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Slow potentials preceding vocalisation
271
Biological Psychology 14 ( 1982) 21 I-276 North-Holland Publishing Company
SLOW POTENTIALS
PRECEDING
VOCALISATION
J.A.C. EMPSON Department Accepted
of Psychology, for publication
University of Hull, Hull HlJ6 7RX. U.K. 29 October
1981
Twenty-four subjects equally represented by males and females, and left- and right-handers, had slow potentials recorded prior to vocalisation of the same word 25 times (‘Yes’), or a different word every sweep, chosen by the subject 5. Negativity on the scalp preceding generated words came earlier than preceding repetitions. Asymmetry in EEG was dependent on handedness, and occurred frontally in females, centrally in males. It is suggested that task-related differences in slow potentials preceding speech, and asymmetries associated with handedness, provide evidence that these potentials are not irretrievably contaminated by movement and respiratory artefacts.
1. Introduction It has been established beyond any doubt that slow cortical potentials preceding movement can reliably be recorded from the scalp, and that these bereitschaftspotentials are asymmetrically distributed, depending on which side of the body is making the response (McAdam and Seales, 1969). An early report (McAdam and Whitaker, 1971) of asymmetry in bereitschaftspotentials preceding the spontaneous articulation of polysyllabic words confirmed clinical evidence (e.g., Geshwind, 1970) that linguistic functions in right-handed individuals tend to be subserved by the left hemisphere. Subsequent work has thrown doubt on the reliability of these recordings. For example, studies based on the CNV paradigm have failed to produce any evidence of asymmetry preceding a verbal response (Michalewski and Weinberg, 1977; House and Naitoh, 1979). A possible explanation for this may be that bereitschaftspotentials preceding speech were confounded by the evoked response to the imperative stimulus, as noted by Empson (1979). More important, it seems indisputable that scalp-recorded potentials preceding speech are inevitably contaminated by movement and respiratory artefacts (Szirtes and Vaughan, 1977; Grozinger, Kornhuber, Kribeel and Murata, 1974; Brooker and Donald, 1980). The question that remains seems to be how overwhelming this contamination is, and whether it is worth trying to assess cortical activity using this methodology. As Brooker and Donald (1980) comment, ‘ . . . the correlation of EEG waveforms with myogenic activity is not 0301-05 11/82/0000-0000/$02.75
0 1982 North-Holland
212
J.A.C.
Empson / Slow’ porentiuls
preceding
oocaliscrt~on
itself irrefutable evidence that they are produced by the same [myogenic] event’. It is being argued here that these potentials may be particularly vulnerable to movement artefacts, but that the technical problems are not insuperable. The routine use of confidence intervals around each average, for instance, allows the rejection of averages contaminated by occasional artefacts. It also permits the use of relatively few sweeps since atypical epochs do not have to be averaged out. So far as regularly recurring artefacts are concerned, to take an analogy, excellent correlations have been shown to exist between EEG alpha and orbital and retinal phenomena (Lippold, 1973) which have been shown subsequently to have no causal relation to observed potentials on the scalp (Cavonius and Estevez-Uscanga, 1974). As Brooker and Donald (1980) have pointed out, slow potentials preceding speech may similarly occur at the same time as activity in the pharynx, but not be caused by it. It seems unlikely that myogenic artefacts should be differentially affected by psychological aspects of speech production, or handedness, so it could be argued that any consistent changes associated with these factors, including interactions with hemispheric asymmetry, would support the view that a major component of these scalp potentials reflect cortical processes, rather than the mechanical preparations necessary for vocalisation. 2. Method 2.1. Subjects This experiment involved 24 undergraduate and postgraduate members of the university who volunteered to take part. Handedness was determined by self-report, followed up by a peg-board performance task. There were 12 left-handers and 12 right-handers, equally represented by men and women. 2.2. Recording procedure Silver silver-chloride electrodes were placed left and right centrally, and left and right frontally (at lo-20 system locations C3, C4, F3 and F4), earthed at the vertex, and referenced to linked mastoids. Elema Schonander EEG amplifiers were set to 200 pV/cm amplification, at a time constant of 1.2 set, and with a bandwidth setting of up to 30 Hz. Averaging was performed on-line, using the DEC software package ‘Advanced Averager set of programs on a PDP 8 computer. Triggering was initiated by speech sound, picked up via a Teat four-track tape recorder with a conventional microphone. Sampling was set to start 800 msec before the trigger, at the rate of 1 per 10 msec. Twenty-five epochs were taken from each subject, and confidence limits for each average were inspected before the
