Epilepsia, 20599-606, 1979.
Raven Press, New York
Recording Small Sharp Spikes with Depth Electroencephalography Barbara F. Westmoreland, Jean Reiher, and Donald W . Klass Mayo Clinic and Mayo Foundation, Rochester. Minnesota 55901
Summary: Two patients with intractable seizures and focal temporal sharp waves also had small sharp spikes as incidental findings in their scalp electroencephalograms. Depth electroencephalography verified the intracerebral origin of the small sharp spikes and differentiated them from the more significant epileptiform abnormalities.
Spikes and sharp waves are important diagnostic features of the electroencephalogram (EEG). These transients in the interictal EEG frequently denote a propensity for the generation of epileptic seizures (Zivin and Ajmone’ Marsan, 1968). However, many different types of spike and sharp wave activity exist, and not all of these types indicate the likelihood of clinical seizures with the same probability. One type of spike activity, named small sharp spikes (SSS) by Gibbs and Gibbs (1952), frequently encountered in EEGs of adults has little importance for the diagnosis or localization of seizures (Small et al., 1968; Reiher and Klass, 1968, 1970; Small, 1970; Westmoreland and Klass, 1972; Klass, 1975; White et al., 1977; Lebel et al., 1977, 1978). Although the name small sharp spikes is unsatisfactory (Reiher and Klass, 1970; Chatrian et al., 1974), the term has achieved widespread use. The name benign epileptiform transients of sleep (BETS) (White et al., 1977) has been suggested as an alternative, but this has not yet been universally accepted.
In this report we propose to verify the cerebral origin of SSS, describe the characteristics of S S S in depth electroencephalographic (DEEG) recordings, compare the characteristics of the SSS in scalp EEG recordings with those occurring in DEEG, and contrast the characteristics of SSS with temporal sharp waves recorded during DEEG. PATIENTS AND METHODS Our observations are based on EEG and DEEG studies of 2 patients who were being evaluated as possible candidates for surgical treatment of intractable seizures. The preoperative EEGs of both patients contained bilateral SSS during drowsiness and light sleep, as well as focal temporal sharp waves that were predominantly unilateral. Patient 1 was an 18-year-old woman who began having brief seizures at the age of 13 years. The seizures were characterized by feelings “as if this had happened before” or “as if I had been here before and heard these same things before.” At first, the sei-
Received December 5, 1978. Key words: Epileptiform activitySpikesSmal1 sharp spikes4EG-Depth electroencephalography. Dr. Reiher’s present address is Centre Hospitalier, Universitaire, Sherbrooke. Quebec, Canada. Resented in part at the meeting of the American Epilepsy Society, New York, N.Y., December 2, 1971.
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zures occurred about once a month and were unaccompanied by other symptoms. At 15 years of age, she began to have episodes of feeling “detached,” followed by unawareness; and after these seizures, she felt an urge to sleep. During the seizures, observers described her as appearing to be dazed, speaking in syllables that were slurred and incoherent, and hanging her head down as if tired. Subsequently, most of her seizures, which were occurring daily, were characterized by a feeling “as if I were going to lose my mind,” difficulty in speaking, and brief unawareness of her surroundings. According to her mother, the patient would say irrelevant and nonsense words and would pick at her clothes and laugh. The seizures lasted from 30 sec to 3 min and were followed by a stuporous state that lasted 20 to 30 min. The patient also had generalized tonic-clonic seizures during the night. Many different anticonvulsant medications had failed to control her seizures. The patient was right-handed. The results of neurologic examination were normal. Radiologic examination of the head, including stereoscopic views and tomograms, revealed a small area of calcification that, to some observers, appeared to be in the right petroclinoid ligament, but to other observers it appeared to be in the mesial aspect of the right temporal lobe. The results of an angiogram, a pneumoencephalogram, and a cerebrospinal fluid examination were normal. On the Wechsler Adult Intelligence Scale the patient attained a verbal IQ of 95, a performance IQ of 107, and a full-scale IQ of 100. The clinical psychologist believed that the patient exhibited a pattern of language difficulty of the type observed among some patients who have lesions of their left temporal lobes. Multiple EEGs recorded with scalp and nasopharyngeal leads during wakefulness and during sleep contained interictal focal sharp waves arising from the right anterior temporal region. Also, the EEGs during light levels of sleep contained bilateral SSS. Epilepsia, Vol. 20, December 1979
On two separate occasions the patient’s typical seizures were induced by pentylenetetrazol administered intravenously. The EEG at the onset of each seizure contained right anterior temporal sharp waves. DEEG was undertaken because of the evidence of right temporal abnormality in the EEG and left temporal abnormality in the psychometric tests. Patient 2 was a 47-year-old man from Iran. At the age of 5 years he had fallen off a donkey and lacerated his left temporal region, but he had not lost consciousness. At the age of 12 years he had his first seizure, which was characterized by staring and loss of awareness for less than a minute. At the age of 17 years he began having repeated seizures manifested as an undefinable generalized strange sensation and the hearing of a sound like the dial tone of a telephone, followed by staring, inability to speak, loss of awareness, and some automatic movements of the right upper extremity. These became more frequent, and at the age of 25 years he began having major motor seizures in addition to the minor spells. The seizures were often followed by long periods of postictal dysphasia that lasted up to 2 days. He was incapacitated by the seizures, which had been refractory to all anticonvulsants. The patient was right-handed. Neurologic examination revealed ataxia and slowed mentation resulting from the toxic effects of anticonvulsant medications. Plain roentgenograms of the skull and a left carotid arteriogram showed no abnormalities. A pneumoencephalogram showed that the left temporal horn of the lateral ventricle was somewhat larger than the right, and this was believed to be caused by localized atrophy. Psychological tests revealed no significant impairment of mental function. Injection of amobarbital into the left carotid artery produced no impairment of memory function. Multiple scalp EEG recordings showed frequent interictal focal sharp wave discharges over the left anterior temporal re-
SMALL SHARP SPIKES IN DEEG
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gion. A recorded seizure consisted initially of a generalized decrement of the ongoing EEG activity, maximal on the left, followed by bilateral rhythmic 7-Hz activity that was maximal over the left anterior temporal region. DEEG was undertaken to determine if the seizures were arising in a resectable region of the left temporal lobe.
