Processing negativity: An evoked-potential reflection of selective attention. Psychol Bull 1982; 92: 605-40. 24. Teder W, Alho K, Reinikainen K, Naatanen R. Interstimulus interval and the selective attention effect
on auditory event-related potentials: Is there a genuine “N I-effect?’. Submitted. 25. Naatanen R, Teder W, Alho K, Lavikainen J. Separability of the selective-attention effect and NI component of the auditory event-related brain potential. In preparation. 26. Giard MH, Perrin F, Pernier J, Peronnet F. Several attention-related waveforms in auditory areas: a topographic study. Electroencepahlogr Clin Neurophysiol 1988; 69: 371-84. 27. Hackley SA, Woldorff M, Hillyard SA. Cross-modal selective attention effects on retinal, myogenic, brainstem and cerebral evoked potentials. Psychophysiology, in press. 28. Woods DL. The physiological basis of selective attention: Implications of event-related potential studies. In: Johnson R Jr, Rohrbaugh JW, Parasuraman R, eds. Event-related brain potentials: Issues and interdisciplinary vantages. New York: Oxford Press, in press. 29. Wolpaw JR, Penry JK. A temporal component of the auditory evoked response. Electroencephalogr Clin Neurophysiol 1975; 39: 609-20. 30. Alho K, Tottola K, Reinikainen K, Sams M, Naatanen R. Brain mechanism of selective listening reflected by event-related potentials. Electroencephalogr Clin Neurophysiol 1987; 68: 458-70. 31. Hansen JC, Hillyard SA. Endogenous brain potentials associated with selective auditory attention. Electroencephalogr Clin Neurophysiol 1980; 49: 277-90. 32. Hansen JC, Hillyard SA. Selective attention to multidimensional auditory stimuli. J Exp Psychol 1983; 9: 1-19. Address for correspondence: R. Naatanen, Department of Psychology, University of Helsinki, Ritarikatu 5, SF-00170 Helsinki, Finland
Attention effects on the auditory event related potential 161
DISCUSSION
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Participants: Hoke, Naatanen, Schreiner
The model might be used to assess objectively communication disorders in patients whose peripheral auditory functions are normal but who are unable to recognize speech under certain conditions, especially in the presence of competing noise. One could use the model to study mismatch negativities to pairs of phonemes and construct a matrix for each patient of which phonemes can be discriminated and which are confused. Preliminary studies have been conducted on four aphasic hearing-impaired patients in Turku, Finland (Aaltonen, O., Tuomainen, J., Niemi, P. and Laine, M. (in press): Discrimination of speech and non-speech sounds by brain-damaged subjects: electrophysiological evidence for distinct perceptual processes. Brain and Language). When the aphasia was due to a posterior lesion, the patient showed no phonemic mismatch negativities but showed normal frequency-change mismatch negativities. If the lesion was in the anterior region, the patient had normal phonemic and speech-mismatch negativities. There is a psychophysical phenomenon that affects the pulsation threshold. If there is an intermittent tone and the gaps are filled with loud noise, as the volume of the noise is increased the tone is perceived as a continuous tone. At the threshold, the onset information about the tone is suppressed (the same is probably true for the offset response), so the tone is no longer perceived as being switched on and off.
ISSN: 0001-6489 (Print) 1651-2251 (Online) Journal homepage: http://www.tandfonline.com/loi/ioto20
Attention Effects on the Auditory Event-related Potential R. Nä;ätänen & W. Teder To cite this article: R. Nä;ätänen & W. Teder (1991) Attention Effects on the Auditory Event-related Potential, Acta Oto-Laryngologica, 111:sup491, 161-167, DOI: 10.3109/00016489109136794 To link to this article: http://dx.doi.org/10.3109/00016489109136794
Published online: 08 Jul 2009.
Submit your article to this journal
Article views: 21
View related articles
Full Terms & Conditions of access and use can be found at http://www.tandfonline.com/action/journalInformation?journalCode=ioto20 Download by: [RMIT University Library]
Date: 25 April 2016, At: 03:15
Acta Otolaryngol (Stockh) 1991; Suppl. 491: 161-167
Attention Effects on the Auditory Event-related Potential R. NUTANEN and W. TEDER From the Department of Psychology, University of Helsinki, Finland
Downloaded by [RMIT University Library] at 03:15 25 April 2016
R. Naatanen, W. Teder. Attention effects on the auditory event-related potential. Acta Otolaryngol (Stockh) 1991; Suppl 491: 161-167. Studies on selective-attention effects on the auditory event-related brain potential (ERP) are reviewed. Brainstem components of the ERP have not been shown to be sensitive to attention. On the other hand, attention effects in the middle-latency range ( 1 2-50 ms from stimulus onset) appear to occur under some conditions but it is not clear whether these effects are exogenous or endogenous. The predominant attention effect on the auditory ERP is the processing negativity, a slow endogenous negativity which often commences well before the exogenous (supratemporal) NI component peaks (at about 100 ms post-stimulus), therefore giving the impression that this exogenous component is attention-sensitive. It is not yet settled, however, whether even these exogenous processes under some conditions might be modulated by selective attention. Key words: selective aiteniion. NI,processing negativity.