digitised average was stored on magnetic tape. If the 95% confidence limits were greater than about 10 pV, on any one of the averages from the four EEG locations, the subject was asked to repeat the task, with special emphasis given to instructions to fixate, not to speak immediately after blinking or moving the eyes, and to keep as still as possible. Every day that recording was taking place the actual gain of the four amplifiers was checked, using a 100 PV square wave impulse averaged on the same settings as the EEG signals, and similarly stored as a calibration file on magnetic tape. Prior to subsequent analysis, every average was standardised to PV metric, with all the points expressed as deviations from the first point averaged. 2.3. Experimental
procedure
The subjects sat in a small, electrically shielded room, facing a small mark on the wall which they were asked to fixate during the experiment. They were instructed very carefully not to speak immediately after any sort of movement, including eye movements and blinks, but to wait a few seconds before resuming. When every preparation was complete, each subject was given his or her final instruction, which was either to say ‘Yes’ repeatedly, with a pause of about 3 set between each vocalisation, or to say a different word every time. The latter group were told to say a word beginning with every letter of the alphabet, and, when they had finished, to start again at the beginning (to allow for trials missed, before E started the average, since no averaging was started until a satisfactorily settled set of EEG traces was emerging on the encephalograph). An event marker indicated vocalisations, and gross artefacts associated with them were therefore easily detected. These invariably resulted in unacceptably wide 95% confidence limits, and the average was taken again. The experiment was therefore a mixed design, with independent factors being sex, handedness and conditions (each subject only performing under one condition) and repeated measures on electrode placement (frontal vs. central and left vs. right). This procedure, using each subject only once, is a departure from the normal practice of making repeated and extended observations on individuals and was designed to minimise the influence of individual variation, which is known to be considerable in speech-related potentials.
3. Results Inferential analysis of the results proceeded by the summing of the subject’s four arrays of 80 data points into four arrays of four data points, being the average of each of four 200 msec blocks preceding vocalisation. Analysis of variance for each block took sex, handedness and conditions (‘Yes’ vs. gener-
214
J.A.C.
Empson / Slow potentials preceding oocaltsution
ated words) as independent repeated measures factors.
factors,
and
frontal-central
and
left-right
as
3.1. Main effects In block 2 (590-400 msec) and block 3 (390-200 msec) potentials preceding ‘Yes’ vocalisations were less negative than those preceding word generation vocalisations (F=4.57, df 1, 16, ~(0.05; F=6.74, dfal, 16, ~(0.05. See fig. 1). In blocks 2, 3 and 4 (590-400 msec, 390-200 msec, and 190 ms-trigger) the two frontal placements showed greater negativity than the two central placements(F=7.16, df 1, 16,p
J.A.C.
Ew~pson / Slow potentruls preceding oocdisution
,
2.5 -
/ 0
,
,
8’
R-N
\\ \1 repetitions
\
,/I //
215
\
\
-
\ \ , \ \ -2.5
-
-5
-
1 , .* 4
I
I
I
I
I
800
600
400
200
0
msec Fig. I. Grand averages preceding the utterance of ‘Yes’ by 12 subjects, words by 12 subjects, all four averages from each subject being summed
Table 1 Average deviation from baseline illustrate higher-order interactions
msec)
Block 4 (- 190 msec - trigger)
novel
for time intervals - 390 - - 200 msec and - 190 - trigger. to of asymmetry with handedness, sex and electrode placement. F3
Block 3 (-390 - -200
and of generated, together.
F4
c3
c4
0.78 -9.21
5.88 -5.69
4.17 -2.77
Male Left-handers Right-handers
0.97 -9.98
Female Left-handers Right-handers
1.16 - 10.07
-0.95 -0.21
3.66 - 1.71
3.82 -3.15
Male Left-handers Right-handers
- 2.50 -11.02
-5.34 - 12.31
4.74 -7.15
0.98 -2.19
Female Left-handers Right-handers
-3.62 - 13.88
-5.73 -2.71
1.20 - 2.32
0.26 -5.36
216
J.A.C.
Empson / Slow potentids
preceding oocdiscrtrot~
any significant asymmetry until block 3, after the development of a significant difference in negativity across the whole scalp in block 2, could be interpreted as evidence that scalp potentials reflecting this lexical search process may not be lateralised, so much as those reflecting processes underlying vocalisation. While, of course, caution should be exercised in making inferences about cortical and linguistic processes from scalp-recorded potentials, it seems that these recordings are not necessarily irretrievably contaminated by extra-cortical activity, and that there are some grounds for encouragement in pursuing this line of research.
