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The temporal component of the auditory evoked potential: A reinterpretation
Electroencephalography and clinical Neurophysiology, 1984, 59:67-71 Elsevier Scientific Publishers Ireland, Ltd.
67
T H E T E M P O R A L C O M P O N E N T O F T H E AUDITORY EVOKED POTENTIAL: A REINTERPRETATION FRANCK PERONNET, MARIE-HELENE GIARD, OLIVIER BERTRAND and JACQUES PERNIER
CEMI-INSERM, 16, avenue du Doyen L~pine, 69500 Bron (France) (Accepted for publication: July 8, 1983)
The 'temporal component' of the auditory evoked potentials (AEPs) was introduced by Wolpaw and Penry (1975). These authors started from the observation that the scalp-recorded AEPs cannot be explained by a single, only volume-conducted, component but by at least two. Such an observation is supported by the peak latency differences between different scalp-located AEPs in man (Wood and Wolpaw 1982) and by intracranial recording in the monkey (Arezzo et al. 1975). In order to differentiate two possible components, Wolpaw and Penry (1975) subtracted from the AEPs recorded from the temporal electrode a weighted part of the AEPs recorded at the vertex. It must be emphasized that the result of such a computation is already contained in the starting hypothesis. In fact, subtracting a weighted part of the vertex response from the temporal response is equivalent to saying: a largely diffuse response peaking at the vertex is superimposed on a temporal component peaking in the temporal region. From such a decomposition the only question is: 'Is the topography of these two components in agreement with the possible known sources of the AEPs?' We think there are several obstacles which make it difficult to give a positive answer to this question. The asymmetry of the responses obtained in neurological patients cannot be explained by such a decomposition (Prronnet and Michel 1977). The spatial orientation of the auditory areas in the supratemporal plane, perpendicular to the temporal bone, cannot give a maximum of potential at the temporal level. We report here another decomposition of similar data (AEPs) leading to two components whose topography is consistent with both the neurological AEP find-
ings and with the electrical distribution of potential along the scalp.
Methods
The data are those reported in a previous paper (Prronnet et al. 1974). Briefly they are AEPs recorded on a coronal chain of 13 electrodes referred to the nose (Fig. 1). The stimuli are pure tones (1 kHz, 150 msec duration, 70 dB intensity above threshold). Twenty-six subjects were recorded in 2 sessions of 100 stimuli each, one for the left ear and the other for the fight ear. The EEG is amplified with a 35 Hz low-pass filter and 0.53 Hz ( - 3 dB) high-pass cut-off frequency. The decomposition of the AEPs into two components was based on the following hypotheses: (a) the first component originates in the supratemporal plane simultaneously in both hemispheres; (b) the responses recorded from the mastoid electrodes are assumed to be influenced only by the ipsilateral hemisphere; (c) the first component of the AEP for each electrode is a linear combination of the two mastoid responses. Let m I and m r be the left and right mastoid responses. The first component y,, on the nth electrode from the right, is expressed by the formula: Yn = an
"
mr + al2-n "ml
with n = 0, 1 . . . . . 12 and a 0 = 1; a12 = 0. The other coefficients a n are obtained from the assumption that Y,,~00 (the value of y, at a latency of 100 msec) is equal to the experimental value at the same latency. The reasons for this assumption are explained in more detail in the Discussion. Applying
0168-5597/84/$03.00 © 1984 Elsevier Scientific Publishers Ireland, Ltd.
F. P E R O N N E T
68
ET A L .
:Fig. 1. S u p e r - a v e r a g e d A E P s f r o m 36 n o r m a l h e a r i n g a d u l t subjects, a l o n g a c o r o n a l c h a i n r e f e r r e d to the nose. Stimuli are 70 dB, 1000 H z p u r e tones. Full lines: left e a r A E P s . D o t t e d lines: r i g h t e a r A E P s . C a l i b r a t i o n : 5/~V, 100 msec.
this assumption to equation 1, we obtain: Yn,lO0 ~ a n " m r , 1 0 0 + a l 2 - n Y l 2 - n . 1 0 0 ~--- a l 2 - n
" ml,10o
" m r , l O O q" a n " m l . 1 0 o
Hence: Yn,100 " m r , 1 0 0 - - Y 1 2 - n,100 " m l , 1 0 o a n =
m2
r,100
_ m2 1,1o0
(d) The second component is obtained by subtracting the first component from the experimental AEPs.