INTRODUCTION Event-related potentials (ERP) might give us some indication as to how the brain selects desired sensory information in audition, i.e., what is selective attention and how is processing of sensory input modified by it. ERP findings claimed to indicate auditory stimulus selection can be classified into three categories: 1) very early effects; 2) enhancement of some exogenous component of the N1 wave; 3) the processing negativity (PN).
VERY EARLY EFFECTS OF AUDITORY SELECTIVE ATTENTION A number of studies (1-6) have explored the possibility that selective attention enhances auditory brainstem responses elicited by attended stimuli and/or attenuates these responses to ignored stimuli. The majority of these studies concluded that brainstem responses are not modified by attention. Lukas (3, 4), however, reported that some part of the brainstem response was larger when the subject attended to auditory stimuli than to visual stimuli. There are, however, some serious problems (see 7, 8) in interpreting these data in this way. In conclusion, it appears, in the light of the evidence available, that selective attention does not modulate auditory brainstem responses. Studies on polysynaptic eye-blink reflexes (see 9) suggest, however, that selective attention might modulate quite early phases of auditory information processing (10, 1 1). On the basis of their quite recent results obtained by combining reflex and ERP measurements, Hackley et al. (12) suggested that whereas evoked auditory activity in the lower brainstem is not modified by attention, later activity mediated in the upper brainstem can be attention-modulated. Puel et al. (13), in a recent study on cochlear echo amplitudes for sound stimuli, concluded that the auditory efferent system might be able to selectively modulate the cochlear response to sound according to the direction of attention. These very interesting results demonstrating an attenuation of the sound-emitted echo amplitude in the closed ear canal when a task demanding visual attention is introduced to a resting subject cannot, however, be regarded as providing a conclusive demonstration for selective modulation. It was not tested whether the echo amplitude might also be reduced compared with resting-state levels during an auditory task as it was during a visual task. To this end, their effect might well have been nonspecific, 11-918418
Downloaded by [RMIT University Library] at 03:15 25 April 2016
162 R. Naatanen and W. Teder i.e., caused by increased nonspecific arousal accompanying task performance. This criticism is similar to that directed to the reduction of the cochlear response to clicks observed by HernAndez-Peon et al. (14) when the cat’s attention was elicited by the appearance of an interesting stimulus (mice in a glass jar) in its visual field (15). The earliest ERP effects of selective attention in audition might occur in the middle-latency range (1 2-50 ms from stimulus onset; (16)). McCallum et al. ( 1 7) observed an early attention effect commencing at a latency of 26 ms in their free-field listening situation. (There was a possible effect even at an onset latency of 15 ms, but this needs to be replicated; see 17). Their effect emerged as a slow negative displacement of the ERP to attended stimuli relative to that to unattended stimuli, suggesting an emergence of an endogenous component rather than a modulation of an exogenous (middle-latency) component. On the other hand, the “P20-50” effect on Woldorff et al. (2) might be of either exogenous (then possibly involving, according to the authors, the Pa component) or endogenous nature, as also suggested by the authors themselves. This effect, obtained in selective listening to dichotic stimuli presented with very short interstimulus intervals (ISI), emerged as a positive ERP displacement commencing at about 20 ms post-stimulus and continuing for some 20-30 ms. On the other hand, Linden et al. (18), using a somewhat different paradigm, found no selective-attentional modulation of the middle-latency components. ATTENTIONAL ENHANCEMENT OF SOME EXOGENOUS COMPONENT OF THE AUDITORY N 1 WAVE In their now classic paper from 1973, Hillyard, Hink, Schwent & Picton (19) were the first to demonstrate an attentional enhancement of the N1 wave so that this could not be questioned on methodological grounds (for a review, see 20). The authors interpreted this finding in terms of an enhancement of an exogenous N1 component, i.e., of some exogenous generator process contributing to the N l wave. (For