References Brooker, B.H. and Donald,
M.W. (1980). Contribution of the speech musculature to apparent human EEG asymmetries prior to vocalization. Brain and Language, 9, 226-245. Cavonius, S.R. and Estevez-Uscanga,‘O. (1974). Local suppression of alpha activity by pattern in half the visual field. Nature, 251, 412-414. Empson, J.A.C. (1979). Psychological significance of the EEG command potential (Bererfschafrspotential): an application of the Donders paradigm, introducing a new method of eliciting Bereitschaftspotentials. Bulletin of British Psychology Society, 32, 19. Geschwind, N. (1970). The organization of language and the brain. Science, 170, 940-944. Grozinger, B., Kornhuber, H.H., Kriebel, J. and Murata, K. (1974). Cerebral potentials during respiration and preceding vocalization. Electroencephalography and Clinical Neurophysiology, 36435-443. House, J.F. and Naitoh, P. (1979). Lateral-frontal slow potential shifts preceding language acts in deaf and hearing adults. Brain and Language, 8, 287-302. Lippold, 0. (1973). The Origin of the Alpha Rhythm. Churchill Livingston: Edinburgh and London. McAdam, D.W. and Seales. D.M. (1969). Bereitschrrfrspotentiul enhancement with increased level of motivation. Electroencephlography and Clinical Neurophysiology, 27, 73-75. McAdam, D.W. and Whitaker, H.A. (1971). Language production: electroencephalographic localization in the normal human brain. Science, 172, 499-502. McGlone, J. (I 980). Sex differences in human brain asymmetry: a critical survey. Behavioral and Brain Sciences, 3, 215-263. Michalewski, H.J. and Weinberg, H. (1977). The CNV and speech production: slow potentials and the area of Broca. Biological Psychology, 9, 83-96. Szirtes, J. and Vaughan, H.G. Jr. (1977). Characteristics of cranial and facial potentials associated with speech production, In: Desmedt, J. (Ed.) Language and Hemispheric Specialisation in Man: Cerebral Event-related Potentials. Karger: Basel, New York, 112-126.
Biological Psychology 14 ( 1982) 21 I-276 North-Holland Publishing Company
SLOW POTENTIALS
PRECEDING
VOCALISATION
J.A.C. EMPSON Department Accepted
of Psychology, for publication
University of Hull, Hull HlJ6 7RX. U.K. 29 October
1981
Twenty-four subjects equally represented by males and females, and left- and right-handers, had slow potentials recorded prior to vocalisation of the same word 25 times (‘Yes’), or a different word every sweep, chosen by the subject 5. Negativity on the scalp preceding generated words came earlier than preceding repetitions. Asymmetry in EEG was dependent on handedness, and occurred frontally in females, centrally in males. It is suggested that task-related differences in slow potentials preceding speech, and asymmetries associated with handedness, provide evidence that these potentials are not irretrievably contaminated by movement and respiratory artefacts.
1. Introduction It has been established beyond any doubt that slow cortical potentials preceding movement can reliably be recorded from the scalp, and that these bereitschaftspotentials are asymmetrically distributed, depending on which side of the body is making the response (McAdam and Seales, 1969). An early report (McAdam and Whitaker, 1971) of asymmetry in bereitschaftspotentials preceding the spontaneous articulation of polysyllabic words confirmed clinical evidence (e.g., Geshwind, 1970) that linguistic functions in right-handed individuals tend to be subserved by the left hemisphere. Subsequent work has thrown doubt on the reliability of these recordings. For example, studies based on the CNV paradigm have failed to produce any evidence of asymmetry preceding a verbal response (Michalewski and Weinberg, 1977; House and Naitoh, 1979). A possible explanation for this may be that bereitschaftspotentials preceding speech were confounded by the evoked response to the imperative stimulus, as noted by Empson (1979). More important, it seems indisputable that scalp-recorded potentials preceding speech are inevitably contaminated by movement and respiratory artefacts (Szirtes and Vaughan, 1977; Grozinger, Kornhuber, Kribeel and Murata, 1974; Brooker and Donald, 1980). The question that remains seems to be how overwhelming this contamination is, and whether it is worth trying to assess cortical activity using this methodology. As Brooker and Donald (1980) comment, ‘ . . . the correlation of EEG waveforms with myogenic activity is not 0301-05 11/82/0000-0000/$02.75
0 1982 North-Holland
212
J.A.C.