Results
The first component of the super-averaged AEPs is shown in Fig. 2. The shape of this potential
distribution is roughly similar to the experimental distribution. It may be pointed out that the positive P200 is less important, particularly at the vertex. We also notice a very small signal amplitude in the temporal region. The polarity reversals of the evoked response components allow the active loci in the supratemporal plane to be identified. The second component shown in Fig. 2, is an N120-P220 complex. The N120 peak is maximum over the contralateral hemisphere between the temporal and the central electrodes. This peak is predominant for the left ear responses. This result is consistent with the existence of another source located in the precentral motor cortex, and is in accordance with the observations of Arezzo et al. (1975) in rhesus monkeys.
69
T E M P O R A L C O M P O N E N T OF AEP
N12o
"[4 I
C~ I
Cz I
C3 I
T3 I
P22O Fig. 2. Top: first component of the super-averaged AEPs. This component is obtained from a linear combination of the right and left mastoid responses (see text for details). Bottom: second component of the super-averaged AEPs. This component is obtained by subtracting the first component from the experimental AEPs (Fig. 1). The coronal distributions of the amplitudes of the peaks N120 and P220 are plotted in the middle of the figure at the bottom. Full lines: left ear responses. Superposed dotted lines: right ear responses. Calibration: 5/~V, 100 msec.
70
Discussion The results presented here show a decomposition of the AEPs into two components. This decomposition is obtained by means of a mathematical device whose arbitrary character we pointed out in our introduction. There are indeed innumerable ways of implementing such a decomposition. In order to select one, we must start from hypotheses enabling us to reach a single solution. The hypotheses we adopted are based on the following postulate: the electrical orientation of the primary auditory areas, located in the supratemporal plane, accounts, if not for the total amplitude of the AEPs, at least for the greater part of it. We therefore looked for a way of extracting from experimentally obtained AEPs a component which could be rigorously explained, from a purely electrical point of view, by our hypothesis. The values Yn of the first component at 100 msec were chosen equal to the experimental values in order to calculate the coefficients an, because the polarity reversal of the evoked responses is most apparent at this latency. This methodology results in the following fact: the first component (Fig. 2, top) very closely resembles the experimental results (Fig. 1), to the extent that close attention is required in order to distinguish between them. We should not forget that this interpretation of the AEP topography, put forward in 1970 by Vaughan and Ritter, rests on simple common sense: the primary cortical areas play a preponderant role in their electrogenesis, as is incontestably the case for the visual and somatosensory modalities. The results we show here support this interpretation. However, the most decisive argument in our view remains the fact that in unilateral lesions of the primary auditory areas, a unilateral inversion of the AEPs is observed (Michel et al. 1976; P6ronnet and Michel 1977). Such a finding discredits the explanation (Kooi et al. 1971) whereby an inversion of potential is due to a wrong choice of the reference electrode, the nose. Moreover, no objection has ever been brought against this argument.
Summary The auditory evoked potentials in man cannot be explained by a single source even though a
F. P E R O N N E T ET AL.
strong influence of the primary areas in the supratemporal plane has been pointed out in different works. In 26 normal adults we mathematically extracted the greater part of the experimental AEPs explicable by such an origin. The residual part obtained by subtracting this first component from the experimental data is in agreement with an origin in the precentral motor cortex.
R6sum6
La composante temporelle du potentiel 6voqu6 auditif" une r6interpr6tation Les potentiels 6voqu6s auditifs chez l'homme ne peuvent s'expliquer par une source unique bien que diff6rents travaux mettent en 6vidence l'influence pr6pond6rante des aires auditives primaires dans le plan supratemporal. Nous avons extrait par un artifice math6matique la plus grande partie des donn6es exp6rimentales explicables par cette origine. La partie r6siduelle obtenue en soustrayant cette premi6re composante des donn6es exp6rimentales est en accord avec une origine dans le cortex moteur pr6central.