a definition of an ERP component, see 21.) In 1978, an endogenous attention effect termed the processing negativity (PN) was, however, described by Naatanen et al. (22). This protracted negativity commenced after the N1 peak and lasted for several hundreds of milliseconds; therefore an exogenous N 1 process could not, presumably, be involved. The authors further suggested that even Hillyard et al.’s (19) effect might have been caused by a PN rather than an enhancement of an exogenous N1 component. According to them, Hillyard and colleagues’ very fast stimulus rate might have caused PN to commence early enough to overlap the “exogenous N1 component”. A number of further studies (for a review, see 23) showed that PN is the main, perhaps the only, effect of selective attention at the N1 latency range. Meanwhile it had become increasingly clear that there are at least three exogenous components in the N1 wave (for a review, see 21) and, further, that if attention indeed enhances some exogenous N l component, then that probably is, judging from similarities in latency and topography, the supratemporal N 1 component (see 8). Quite recent studies (2, 12) from Hillyard’s laboratory, however, demonstrated an attention effect with a time course which very closely paralleled that of the supratemporal N1 component. These results were obtained under heavy-load dichotic conditions requiring a very strong attentional focus, with the most essential aspect of this design being the use of very short ISIs. Therefore the authors proposed that under such conditions, some exogenous N1 generator process might be modulated by selective attention. Teder et al. (24) wished to demonstrate that the selective-attention effect obtained even with very short ISIs is due to a PN rather than to an enhancement of some exogenous N1 process. These authors compared attention effects with four different IS1 (random, rectangular distribution) conditions: (A) 60-100 ms; (B) 120-200 ms; (C) 360-600 ms; (D) 600-1000 ms.
Attention effects on the auditory event related potential
163
Unattend/attend ERPs, left ear, Cz - unaiiend,
- attend
1%:
Downloaded by [RMIT University Library] at 03:15 25 April 2016
ISI: 600-1000 ms
360-600 ms
1 ISI: 120-200 ms
ISI: 60- 100 rns
Difference waves: attend-unattend (Nd) -4pv
Random ISls: 60-100 ms - 120-200 ms 360.600 ms 600-loo0 ms .....
+4pv
-
Fig. 1. Top: Grand-average vertex (Cz) ERPs to unattended and attended tones for left-ear stimuli from four random-IS1 conditions (60-100 ms, 120-200 ms, 360-600 ms, 600-1 000 ms). S=stimulus onset. Bottom: Superimposition of difference waves obtained by subtracting ERPs to unattended stimuli from those to attended stimuli separately for each IS1 condition shown above.
Standard stimuli (96%) were tones of 300 Hz,deviant stimuli (4%) tones of 330 Hz.The ear of entry was random. The subject’s task was to press a button each time a deviant stimulus (a “target”) appeared within the input stream to a designated ear. Fig. 1 (two top rows) presents grand-average (10 subjects) vertex ERPs for attended and ignored stimuli separately for each IS1 condition. The difference waves (Nd) obtained by subtracting unattend ERPs from the respective attend ERPs are shown in the bottom of the figure. A comparison of the Nds from the two “short-ISI” conditions with those from the two “long-ISI” conditions shows a slight prolongation of the peak of the early Nd phase with IS1 prolongation. This pattern of data, therefore, seems to suggest that the peak latency of the early Nd might, within a certain range, be a rather continuous function of the mean ISI. This supports the interpretation that even with very short ISIs, the ERP attention effect is due to PN rather than to an enhancement of a n exogenous N1 component. Further evidence for this interpretation was provided by the very recent results of Naatanen et al. (25). These authors presented tones of 300 Hz to the subject’s left ear and those of 6000 Hz to the right ear in random order and with ISIs randomly varying from 60 ms to 200 ms. The subject was instructed to count occasional slightly higher tones within a designated input stream.
164 R. Naatanen and W. Teder
Left, 300 Hz
Right, 6000 Hz
CZ
-+1pV
Difference Downloaded by [RMIT University Library] at 03:15 25 April 2016
(Nd)
Fig. 2. Grand-average vertex (Cz)ERPs to attended and unattended tones (foprow) and respective difference waves (attend minus unattend) for left-ear (300 Hz)and right-ear stimuli (6000 Hz). ISI: random 60-200 ms. S=stimulus onset.
