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‘Limbic spindles’: A re-appraisal
Electroencephalography and Clinical Neurophysiology, 1978, 4 4 : 3 8 9 - - 3 9 2 © Elsevier/North-Holland Scientific Publishers, Ltd.
389
Clinical note 'LIMBIC SPINDLES': A RE-APPRAISAL J. ENGEL JR.*, S. JERRETT, E. NIEDERMEYER, G. SCHENK, G. GUCER and R. BURNITE
The Saul R. Korey Department of Neurology and the Department of Neuroscience, Albert Einstein College of Medicine, Bronx, N.Y., 10461 and Departments o f Neurology and Neurological Surgery, The Johns Ho~)kins University School of Medicine and Hospital, Baltimore, Md. 21205 (U.S.A.) (Accepted for publication: August 8, 1977)
Respiration-linked 20--40 c/sec spindles have been recorded from the amygdalae and adjacent structures of dogs and monkeys (Domino and Ueki 1960; Ueki and Domino 1961), cats (Gault and Leaton 1963), chimpanzees (Adey 1970; Delgado et al. 1970; Reite et al. 1967) and man (Lesse et al. 1955). Similar spindles also occur in the olfactory bulb of lower animals (Domino and Ueki 1960; Freeman 1959; Gault and Leaton 1963; Peneioza-Rojas and AlcocerCuaron 1967; Ueki and Domino 1961) and man (Hughes 1971). These phenomena are reported by some to be related to odorous stimuli (Delgado et al. 1970; Hughes 1971; Lesse et al. 1955) but not by others (Reite et al. 1967, Ueki and Domino 1961), to sniffing (Gault and Leaton 1963; Lesse et al. 1955; Reite et al. 1967), to mechanical stimulation of the olfactory mucosa by some (Ueki and Domino 1961) but not others (Peneloza-Rojas and AicocerCuaron 1967), to memories (Lesse et al. 1955), to anger and excitement (Domino and Ueki 1960, Reite et al. 1967) and to sleep (Adey 1970; Reite et al. 1967). The relationship of these physiological phenomena to limbic function is of interest and the recent demonstration of very similar spindle-like activity (in the range of 20--50 c/sec) in human nasopharyngeal recordings by Reite and co-workers (1975) and Goldensohn and Santana (1976) suggested that direct recording of limbic activity could be achieved in man. However, in view of the well known instability of nasopharyngeal electrodes, the possibility of an artifact cannot be easily dismissed (Niedermeyer et al. 1976). For this reason, a few examples of our own observations will be demonstrated for a critical re-appraisal of nasopharyngeal recordings of limbic spindles in man. At the Bronx Municipal Hospital Center (BMHC), where only sphenoidal recordings are done, only one * Present address: Reed Neurological Research Center,
Univ. of Calif. Center for the Health Sciences, Los" Angeles, Calif. 90024, U.S.A.
example of spindling (Case 1 below) was observed in over 100 consecutive procedures. In contrast, 20 patients with these spindles were collected from The Johns Hopkins Hospital (JHH) in 86 consecutive cases of nasopharyngeal recordings. The single sphenoidal and 2 representative nasopharyngeal records were chosen for the following brief reports.
Materials and methods
In both institutions, the EEG records were carried out on 16 and 8 channels. The International Electrode System was employed and gold-plated silver electrodes were used. The insertion of the sphenoidal leads at BMHC followed the method described by Pampiglione and Kerridge (1956) though the needle itself (thin-walled 22 gauge) was used only to introduce a Teflon-coated silver wire (0.15 mm) and was withdrawn before the recording began. Commercially available nasopharyngeal electrodes were used by the Johns Hopkins Hospital.