Empson / Slow’ porentiuls
preceding
oocaliscrt~on
itself irrefutable evidence that they are produced by the same [myogenic] event’. It is being argued here that these potentials may be particularly vulnerable to movement artefacts, but that the technical problems are not insuperable. The routine use of confidence intervals around each average, for instance, allows the rejection of averages contaminated by occasional artefacts. It also permits the use of relatively few sweeps since atypical epochs do not have to be averaged out. So far as regularly recurring artefacts are concerned, to take an analogy, excellent correlations have been shown to exist between EEG alpha and orbital and retinal phenomena (Lippold, 1973) which have been shown subsequently to have no causal relation to observed potentials on the scalp (Cavonius and Estevez-Uscanga, 1974). As Brooker and Donald (1980) have pointed out, slow potentials preceding speech may similarly occur at the same time as activity in the pharynx, but not be caused by it. It seems unlikely that myogenic artefacts should be differentially affected by psychological aspects of speech production, or handedness, so it could be argued that any consistent changes associated with these factors, including interactions with hemispheric asymmetry, would support the view that a major component of these scalp potentials reflect cortical processes, rather than the mechanical preparations necessary for vocalisation. 2. Method 2.1. Subjects This experiment involved 24 undergraduate and postgraduate members of the university who volunteered to take part. Handedness was determined by self-report, followed up by a peg-board performance task. There were 12 left-handers and 12 right-handers, equally represented by men and women. 2.2. Recording procedure Silver silver-chloride electrodes were placed left and right centrally, and left and right frontally (at lo-20 system locations C3, C4, F3 and F4), earthed at the vertex, and referenced to linked mastoids. Elema Schonander EEG amplifiers were set to 200 pV/cm amplification, at a time constant of 1.2 set, and with a bandwidth setting of up to 30 Hz. Averaging was performed on-line, using the DEC software package ‘Advanced Averager set of programs on a PDP 8 computer. Triggering was initiated by speech sound, picked up via a Teat four-track tape recorder with a conventional microphone. Sampling was set to start 800 msec before the trigger, at the rate of 1 per 10 msec. Twenty-five epochs were taken from each subject, and confidence limits for each average were inspected before the
digitised average was stored on magnetic tape. If the 95% confidence limits were greater than about 10 pV, on any one of the averages from the four EEG locations, the subject was asked to repeat the task, with special emphasis given to instructions to fixate, not to speak immediately after blinking or moving the eyes, and to keep as still as possible. Every day that recording was taking place the actual gain of the four amplifiers was checked, using a 100 PV square wave impulse averaged on the same settings as the EEG signals, and similarly stored as a calibration file on magnetic tape. Prior to subsequent analysis, every average was standardised to PV metric, with all the points expressed as deviations from the first point averaged. 2.3. Experimental
procedure
The subjects sat in a small, electrically shielded room, facing a small mark on the wall which they were asked to fixate during the experiment. They were instructed very carefully not to speak immediately after any sort of movement, including eye movements and blinks, but to wait a few seconds before resuming. When every preparation was complete, each subject was given his or her final instruction, which was either to say ‘Yes’ repeatedly, with a pause of about 3 set between each vocalisation, or to say a different word every time. The latter group were told to say a word beginning with every letter of the alphabet, and, when they had finished, to start again at the beginning (to allow for trials missed, before E started the average, since no averaging was started until a satisfactorily settled set of EEG traces was emerging on the encephalograph). An event marker indicated vocalisations, and gross artefacts associated with them were therefore easily detected. These invariably resulted in unacceptably wide 95% confidence limits, and the average was taken again. The experiment was therefore a mixed design, with independent factors being sex, handedness and conditions (each subject only performing under one condition) and repeated measures on electrode placement (frontal vs. central and left vs. right). This procedure, using each subject only once, is a departure from the normal practice of making repeated and extended observations on individuals and was designed to minimise the influence of individual variation, which is known to be considerable in speech-related potentials.
3. Results Inferential analysis of the results proceeded by the summing of the subject’s four arrays of 80 data points into four arrays of four data points, being the average of each of four 200 msec blocks preceding vocalisation. Analysis of variance for each block took sex, handedness and conditions (‘Yes’ vs. gener-
214
J.A.C.