Grand-average (9 subjects) vertex data are shown in Fig. 2. The top row of this figure shows that ERPs both to unattended and attended stimuli are much larger for the low than high tones (see 21). On the other hand, Nds for the two tones are very similar. This pattern of data suggests that mechanisms of exogenous N1 generation and those of the attention effect are different for one would expect the attention effect to be proportional t o the strength of the generator response elicited in the a b s e v e of attention. Consequently, it appers that the supratemporal component of the exogenous N1 is not modulated by selective attention. Giard et al. (26), however, have obtained an interesting attention effect which may or may not express an attentional enhancement of some exogenous type of neuronal population on the supratemporal cortex. This effect emerged as a small negativity which preceded the early phase of the typical Nd and showed a pitch-specific distribution. Finally, two recent studies (27,28) suggest that when irrelevant stimuli are visual, attending t o auditory stimuli causes an enhancement of the negative component belonging to the Tcomplex (see 29). PROCESSING NEGATIVITIES Processing negativities (PN) were already illustrated in the afore-going (Figs. 1 and 2). The early, sensory-specific component of the P N was suggested by Naatanen (8, 23) to be generated by an on-line matching process by which the brain rapidly chooses relevant stimuli among irrelevant stimuIi for further processing or response. This matching process occurs, on this hypothesis, between a sensory input and a voluntarily maintained neural representation, “the attentional trace”, where sensory information essential for selecting relevant stimuli among irrelevant stimuli is stored. This theory predicts that even irrelevant stimuli elicit some P N and, further, that this P N is larger and longer, the more similar an irrelevant stimulus is to the relevant. These and some other predictions of the attentional-trace theory were confirmed in a series of studies by Alho et al. (e.g., 30; for a review, see 8). Thus the negative difference wave (Nd) does not reveal the PN but rather the difference between PNs t o relevant and irrelevant stimuli (23, 30). P N also has a later, frontal component (31, see also 20) but its functional significance is still an open question. This component might reflect further processing of stimuli selected in initial
Attention effects on the auditory event related potential 165 attentional-trace selection or rehearsal activity maintaining the attentional trace (23, see also 32). Naatanen & Picton (21) proposed, in line with the latter interpretation, that this component might be generated by a central “executive” mechanism which initiates and controls the selective-attention state, more specifically, the sensory-specific mechanism of stimulus selection, the attentional trace.
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CONCLUDING SUMMARY The earliest selective-attention effects on the auditory ERP are not yet settled. Whereas it is quite clear that brainstem respones are not modulated by attention, effects at the middlelatency range under certain conditions seem to be quite firmly established. On the other hand, it is unclear whether they are of exogenous or endogenous nature although in the light of the available evidence, the latter alternative appears more likely. Puel et al.’s (13) data tentatively suggest that even the cochlear response might be sensitive to selective attention but an alternative interpretation in terms of a nonspecific effect should be ruled out. PN appears to be the predominant, in many conditions even the only, effect of selective attention on auditory ERPs. However, the long controversy involving a possible selectiveattention effect on some exogenous N1 component is not yet settled. Tentatively, it appears that the supratemporal N1 component is insensitive to attention (unless Giard et al.’s ( 2 5 ) effect originate as from an attentionally sensitive subpopulation of neurons generating this component). On the other hand, the negative component of the T-complex (maximal over the temporal sites) might be sensitive to intermodal selective attention.
ACKNOWLEDGEMENTS This study was supported by The Academy of Finland and by The Signe and Ane Gyllenberg Foundation (Helsinki, Finland).
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DISCUSSION
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Participants: Hoke, Naatanen, Schreiner
The model might be used to assess objectively communication disorders in patients whose peripheral auditory functions are normal but who are unable to recognize speech under certain conditions, especially in the presence of competing noise. One could use the model to study mismatch negativities to pairs of phonemes and construct a matrix for each patient of which phonemes can be discriminated and which are confused. Preliminary studies have been conducted on four aphasic hearing-impaired patients in Turku, Finland (Aaltonen, O., Tuomainen, J., Niemi, P. and Laine, M. (in press): Discrimination of speech and non-speech sounds by brain-damaged subjects: electrophysiological evidence for distinct perceptual processes. Brain and Language). When the aphasia was due to a posterior lesion, the patient showed no phonemic mismatch negativities but showed normal frequency-change mismatch negativities. If the lesion was in the anterior region, the patient had normal phonemic and speech-mismatch negativities. There is a psychophysical phenomenon that affects the pulsation threshold. If there is an intermittent tone and the gaps are filled with loud noise, as the volume of the noise is increased the tone is perceived as a continuous tone. At the threshold, the onset information about the tone is suppressed (the same is probably true for the offset response), so the tone is no longer perceived as being switched on and off.