Case reports
Case 1 (BMHC No. 883137) A 43-year-old alcoholic with hepatic encephalopathy and a history of epileptic seizures (grand real, left-sided focal motor) since having pneumococcal meningitis in 1973. The EEG recording was carried out when the patient was lethargic but arouseable. It was abnormal with diffuse 4--6 c/sec activity (a previously noted right parietal sharp wave focus was no longer present). Sphenoidal recording showed the respirationlinked rhythmical bursts of spindle-like character (Fig. 1A), without spread to scalp derivations. The frequency ranged from 14 to 28 c]sec. These bursts were time-locked to both inspiration and expiration;
390
F4-C4
C3-P3
_
| L,,,.
i Fs"T4 T4-T6
FPI"FT_~_.~_~__. . . . . . T3-Ts Ts-O1 Fig. 1. Examples of spindles in sphenoidal leads. Case 1, age 43 years. A: low voltage 14--28 e/see spindles, occurring with both inspiration and expiration appear only from sphenoidal derivations. B: when the mandible was elevated to relieve airway obstruction, these spindles disappeared. C: spindles reappeared as soon as the mandible was released. Calibration 1 see, 100 ~uV. Insert shows spindle detail more clearly.
at times, there was audible snoring during these bursts and at other times not. When her mandible was lifted to open the pharyngeal air passage, the spindles disappeared (Fig. 1B) and, when it was allowed to fall, the spindles reappeared (Fig. 1C). This maneuver was repeated frequently and there was good evidence that the sphenoidal spindles occurred only during airway obstruction.
Case 2 (JHH No. 1043406) Age 62 years, recent onset of psychomotor automatisms with decreased cerebral blood flow demonstrated by dynamic brain scan. The EEG showed left frontotemporal spikes. In sleep (Fig. 2A), unusually slow sleep spindles
(9--10 c/sec) were noticed and there were repetitive runs of 12--16 c/sec waves in both nasopharyngeal leads in synchrony with respiration. This activity was not accompanied by audible snoring and there was no spread from the nasopharyngeal leads into any adjacent electrodes.
Case 3 (JHH No. 1407919) Age 33 years. Four-year-history of epileptic seizures (grand mal, psychomotor automatisms). Numerous EEG tracings consistently revealed a left anterior temporal spike focus. Fig. 2B was taken from two portions of the sleep record. There are recurrent bursts of rhythmical 30--35 c/sec activity seen only in the nasopharyngeal
t
i
t
~
.
~sec ] 50t.,v
I
.
1
.
.
.
(
I
T6- 0 2
Fp -C
B
Fig. 2. Examples of spindles in nasopharyngeal leads. A: case 2, age 62 years. Sleep record with unusually slow (9--10 c/see) sleep spindles (channels 1--3, 5). Note 12--16 c/see spindle-like activity in nasopharyngeal leads and relationship to respiration (thermocouple electrodes). B: case 3, age 33 years. Sleep record. Note 30--35 c/see spindle-like activity in nasopharyngeal leads. On the right side, the artifactual character of these bursts becomes quite obvious. Inserts show that bursts are spindles and not muscle artifact.
T6-O 2
T4-T s
PG~,-T4
FB-PG2
Fp2-F8
Ts-o,
Fp~-F7
Respiration
C4-P4
EKG
p3-o,
A
F..a
CO
392 leads. On the right side, one of these bursts reaches high voltage and clearly reveals the artifactual nature of the discharge.
Discussion
Our data suggest that the demonstration of fast spindle-like activity in nasopharyngeal and sphenoidal leads must be viewed with greatest caution. Several aspects of our cases argue for an artifactual origin of these spindles. The relatively frequent occurrence during nasopharyngeal recordings (23% in our series and 15% reported by others; Goldensohn and Santana 1975) and the extreme rarity of spindles during sphenoidal recordings (less than 1% in our series and never by Driver in over 3000 sphenoidal recordings at The Maudsley Hospital in London; personal communication) is consistent with a conclusion that spindle-like artifact appears when electrode contacts are unstable. The instability of nasopharyngeal electrodes with respect to sphenoidal electrodes is well known. The ability of mandibular manipulation to abolish spindling strongly suggests that they occur only during airway obstruction. The absence of any spindle activity ever appearing from surface derivations even when very high amplitude spindles are recorded from nasopharyngeal leads should make even a deep or mesial temporal generator suspect. The frequency, duration and spatial distribution of the realistic appearing 'limbic' spindles seen in Fig. 3 match those of the subsequent high voltage burst which is clearly artifact. These arguments have convinced us that the 'limbic' spindles that appear during nasopharyngeal recordings do not represent intracerebrally generated neuronal activity, but rather represent unstable electrode pick-up of palatal vibration caused by respiration during partial airway obstruction.
