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Quantification of spindles in comatose patients
ElectrOencephalography and clinical Neurophysiologv, 1983, 56:114-116
114
ElseVier Scientific Publishers Ireland, Ltd.
Short communication Q U A N T I F I C A T I O N OF S P I N D L E S IN C O M A T O S E P A T I E N T S t G. P F U R T S C H E L L E R
,.2
G. S C H W A R Z **, B. P F U R T S C H E L L E R ** and W. LIST **
* Department of Computing Institute of Biomedical Engineering Technical University of Graz, .4-8010 Graz, and ** Institute of Anaesthesiology, University of Graz, A-8036 Graz (Austria) (Accepted for publication: April 6, 1983)
The spindles which are produced in reaction to external stimuli are of great importance to characterize the depth of a coma (Arfel 1975; Rumpl 1979). The spindle activity can be within the alpha hand or even higher (e.g., 14 c/see). Spindles are always a sign of favourable prognosis; no reactivity to external stimuli is seen in patients in the full stage of the apallic syndrome and is therefore an unfavourable sign. Using follow-up measurements in one comatose patient it is demonstrated that spindles are bursts of rhythmic activity within the alpha (beta) band and therefore considered as a type of negative 'event-related desynchronization' (ERD). The positive E R D is an event-related attenuation or blocking of rhythmic activity within the alpha (beta) band and observable after visual and somatosensory stimulation but also before a voluntary, self-paced hand movement (Pfurtscheiler and Aranibar 1979; Pfurtscheller 1981).
I
"!BLOCKING
0
3
~sec
Method I
Changes of rhythmic activity within the alpha or beta frequency band can be quantified by a method introduced by Pfurtscbelter and Aranibar (1979, 1980) and Pfurtschelter (1981). The result of the analysis is a power-versus-time diagram showing the distribution of average alpha or beta power over a 6 sec epoch, 3 sec before and 3 sec after stimulation. The stimulus used was a 1 sec light pulse presented 60 times at intervals of 10 sec. The EEG ( T = 0.1 sec, f = 30 Hz) was recorded from O i-O2. Stimulus-related 6 sec trials were sampled at 64 Hz, averaged and the VEP measured. Thereafter. the same trials were used for the calculation of the E R D within the 6 - 1 4 Hz band. The power in the first 2 sec of each 6 sec trial was assumed to be 100% (reference period) and the increase or decrease of alpha or beta power during the 1 so: interval of stimulation was determined as a percentage. Increase of power indicates a negative E R D (spindles) (Fig. 1), decrease a positive
f
O I Supported by the ' F o n d s zur FOrderun 8 der wissenschaftlichen Forsehung', Project 4109, the Styrian Research Fonds, and the 'Osterr, Nationalbank', Project 1915. 2 Address for correspondence: Prof. Dr. G. Pfurtscheller, Inst. f. Elektro- und Biomed. Technik der Techniscben Universit~t Graz, Inffeldgasse 18, A-8010 Graz, Austria.
3
Fig. 1. Example of raw EEG data during stimulation and the power vs. time diagram displaying the average power within the alpha band over an epoch of 6 sec. Alpha power before stimulation is assumed to be 100%, alpha spindles are indicated by an increase of alpha power (neg. ERD), alpha blocking by a decrease (pos. ERD).
0013-4649/83/$03.00 © 1983 Elsevier Scientific Publishers Ireland, Ltd.
115
QUANTIFICATION OF SPINDLES IN COMATOSE PATIENTS
p_.....
ERDv~ 40
,/
.......
~'~RD
t:
v
0 Spindling
-40
VEP [10 SNR
Hol, Brainstem Haemorrhage
-80 ~11~] Coma Scale
0
4
8 weeks
Fig. 2. Glasgow Coma Scale, ERD and VEP in a patient with a brain stem lesion. ERD is given in per cent, negative ERD marks alpha spindles, positive ERD alpha blocking. For the quantification of the VEP the signal-to-noise ratio (SNR) is used: quotient maximal peak-to-peak amplitude 0-0.5 sec after stimulation/standard deviation calculated in the reference interval.
ERD. Further details about the processing of data, including the statistical treatment, are reported elsewhere (Pfurtscheller and Aranibar 1980).