References Arezzo, J., Pickoff, A. and Vaughan, H.G. The sources and intracerebral distribution of auditory evoked potentials in the alert rhesus monkey. Brain Res., 1975, 90: 57-73. Kooi, K.A., Tipton, A.C. and Marshall, R.E. Polarities and field configuration of the vertex component of the h u m a n auditory evoked response: a reinterpretation. Electroenceph. clin. Neurophysiol., 1971, 31: 166-169. Michel, F., P6ronnet, F. et Schott, B. A p r o p o s d'un cas de surdit6 de l'h6misph6re gauche (h6mianacousie droite). Rev. E.E.G. Neurophysiol., 1976, 6: 175-178. P6ronnet, F. and Michel, F. The asymmetry of the auditory evoked potentials in normal m a n and in patients with brain lesions. In: J.E. Desmedt (Ed.), Auditory Evoked Potentials in Man, Psychopharmacology Correlates of EPs. Karger, Basel, 1977: 130-141. P6ronnet, F., Michel, F., Echallier, J.F. and Girod, J. Coronal topography of h u m a n auditory evoked responses. Electroenceph, clin. Neurophysiol., 1974, 37: 225-230. Vaughan, H.G. and Ritter, W. The sources of auditory evoked responses recorded from the h u m a n scalp. Electroenceph. clin. Neurophysiol., 1970, 28: 360-367.
TEMPORAL COMPONENT OF AEP Wolpaw, J.R. and Penry, J.K. A temporal component of the auditory evoked response. Electroenceph. clin. Neurophysiol., 1975, 39: 609-620. Wood, C.C. and Wolpaw, J.R. Scalp distribution of human
71 auditory evoked potentials. I1. Evidence for overlapping sources and involvement of auditory cortex. Electroenceph. clin. Neurophysiol., 1982, 54: 25-38.
67
T H E T E M P O R A L C O M P O N E N T O F T H E AUDITORY EVOKED POTENTIAL: A REINTERPRETATION FRANCK PERONNET, MARIE-HELENE GIARD, OLIVIER BERTRAND and JACQUES PERNIER
CEMI-INSERM, 16, avenue du Doyen L~pine, 69500 Bron (France) (Accepted for publication: July 8, 1983)
The 'temporal component' of the auditory evoked potentials (AEPs) was introduced by Wolpaw and Penry (1975). These authors started from the observation that the scalp-recorded AEPs cannot be explained by a single, only volume-conducted, component but by at least two. Such an observation is supported by the peak latency differences between different scalp-located AEPs in man (Wood and Wolpaw 1982) and by intracranial recording in the monkey (Arezzo et al. 1975). In order to differentiate two possible components, Wolpaw and Penry (1975) subtracted from the AEPs recorded from the temporal electrode a weighted part of the AEPs recorded at the vertex. It must be emphasized that the result of such a computation is already contained in the starting hypothesis. In fact, subtracting a weighted part of the vertex response from the temporal response is equivalent to saying: a largely diffuse response peaking at the vertex is superimposed on a temporal component peaking in the temporal region. From such a decomposition the only question is: 'Is the topography of these two components in agreement with the possible known sources of the AEPs?' We think there are several obstacles which make it difficult to give a positive answer to this question. The asymmetry of the responses obtained in neurological patients cannot be explained by such a decomposition (Prronnet and Michel 1977). The spatial orientation of the auditory areas in the supratemporal plane, perpendicular to the temporal bone, cannot give a maximum of potential at the temporal level. We report here another decomposition of similar data (AEPs) leading to two components whose topography is consistent with both the neurological AEP find-
ings and with the electrical distribution of potential along the scalp.