Summary Respiration-linked spindles are frequently recorded from nasopharyngeal electrodes and these have been reported to represent neuronally generated limbic activity. Evidence is presented from sphenoidal and nasopharyngeal recordings suggesting that these spindles are artifactual, due to unstable electrode contacts that record palatal vibration during partial airway obstruction.
R6sum6
Spindles limbiques: rdconsiddration Des fuseaux li6s fi la respiration sont fr6quemment enregistr6s au moyen d'61ectrodes nasopharyng6s et
ont 6t6 interpr6t6s comme repr6sentant l'activit6 neuronale limbique. Les auteurs pr6sentent des donn6es partir d'enregistrements sph6noidaux et nasopharyng6s sugg6rant que ces fuseaux sont des art6facts dus fi des contacts instables d'6lectrodes qui enregistrent la vibration du palais au cours de l'obstruction partielle des voles a6riennes.
References
Adey, W.R. Higher olfactory center. In G.E.W. Wolstenholme and J. Knight (Eds.), Ciba foundation symposium on taste and smell in vertebrates. Churchill, London, 1970: 357--378. Delgado, J.M.R., Johnston, V.S., Wallace, J.D. and Bradley, R.J. Operant conditioning of amygdala spindling in the free chimpanzee. Brain Res., 1970, 22: 347--362. Domino, E.F. and Ueki, S. An analysis of the electrical burst p h e n o m e n o n in some rhinencephalic structures of the dog and monkey. Electroenceph. clin. Neurophysiol., 1960, 12: 635--648. Freeman, W.J. Distribution in time and space of prepyriform electrical activity. J. Neurophysiol., 1959, 22: 644--665." Gault, F.P. and Leaton, R.N. Electrical activity of the olfactory system. Electroenceph. clin. Neurophysiol., 1963, 15: 299--304. Goldensohn, E. and Santana, H. 'Uncal spindles' at nasopharyngeal electrodes. Electroenceph. clin. Neurophysiot., 1976, 40: 333. Hughes, J.R. Discussion of 'Peripheral mechanisms of olfactory discrimination' by P. Macleod. In G. Ohloff and A.F. Thomas (Eds.) Gustation and olfaction. Academic Press, London, 1971: 38--41. Lesse, H., Heath, R.G., Mickle, W.A., Monroe, R.R. and Miller, W.H. Rhinencephalic activity during thought. J. nerv. ment. Dis., 1955, 122: 433--440. Niedermeyer, E., Schenk, G., Gucer, G. and Burnite, R. 'Limbic spindles': fact or artifacts? Electroenceph. clin. Neurophysiol., 1976, 41: 201. Pampiglione, G. and Kerridge, J. EEG abnormalities from the temporal lobe studied with sphenoidal electrodes. J. Neurol. Neurosurg. Psychiat., 1956, 16: 117--129. Peneloza-Rojas, J.H. and Alcocer-Cuaron, C. The electrical activity of the olfactory bulb in cats with nasal and tracheal breathing. Electroenceph. clin. Neurophysiol., 1967, 22: 468--472, Reite, M. Non-invasive recording of limbic spindles in man. Electroenceph. clin. Neurophysiol., 1975, 38: 539--541. Reite, M., Stephens, L. and Pegram, G.V. Uncal spindling in the chimpanzee. Brain Res., 1966-67, 3: 392--395. Ueki, S.V. and Domino, E.F. Some evidence for a mechanical receptor in olfactory function. J. Neurophysiol., 1961, 24: 12--25.