Results In a comatose patient with a localized haemorrhage in the mesencephalic-pontine region of the brain stem (HOL, 20a) serial EEG measurements were performed. The Glasgow Coma Scale (GCS), visual evoked potential (VEP) (measured by signal-to-noise ratio) and ERD were determined in different comatose states and after complete clinical recovery (Fig. 2). In the first measurement in deep coma (GCS = 4), a relatively normal amplitude VEP, a very small amplitude somatosensory evoked potential (SEP) and a negative ERD of 65~ were found. The latter was highly significant, indicating spindling activity. In parallel with the clinical improvement, the spindles became smaller and alpha blocking (positive ERD) occurred. It is of interest that, after complete recovery, the VEP was about the same size and form compared with the VEP during deep coma, but the other reaction to visual afferences, the ERD, was clearly different in the stages of unconsciousness and consciousness.
specific pathway via the lateral geniculate body to the visual cortex was not disturbed. At the same time the somatosensory evoked potential was abolished. Besides the VEP, the alpha spindles and alpha blocking are provoked by the same visual afferents but transmitted by a different system and controlled by reticular influences. The alpha blocking implies a blockade of inhibitory intrathalamic influences (Andersen and Andersson 1968); such a mechanism has been called disinhibition (Schlag 1974). Disinhibitory impulses could reach the thalamic interneurones via specific visual afferents or via an unspecific path, e.g., from the mesencephalic reticular formation (Singer and Drager 1972). We could assume that the liaemorrhage in the mesencephalic-pontine segment was affecting the unspecific afferents from the reticular formation, resulting in the generation of spindle activity. The example demonstrates very clearly the importance of parallel VEP and ERD measurements in comatose patients and the different prognostic information in the two parameters, although they are provoked by the same exogenous stimulus. Additional information about the neuronal systems is available when vibratory stimuli are used also and SEP and ERD are measured over the sensorimotor cortex.
Summary Quantification of spindles in comatose patients is easily possible by measurement of ERD (event-related desynchronization). ERD can either be positive (e.g., alpha blocking or alpha attenuation) or negative (spindle activity within the alpha band) or can be missing. Follow-up measurements in a comatose patient demonstrate the different time courses of VEP (visual evoked potential) and ERD during clinical recovery. That means that VEP and ERD are generated by different neuronal systems as reactions to the same external stimulus.
Rtsum6
Quantification des fuseaux chez des patients comateux La quantification des fuseaux chez les patients comateux est aistment faisable en mesurant la dtsynchronisation lite /t rtvtnement (ERD). Celle-ci peut-i~tre soit positive (bloquage ou atttnuation de ralpha), soit ntgative (activit6 de type fuseau dans la bande alpha), soit nulle. En suivant l'tvolution d'un patient comateux on peut noter la difftrence des dtcours entre le potentiel 6voqu6 visuel (PEV) et rERD pendant la restauration clinique. Autrement dit, le PEV et I'ERD sont lits /~ la rtaction de deux systtmes neuronaux difftrents, /~ un m6me stimulus externe.
References Discussion The preservation of the VEP in the comatose patient indicates a primary brain stem lesion (Cant 1980) because the
Andersen, P. and Andersson, S.A. Physiological Basis of the Alpha Rhythm. Appleton-Century-Crofts,New York, 1968: 235 pp.
116 Arfel, G. Introduction to cfinical and EEG studies in coma. In: A. R6mond (Ed.), Clinical EEG. II. Handbook of Electroencephalography and clinical Neurophysiology, Vol. 12. Elsevier, Amsterdam, 1975: 5-23. Cant, B.R. Somatosensory and auditory evoked potentials in patients with disorders of consciousness. In: J.E. Desmedt (Ed.), Clinical Uses of Cerebral, Brainstem and Spinal Somatosensory Evoked Potentials. Prog. clin. Neurophysiol., Vol. 7. Karger, Basel, 1980: 282-291. Pfurtscheller, G. Central beta rhythm during sensorimotor activities in man. Electroenceph. clin. Neurophysiol., 1981, 51 : 253-264. Pfurtscheller, G. and Aranibar, A. Evaluation of event-related desynchronization (ERD) preceding and following selfpaced movement. Electroeneeph. olin. Neurophysiol., 1979, 46: t38-146.
G. PFURTSCHELLER ET AL. Pfurtscheller. G. and Aranibar. A. Voluntary movement ERD: normative studies. In: G. Pfurtscheller, P. Buser. F.H. Lopes da Silva and H. Petsche (Eds.), Rhythmic EEG Activities and Cortical Functioning. Elsevier, Amsterdam. 1980: 151-177. Rumpl, E. Elektro-neurologische Korrelationen in den frtihen Phasen des posttranmatisehen Komas. Z.EEG-EMG. 1979. 10: 148-157. Schlag, J. Reticular influences on thalamo-cortical activity. In: O. Creutzfeldt (Ed.), The Neuronal Generation of the EEG. Handbook of Electroeneephalography and olin. Neurophysiology, Vol. 2C. Elsevier. Amsterdam. 1974: 119-134. Singer, W. and Driiger, U. Postsynaptic potentials in relay neurons of cat lateral geniculate nucleus after stimulation of the mesencephafic reticular formation. Brain Res.. 1972. 41: 214-220.