Methods
The data are those reported in a previous paper (Prronnet et al. 1974). Briefly they are AEPs recorded on a coronal chain of 13 electrodes referred to the nose (Fig. 1). The stimuli are pure tones (1 kHz, 150 msec duration, 70 dB intensity above threshold). Twenty-six subjects were recorded in 2 sessions of 100 stimuli each, one for the left ear and the other for the fight ear. The EEG is amplified with a 35 Hz low-pass filter and 0.53 Hz ( - 3 dB) high-pass cut-off frequency. The decomposition of the AEPs into two components was based on the following hypotheses: (a) the first component originates in the supratemporal plane simultaneously in both hemispheres; (b) the responses recorded from the mastoid electrodes are assumed to be influenced only by the ipsilateral hemisphere; (c) the first component of the AEP for each electrode is a linear combination of the two mastoid responses. Let m I and m r be the left and right mastoid responses. The first component y,, on the nth electrode from the right, is expressed by the formula: Yn = an
"
mr + al2-n "ml
with n = 0, 1 . . . . . 12 and a 0 = 1; a12 = 0. The other coefficients a n are obtained from the assumption that Y,,~00 (the value of y, at a latency of 100 msec) is equal to the experimental value at the same latency. The reasons for this assumption are explained in more detail in the Discussion. Applying
0168-5597/84/$03.00 © 1984 Elsevier Scientific Publishers Ireland, Ltd.
F. P E R O N N E T
68
ET A L .
:Fig. 1. S u p e r - a v e r a g e d A E P s f r o m 36 n o r m a l h e a r i n g a d u l t subjects, a l o n g a c o r o n a l c h a i n r e f e r r e d to the nose. Stimuli are 70 dB, 1000 H z p u r e tones. Full lines: left e a r A E P s . D o t t e d lines: r i g h t e a r A E P s . C a l i b r a t i o n : 5/~V, 100 msec.
this assumption to equation 1, we obtain: Yn,lO0 ~ a n " m r , 1 0 0 + a l 2 - n Y l 2 - n . 1 0 0 ~--- a l 2 - n
" ml,10o
" m r , l O O q" a n " m l . 1 0 o
Hence: Yn,100 " m r , 1 0 0 - - Y 1 2 - n,100 " m l , 1 0 o a n =
m2
r,100
_ m2 1,1o0
(d) The second component is obtained by subtracting the first component from the experimental AEPs.
Results
The first component of the super-averaged AEPs is shown in Fig. 2. The shape of this potential
distribution is roughly similar to the experimental distribution. It may be pointed out that the positive P200 is less important, particularly at the vertex. We also notice a very small signal amplitude in the temporal region. The polarity reversals of the evoked response components allow the active loci in the supratemporal plane to be identified. The second component shown in Fig. 2, is an N120-P220 complex. The N120 peak is maximum over the contralateral hemisphere between the temporal and the central electrodes. This peak is predominant for the left ear responses. This result is consistent with the existence of another source located in the precentral motor cortex, and is in accordance with the observations of Arezzo et al. (1975) in rhesus monkeys.
69
T E M P O R A L C O M P O N E N T OF AEP
N12o
"[4 I
C~ I
Cz I
C3 I
T3 I
P22O Fig. 2. Top: first component of the super-averaged AEPs. This component is obtained from a linear combination of the right and left mastoid responses (see text for details). Bottom: second component of the super-averaged AEPs. This component is obtained by subtracting the first component from the experimental AEPs (Fig. 1). The coronal distributions of the amplitudes of the peaks N120 and P220 are plotted in the middle of the figure at the bottom. Full lines: left ear responses. Superposed dotted lines: right ear responses. Calibration: 5/~V, 100 msec.