389
Clinical note 'LIMBIC SPINDLES': A RE-APPRAISAL J. ENGEL JR.*, S. JERRETT, E. NIEDERMEYER, G. SCHENK, G. GUCER and R. BURNITE
The Saul R. Korey Department of Neurology and the Department of Neuroscience, Albert Einstein College of Medicine, Bronx, N.Y., 10461 and Departments o f Neurology and Neurological Surgery, The Johns Ho~)kins University School of Medicine and Hospital, Baltimore, Md. 21205 (U.S.A.) (Accepted for publication: August 8, 1977)
Respiration-linked 20--40 c/sec spindles have been recorded from the amygdalae and adjacent structures of dogs and monkeys (Domino and Ueki 1960; Ueki and Domino 1961), cats (Gault and Leaton 1963), chimpanzees (Adey 1970; Delgado et al. 1970; Reite et al. 1967) and man (Lesse et al. 1955). Similar spindles also occur in the olfactory bulb of lower animals (Domino and Ueki 1960; Freeman 1959; Gault and Leaton 1963; Peneioza-Rojas and AlcocerCuaron 1967; Ueki and Domino 1961) and man (Hughes 1971). These phenomena are reported by some to be related to odorous stimuli (Delgado et al. 1970; Hughes 1971; Lesse et al. 1955) but not by others (Reite et al. 1967, Ueki and Domino 1961), to sniffing (Gault and Leaton 1963; Lesse et al. 1955; Reite et al. 1967), to mechanical stimulation of the olfactory mucosa by some (Ueki and Domino 1961) but not others (Peneloza-Rojas and AicocerCuaron 1967), to memories (Lesse et al. 1955), to anger and excitement (Domino and Ueki 1960, Reite et al. 1967) and to sleep (Adey 1970; Reite et al. 1967). The relationship of these physiological phenomena to limbic function is of interest and the recent demonstration of very similar spindle-like activity (in the range of 20--50 c/sec) in human nasopharyngeal recordings by Reite and co-workers (1975) and Goldensohn and Santana (1976) suggested that direct recording of limbic activity could be achieved in man. However, in view of the well known instability of nasopharyngeal electrodes, the possibility of an artifact cannot be easily dismissed (Niedermeyer et al. 1976). For this reason, a few examples of our own observations will be demonstrated for a critical re-appraisal of nasopharyngeal recordings of limbic spindles in man. At the Bronx Municipal Hospital Center (BMHC), where only sphenoidal recordings are done, only one * Present address: Reed Neurological Research Center,
Univ. of Calif. Center for the Health Sciences, Los" Angeles, Calif. 90024, U.S.A.
example of spindling (Case 1 below) was observed in over 100 consecutive procedures. In contrast, 20 patients with these spindles were collected from The Johns Hopkins Hospital (JHH) in 86 consecutive cases of nasopharyngeal recordings. The single sphenoidal and 2 representative nasopharyngeal records were chosen for the following brief reports.
Materials and methods
In both institutions, the EEG records were carried out on 16 and 8 channels. The International Electrode System was employed and gold-plated silver electrodes were used. The insertion of the sphenoidal leads at BMHC followed the method described by Pampiglione and Kerridge (1956) though the needle itself (thin-walled 22 gauge) was used only to introduce a Teflon-coated silver wire (0.15 mm) and was withdrawn before the recording began. Commercially available nasopharyngeal electrodes were used by the Johns Hopkins Hospital.