114
ElseVier Scientific Publishers Ireland, Ltd.
Short communication Q U A N T I F I C A T I O N OF S P I N D L E S IN C O M A T O S E P A T I E N T S t G. P F U R T S C H E L L E R
,.2
G. S C H W A R Z **, B. P F U R T S C H E L L E R ** and W. LIST **
* Department of Computing Institute of Biomedical Engineering Technical University of Graz, .4-8010 Graz, and ** Institute of Anaesthesiology, University of Graz, A-8036 Graz (Austria) (Accepted for publication: April 6, 1983)
The spindles which are produced in reaction to external stimuli are of great importance to characterize the depth of a coma (Arfel 1975; Rumpl 1979). The spindle activity can be within the alpha hand or even higher (e.g., 14 c/see). Spindles are always a sign of favourable prognosis; no reactivity to external stimuli is seen in patients in the full stage of the apallic syndrome and is therefore an unfavourable sign. Using follow-up measurements in one comatose patient it is demonstrated that spindles are bursts of rhythmic activity within the alpha (beta) band and therefore considered as a type of negative 'event-related desynchronization' (ERD). The positive E R D is an event-related attenuation or blocking of rhythmic activity within the alpha (beta) band and observable after visual and somatosensory stimulation but also before a voluntary, self-paced hand movement (Pfurtscheiler and Aranibar 1979; Pfurtscheller 1981).
I
"!BLOCKING
0
3
~sec
Method I
Changes of rhythmic activity within the alpha or beta frequency band can be quantified by a method introduced by Pfurtscbelter and Aranibar (1979, 1980) and Pfurtschelter (1981). The result of the analysis is a power-versus-time diagram showing the distribution of average alpha or beta power over a 6 sec epoch, 3 sec before and 3 sec after stimulation. The stimulus used was a 1 sec light pulse presented 60 times at intervals of 10 sec. The EEG ( T = 0.1 sec, f = 30 Hz) was recorded from O i-O2. Stimulus-related 6 sec trials were sampled at 64 Hz, averaged and the VEP measured. Thereafter. the same trials were used for the calculation of the E R D within the 6 - 1 4 Hz band. The power in the first 2 sec of each 6 sec trial was assumed to be 100% (reference period) and the increase or decrease of alpha or beta power during the 1 so: interval of stimulation was determined as a percentage. Increase of power indicates a negative E R D (spindles) (Fig. 1), decrease a positive
f
O I Supported by the ' F o n d s zur FOrderun 8 der wissenschaftlichen Forsehung', Project 4109, the Styrian Research Fonds, and the 'Osterr, Nationalbank', Project 1915. 2 Address for correspondence: Prof. Dr. G. Pfurtscheller, Inst. f. Elektro- und Biomed. Technik der Techniscben Universit~t Graz, Inffeldgasse 18, A-8010 Graz, Austria.
3
Fig. 1. Example of raw EEG data during stimulation and the power vs. time diagram displaying the average power within the alpha band over an epoch of 6 sec. Alpha power before stimulation is assumed to be 100%, alpha spindles are indicated by an increase of alpha power (neg. ERD), alpha blocking by a decrease (pos. ERD).
0013-4649/83/$03.00 © 1983 Elsevier Scientific Publishers Ireland, Ltd.
115
QUANTIFICATION OF SPINDLES IN COMATOSE PATIENTS
p_.....
ERDv~ 40
,/
.......
~'~RD
t:
v
0 Spindling
-40
VEP [10 SNR
Hol, Brainstem Haemorrhage
-80 ~11~] Coma Scale
0
4
8 weeks
Fig. 2. Glasgow Coma Scale, ERD and VEP in a patient with a brain stem lesion. ERD is given in per cent, negative ERD marks alpha spindles, positive ERD alpha blocking. For the quantification of the VEP the signal-to-noise ratio (SNR) is used: quotient maximal peak-to-peak amplitude 0-0.5 sec after stimulation/standard deviation calculated in the reference interval.
ERD. Further details about the processing of data, including the statistical treatment, are reported elsewhere (Pfurtscheller and Aranibar 1980).