70
Discussion The results presented here show a decomposition of the AEPs into two components. This decomposition is obtained by means of a mathematical device whose arbitrary character we pointed out in our introduction. There are indeed innumerable ways of implementing such a decomposition. In order to select one, we must start from hypotheses enabling us to reach a single solution. The hypotheses we adopted are based on the following postulate: the electrical orientation of the primary auditory areas, located in the supratemporal plane, accounts, if not for the total amplitude of the AEPs, at least for the greater part of it. We therefore looked for a way of extracting from experimentally obtained AEPs a component which could be rigorously explained, from a purely electrical point of view, by our hypothesis. The values Yn of the first component at 100 msec were chosen equal to the experimental values in order to calculate the coefficients an, because the polarity reversal of the evoked responses is most apparent at this latency. This methodology results in the following fact: the first component (Fig. 2, top) very closely resembles the experimental results (Fig. 1), to the extent that close attention is required in order to distinguish between them. We should not forget that this interpretation of the AEP topography, put forward in 1970 by Vaughan and Ritter, rests on simple common sense: the primary cortical areas play a preponderant role in their electrogenesis, as is incontestably the case for the visual and somatosensory modalities. The results we show here support this interpretation. However, the most decisive argument in our view remains the fact that in unilateral lesions of the primary auditory areas, a unilateral inversion of the AEPs is observed (Michel et al. 1976; P6ronnet and Michel 1977). Such a finding discredits the explanation (Kooi et al. 1971) whereby an inversion of potential is due to a wrong choice of the reference electrode, the nose. Moreover, no objection has ever been brought against this argument.
Summary The auditory evoked potentials in man cannot be explained by a single source even though a
F. P E R O N N E T ET AL.
strong influence of the primary areas in the supratemporal plane has been pointed out in different works. In 26 normal adults we mathematically extracted the greater part of the experimental AEPs explicable by such an origin. The residual part obtained by subtracting this first component from the experimental data is in agreement with an origin in the precentral motor cortex.
R6sum6
La composante temporelle du potentiel 6voqu6 auditif" une r6interpr6tation Les potentiels 6voqu6s auditifs chez l'homme ne peuvent s'expliquer par une source unique bien que diff6rents travaux mettent en 6vidence l'influence pr6pond6rante des aires auditives primaires dans le plan supratemporal. Nous avons extrait par un artifice math6matique la plus grande partie des donn6es exp6rimentales explicables par cette origine. La partie r6siduelle obtenue en soustrayant cette premi6re composante des donn6es exp6rimentales est en accord avec une origine dans le cortex moteur pr6central.
References Arezzo, J., Pickoff, A. and Vaughan, H.G. The sources and intracerebral distribution of auditory evoked potentials in the alert rhesus monkey. Brain Res., 1975, 90: 57-73. Kooi, K.A., Tipton, A.C. and Marshall, R.E. Polarities and field configuration of the vertex component of the h u m a n auditory evoked response: a reinterpretation. Electroenceph. clin. Neurophysiol., 1971, 31: 166-169. Michel, F., P6ronnet, F. et Schott, B. A p r o p o s d'un cas de surdit6 de l'h6misph6re gauche (h6mianacousie droite). Rev. E.E.G. Neurophysiol., 1976, 6: 175-178. P6ronnet, F. and Michel, F. The asymmetry of the auditory evoked potentials in normal m a n and in patients with brain lesions. In: J.E. Desmedt (Ed.), Auditory Evoked Potentials in Man, Psychopharmacology Correlates of EPs. Karger, Basel, 1977: 130-141. P6ronnet, F., Michel, F., Echallier, J.F. and Girod, J. Coronal topography of h u m a n auditory evoked responses. Electroenceph, clin. Neurophysiol., 1974, 37: 225-230. Vaughan, H.G. and Ritter, W. The sources of auditory evoked responses recorded from the h u m a n scalp. Electroenceph. clin. Neurophysiol., 1970, 28: 360-367.
TEMPORAL COMPONENT OF AEP Wolpaw, J.R. and Penry, J.K. A temporal component of the auditory evoked response. Electroenceph. clin. Neurophysiol., 1975, 39: 609-620. Wood, C.C. and Wolpaw, J.R. Scalp distribution of human
71 auditory evoked potentials. I1. Evidence for overlapping sources and involvement of auditory cortex. Electroenceph. clin. Neurophysiol., 1982, 54: 25-38.