Case reports
Case 1 (BMHC No. 883137) A 43-year-old alcoholic with hepatic encephalopathy and a history of epileptic seizures (grand real, left-sided focal motor) since having pneumococcal meningitis in 1973. The EEG recording was carried out when the patient was lethargic but arouseable. It was abnormal with diffuse 4--6 c/sec activity (a previously noted right parietal sharp wave focus was no longer present). Sphenoidal recording showed the respirationlinked rhythmical bursts of spindle-like character (Fig. 1A), without spread to scalp derivations. The frequency ranged from 14 to 28 c]sec. These bursts were time-locked to both inspiration and expiration;
390
F4-C4
C3-P3
_
| L,,,.
i Fs"T4 T4-T6
FPI"FT_~_.~_~__. . . . . . T3-Ts Ts-O1 Fig. 1. Examples of spindles in sphenoidal leads. Case 1, age 43 years. A: low voltage 14--28 e/see spindles, occurring with both inspiration and expiration appear only from sphenoidal derivations. B: when the mandible was elevated to relieve airway obstruction, these spindles disappeared. C: spindles reappeared as soon as the mandible was released. Calibration 1 see, 100 ~uV. Insert shows spindle detail more clearly.
at times, there was audible snoring during these bursts and at other times not. When her mandible was lifted to open the pharyngeal air passage, the spindles disappeared (Fig. 1B) and, when it was allowed to fall, the spindles reappeared (Fig. 1C). This maneuver was repeated frequently and there was good evidence that the sphenoidal spindles occurred only during airway obstruction.
Case 2 (JHH No. 1043406) Age 62 years, recent onset of psychomotor automatisms with decreased cerebral blood flow demonstrated by dynamic brain scan. The EEG showed left frontotemporal spikes. In sleep (Fig. 2A), unusually slow sleep spindles
(9--10 c/sec) were noticed and there were repetitive runs of 12--16 c/sec waves in both nasopharyngeal leads in synchrony with respiration. This activity was not accompanied by audible snoring and there was no spread from the nasopharyngeal leads into any adjacent electrodes.
Case 3 (JHH No. 1407919) Age 33 years. Four-year-history of epileptic seizures (grand mal, psychomotor automatisms). Numerous EEG tracings consistently revealed a left anterior temporal spike focus. Fig. 2B was taken from two portions of the sleep record. There are recurrent bursts of rhythmical 30--35 c/sec activity seen only in the nasopharyngeal
t
i
t
~
.
~sec ] 50t.,v
I
.
1
.
.
.
(
I
T6- 0 2
Fp -C
B
Fig. 2. Examples of spindles in nasopharyngeal leads. A: case 2, age 62 years. Sleep record with unusually slow (9--10 c/see) sleep spindles (channels 1--3, 5). Note 12--16 c/see spindle-like activity in nasopharyngeal leads and relationship to respiration (thermocouple electrodes). B: case 3, age 33 years. Sleep record. Note 30--35 c/see spindle-like activity in nasopharyngeal leads. On the right side, the artifactual character of these bursts becomes quite obvious. Inserts show that bursts are spindles and not muscle artifact.
T6-O 2
T4-T s
PG~,-T4
FB-PG2
Fp2-F8
Ts-o,
Fp~-F7
Respiration
C4-P4
EKG
p3-o,
A
F..a
CO
392 leads. On the right side, one of these bursts reaches high voltage and clearly reveals the artifactual nature of the discharge.
Discussion
Our data suggest that the demonstration of fast spindle-like activity in nasopharyngeal and sphenoidal leads must be viewed with greatest caution. Several aspects of our cases argue for an artifactual origin of these spindles. The relatively frequent occurrence during nasopharyngeal recordings (23% in our series and 15% reported by others; Goldensohn and Santana 1975) and the extreme rarity of spindles during sphenoidal recordings (less than 1% in our series and never by Driver in over 3000 sphenoidal recordings at The Maudsley Hospital in London; personal communication) is consistent with a conclusion that spindle-like artifact appears when electrode contacts are unstable. The instability of nasopharyngeal electrodes with respect to sphenoidal electrodes is well known. The ability of mandibular manipulation to abolish spindling strongly suggests that they occur only during airway obstruction. The absence of any spindle activity ever appearing from surface derivations even when very high amplitude spindles are recorded from nasopharyngeal leads should make even a deep or mesial temporal generator suspect. The frequency, duration and spatial distribution of the realistic appearing 'limbic' spindles seen in Fig. 3 match those of the subsequent high voltage burst which is clearly artifact. These arguments have convinced us that the 'limbic' spindles that appear during nasopharyngeal recordings do not represent intracerebrally generated neuronal activity, but rather represent unstable electrode pick-up of palatal vibration caused by respiration during partial airway obstruction.