Empson / Slow potentials preceding oocaltsution
ated words) as independent repeated measures factors.
factors,
and
frontal-central
and
left-right
as
3.1. Main effects In block 2 (590-400 msec) and block 3 (390-200 msec) potentials preceding ‘Yes’ vocalisations were less negative than those preceding word generation vocalisations (F=4.57, df 1, 16, ~(0.05; F=6.74, dfal, 16, ~(0.05. See fig. 1). In blocks 2, 3 and 4 (590-400 msec, 390-200 msec, and 190 ms-trigger) the two frontal placements showed greater negativity than the two central placements(F=7.16, df 1, 16,p
J.A.C.
Ew~pson / Slow potentruls preceding oocdisution
,
2.5 -
/ 0
,
,
8’
R-N
\\ \1 repetitions
\
,/I //
215
\
\
-
\ \ , \ \ -2.5
-
-5
-
1 , .* 4
I
I
I
I
I
800
600
400
200
0
msec Fig. I. Grand averages preceding the utterance of ‘Yes’ by 12 subjects, words by 12 subjects, all four averages from each subject being summed
Table 1 Average deviation from baseline illustrate higher-order interactions
msec)
Block 4 (- 190 msec - trigger)
novel
for time intervals - 390 - - 200 msec and - 190 - trigger. to of asymmetry with handedness, sex and electrode placement. F3
Block 3 (-390 - -200
and of generated, together.
F4
c3
c4
0.78 -9.21
5.88 -5.69
4.17 -2.77
Male Left-handers Right-handers
0.97 -9.98
Female Left-handers Right-handers
1.16 - 10.07
-0.95 -0.21
3.66 - 1.71
3.82 -3.15
Male Left-handers Right-handers
- 2.50 -11.02
-5.34 - 12.31
4.74 -7.15
0.98 -2.19
Female Left-handers Right-handers
-3.62 - 13.88
-5.73 -2.71
1.20 - 2.32
0.26 -5.36
216
J.A.C.
Empson / Slow potentids
preceding oocdiscrtrot~
any significant asymmetry until block 3, after the development of a significant difference in negativity across the whole scalp in block 2, could be interpreted as evidence that scalp potentials reflecting this lexical search process may not be lateralised, so much as those reflecting processes underlying vocalisation. While, of course, caution should be exercised in making inferences about cortical and linguistic processes from scalp-recorded potentials, it seems that these recordings are not necessarily irretrievably contaminated by extra-cortical activity, and that there are some grounds for encouragement in pursuing this line of research.
References Brooker, B.H. and Donald,
M.W. (1980). Contribution of the speech musculature to apparent human EEG asymmetries prior to vocalization. Brain and Language, 9, 226-245. Cavonius, S.R. and Estevez-Uscanga,‘O. (1974). Local suppression of alpha activity by pattern in half the visual field. Nature, 251, 412-414. Empson, J.A.C. (1979). Psychological significance of the EEG command potential (Bererfschafrspotential): an application of the Donders paradigm, introducing a new method of eliciting Bereitschaftspotentials. Bulletin of British Psychology Society, 32, 19. Geschwind, N. (1970). The organization of language and the brain. Science, 170, 940-944. Grozinger, B., Kornhuber, H.H., Kriebel, J. and Murata, K. (1974). Cerebral potentials during respiration and preceding vocalization. Electroencephalography and Clinical Neurophysiology, 36435-443. House, J.F. and Naitoh, P. (1979). Lateral-frontal slow potential shifts preceding language acts in deaf and hearing adults. Brain and Language, 8, 287-302. Lippold, 0. (1973). The Origin of the Alpha Rhythm. Churchill Livingston: Edinburgh and London. McAdam, D.W. and Seales. D.M. (1969). Bereitschrrfrspotentiul enhancement with increased level of motivation. Electroencephlography and Clinical Neurophysiology, 27, 73-75. McAdam, D.W. and Whitaker, H.A. (1971). Language production: electroencephalographic localization in the normal human brain. Science, 172, 499-502. McGlone, J. (I 980). Sex differences in human brain asymmetry: a critical survey. Behavioral and Brain Sciences, 3, 215-263. Michalewski, H.J. and Weinberg, H. (1977). The CNV and speech production: slow potentials and the area of Broca. Biological Psychology, 9, 83-96. Szirtes, J. and Vaughan, H.G. Jr. (1977). Characteristics of cranial and facial potentials associated with speech production, In: Desmedt, J. (Ed.) Language and Hemispheric Specialisation in Man: Cerebral Event-related Potentials. Karger: Basel, New York, 112-126.