Results In a comatose patient with a localized haemorrhage in the mesencephalic-pontine region of the brain stem (HOL, 20a) serial EEG measurements were performed. The Glasgow Coma Scale (GCS), visual evoked potential (VEP) (measured by signal-to-noise ratio) and ERD were determined in different comatose states and after complete clinical recovery (Fig. 2). In the first measurement in deep coma (GCS = 4), a relatively normal amplitude VEP, a very small amplitude somatosensory evoked potential (SEP) and a negative ERD of 65~ were found. The latter was highly significant, indicating spindling activity. In parallel with the clinical improvement, the spindles became smaller and alpha blocking (positive ERD) occurred. It is of interest that, after complete recovery, the VEP was about the same size and form compared with the VEP during deep coma, but the other reaction to visual afferences, the ERD, was clearly different in the stages of unconsciousness and consciousness.
specific pathway via the lateral geniculate body to the visual cortex was not disturbed. At the same time the somatosensory evoked potential was abolished. Besides the VEP, the alpha spindles and alpha blocking are provoked by the same visual afferents but transmitted by a different system and controlled by reticular influences. The alpha blocking implies a blockade of inhibitory intrathalamic influences (Andersen and Andersson 1968); such a mechanism has been called disinhibition (Schlag 1974). Disinhibitory impulses could reach the thalamic interneurones via specific visual afferents or via an unspecific path, e.g., from the mesencephalic reticular formation (Singer and Drager 1972). We could assume that the liaemorrhage in the mesencephalic-pontine segment was affecting the unspecific afferents from the reticular formation, resulting in the generation of spindle activity. The example demonstrates very clearly the importance of parallel VEP and ERD measurements in comatose patients and the different prognostic information in the two parameters, although they are provoked by the same exogenous stimulus. Additional information about the neuronal systems is available when vibratory stimuli are used also and SEP and ERD are measured over the sensorimotor cortex.
Summary Quantification of spindles in comatose patients is easily possible by measurement of ERD (event-related desynchronization). ERD can either be positive (e.g., alpha blocking or alpha attenuation) or negative (spindle activity within the alpha band) or can be missing. Follow-up measurements in a comatose patient demonstrate the different time courses of VEP (visual evoked potential) and ERD during clinical recovery. That means that VEP and ERD are generated by different neuronal systems as reactions to the same external stimulus.
Rtsum6
Quantification des fuseaux chez des patients comateux La quantification des fuseaux chez les patients comateux est aistment faisable en mesurant la dtsynchronisation lite /t rtvtnement (ERD). Celle-ci peut-i~tre soit positive (bloquage ou atttnuation de ralpha), soit ntgative (activit6 de type fuseau dans la bande alpha), soit nulle. En suivant l'tvolution d'un patient comateux on peut noter la difftrence des dtcours entre le potentiel 6voqu6 visuel (PEV) et rERD pendant la restauration clinique. Autrement dit, le PEV et I'ERD sont lits /~ la rtaction de deux systtmes neuronaux difftrents, /~ un m6me stimulus externe.
References Discussion The preservation of the VEP in the comatose patient indicates a primary brain stem lesion (Cant 1980) because the
Andersen, P. and Andersson, S.A. Physiological Basis of the Alpha Rhythm. Appleton-Century-Crofts,New York, 1968: 235 pp.
116 Arfel, G. Introduction to cfinical and EEG studies in coma. In: A. R6mond (Ed.), Clinical EEG. II. Handbook of Electroencephalography and clinical Neurophysiology, Vol. 12. Elsevier, Amsterdam, 1975: 5-23. Cant, B.R. Somatosensory and auditory evoked potentials in patients with disorders of consciousness. In: J.E. Desmedt (Ed.), Clinical Uses of Cerebral, Brainstem and Spinal Somatosensory Evoked Potentials. Prog. clin. Neurophysiol., Vol. 7. Karger, Basel, 1980: 282-291. Pfurtscheller, G. Central beta rhythm during sensorimotor activities in man. Electroenceph. clin. Neurophysiol., 1981, 51 : 253-264. Pfurtscheller, G. and Aranibar, A. Evaluation of event-related desynchronization (ERD) preceding and following selfpaced movement. Electroeneeph. olin. Neurophysiol., 1979, 46: t38-146.
G. PFURTSCHELLER ET AL. Pfurtscheller. G. and Aranibar. A. Voluntary movement ERD: normative studies. In: G. Pfurtscheller, P. Buser. F.H. Lopes da Silva and H. Petsche (Eds.), Rhythmic EEG Activities and Cortical Functioning. Elsevier, Amsterdam. 1980: 151-177. Rumpl, E. Elektro-neurologische Korrelationen in den frtihen Phasen des posttranmatisehen Komas. Z.EEG-EMG. 1979. 10: 148-157. Schlag, J. Reticular influences on thalamo-cortical activity. In: O. Creutzfeldt (Ed.), The Neuronal Generation of the EEG. Handbook of Electroeneephalography and olin. Neurophysiology, Vol. 2C. Elsevier. Amsterdam. 1974: 119-134. Singer, W. and Driiger, U. Postsynaptic potentials in relay neurons of cat lateral geniculate nucleus after stimulation of the mesencephafic reticular formation. Brain Res.. 1972. 41: 214-220.