Summary Respiration-linked spindles are frequently recorded from nasopharyngeal electrodes and these have been reported to represent neuronally generated limbic activity. Evidence is presented from sphenoidal and nasopharyngeal recordings suggesting that these spindles are artifactual, due to unstable electrode contacts that record palatal vibration during partial airway obstruction.
R6sum6
Spindles limbiques: rdconsiddration Des fuseaux li6s fi la respiration sont fr6quemment enregistr6s au moyen d'61ectrodes nasopharyng6s et
ont 6t6 interpr6t6s comme repr6sentant l'activit6 neuronale limbique. Les auteurs pr6sentent des donn6es partir d'enregistrements sph6noidaux et nasopharyng6s sugg6rant que ces fuseaux sont des art6facts dus fi des contacts instables d'6lectrodes qui enregistrent la vibration du palais au cours de l'obstruction partielle des voles a6riennes.
References
Adey, W.R. Higher olfactory center. In G.E.W. Wolstenholme and J. Knight (Eds.), Ciba foundation symposium on taste and smell in vertebrates. Churchill, London, 1970: 357--378. Delgado, J.M.R., Johnston, V.S., Wallace, J.D. and Bradley, R.J. Operant conditioning of amygdala spindling in the free chimpanzee. Brain Res., 1970, 22: 347--362. Domino, E.F. and Ueki, S. An analysis of the electrical burst p h e n o m e n o n in some rhinencephalic structures of the dog and monkey. Electroenceph. clin. Neurophysiol., 1960, 12: 635--648. Freeman, W.J. Distribution in time and space of prepyriform electrical activity. J. Neurophysiol., 1959, 22: 644--665." Gault, F.P. and Leaton, R.N. Electrical activity of the olfactory system. Electroenceph. clin. Neurophysiol., 1963, 15: 299--304. Goldensohn, E. and Santana, H. 'Uncal spindles' at nasopharyngeal electrodes. Electroenceph. clin. Neurophysiot., 1976, 40: 333. Hughes, J.R. Discussion of 'Peripheral mechanisms of olfactory discrimination' by P. Macleod. In G. Ohloff and A.F. Thomas (Eds.) Gustation and olfaction. Academic Press, London, 1971: 38--41. Lesse, H., Heath, R.G., Mickle, W.A., Monroe, R.R. and Miller, W.H. Rhinencephalic activity during thought. J. nerv. ment. Dis., 1955, 122: 433--440. Niedermeyer, E., Schenk, G., Gucer, G. and Burnite, R. 'Limbic spindles': fact or artifacts? Electroenceph. clin. Neurophysiol., 1976, 41: 201. Pampiglione, G. and Kerridge, J. EEG abnormalities from the temporal lobe studied with sphenoidal electrodes. J. Neurol. Neurosurg. Psychiat., 1956, 16: 117--129. Peneloza-Rojas, J.H. and Alcocer-Cuaron, C. The electrical activity of the olfactory bulb in cats with nasal and tracheal breathing. Electroenceph. clin. Neurophysiol., 1967, 22: 468--472, Reite, M. Non-invasive recording of limbic spindles in man. Electroenceph. clin. Neurophysiol., 1975, 38: 539--541. Reite, M., Stephens, L. and Pegram, G.V. Uncal spindling in the chimpanzee. Brain Res., 1966-67, 3: 392--395. Ueki, S.V. and Domino, E.F. Some evidence for a mechanical receptor in olfactory function. J. Neurophysiol., 1961, 24: 12--25.