was inserted through a right frontal burr hole and was directed posteriorly, with the tip residing in the paramedial frontal area. Leads VI and VII were inserted through a left temporal burr hole: lead VI (contacts 38-43) was directed anteriorly, with the tip residing in the inferior medial portion of the left temporal lobe; lead VII (contacts 45-50) was directed posteriorly, with the tip residing in the parietal lobe. DEEG In the second patient, seven depth leads In the first patient, five depth leads were were implanted in the left hemisphere inserted into the right frontotemporal lobe, within the left frontal, temporal, parietal, and two depth leads were inserted within and occipital lobes (Fig. 2). Electrode Q the left temporal region (Fig. 1). Leads I, 11, (contacts 1-6) was inserted through a left and I11 were inserted through a right an- frontal burr hole and was directed posteriterior temporal burr hole: lead I (contacts orly and medially, with the tip residing in 1-6) was directed medially and superiorly, the mesial portion of the frontal lobe. Elecwith the tip residing in the thalamus; lead I1 trodes R (contacts 7-12), S (contacts (contacts 8- 13) was directed anteriorly, 13-18), and T (contacts 19-24) were inwith the tip residing near the medial surface serted through a left midtemporal burr hole: of the temporal pole; lead I11 (contacts electrode R was directed anteriorly and 15-20) was directed posteriorly and in- medially, with the tip residing in the inferior feriorly, with the tip residing in the poste- medial portion of the frontal lobe; electrode rior temporal lbbe. Lead IV (contacts S was directed superiorly and medially, 22-27) was inserted through a right poste- with the tip near the left pulvinar; electrode rior temporal burr hole in a mesial direc- T was inserted horizontally and medially, tion, with the tip residing near the with the tip located in the posterior medial thalamus. Electrode V (contacts 3 1-36) portion of the left temporal lobe near the
I -
i
Med Temp f f - 6 J Ant Temp ( 8 - 1 3 ) Post Tamp lf5-201 LV - Mid Temp P2-271 Z - Frontol (31-36) - - - - - + Indicates drrection of inseriion
ll Ill -
Right
-----+ Indicotes direction of insertion
FIG. 1. Diagrams showing location of depth leads in patient 1. A: Segment shows right-sided leads (I-V). B Segment shows left-sided leads (VI and VII). The lowest contact number on each lead is located at the tip. Dotted area represents distribution of SSS. Cross-hatched area represents distribution of temporal sharp waves. Epilepsie, Vol. 20, December 7979
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followed by a low-voltage slow-wave component), and the depth recordings were scanned for concurrent events. Thirty-two channels were used to record the activity from the intracerebral and scalp leads during wakefulness and spontaneous sleep.
Left
I R S T U V X
-
Fronta-Temp Temp I n f Temp Supm-insular Inf rSmp Occipital
I 7-VI (i3-rBI (19-241 (25-301 (3i-361 (37-421
FIG. 2. Diagram showing location of seven depth leads (Q-X) inserted on the left side in patient 2. Dotted area indicates distribution of SSS. Cross-hatched area indicates distribution of temporal sharp waves.
hippocampus. Electrodes U (contacts 25-30), V (contacts 31-36), and X (contacts 37-42) were inserted through a left posterior temporal burr hole: electrode U was directed superiorly and medially, with the tip located in the anterior limb of the internal capsule; electrode V was directed inferiorly and medially, with the tip located in the medial aspect of the left temporal lobe near the amygdala; electrode X was directed posteriorly and superiorly, with the tip located in the anterior occipital lobe. The depth leads were composed of stainless-steel wires insulated with a thermoplastic resin (Formvar’?), except for a I-mm uninsulated portion at the tip of each wire. Each depth lead was constructed of six wires stranded together so that the recording contacts were spaced at 1-cm intervals. The locations of the contact points were determined from postoperative roentgenograms and the Yoss atlas and from measurements made during surgery. Twelve electrodes also were sutured in the scalp beneath the head bandage. SSS were identified by their characteristic appearance in the scalp recordings (short-duration low-voltage diphasic spikes with steep ascending and descending limbs, sometimes Epilepsia, VoL 20, December 1979
RESULTS In the EEGs of both patients, whenever an SSS occurred in the scalp recording, a spike or spike-wave discharge was invariably present also in the recording from intracerebral leads. The SSS were present in bipolar recordings from the depth leads, as well as in referential recordings to extracerebral leads consisting of ear, chin, central, or central vertex leads (Figs. 3 and 4A). The waveforms seen in the depth leads of the two patients corresponding to the SSS on the surface consisted of a very brief (< 50 msec) monophasic or diphasic initial spike that at times was followed by a monophasic component or a ‘diphasic slow-wave component of lower amplitude (Figs. 3 and 4A). The amplitude of the spike ranged from 50 to 250pV. The polarity at the peak was either negative or positive. The morphologic features of the spike discharges in the depth leads were similar to those seen in the surface recording. The SSS in the depth recording occurred singly and sporadically without an associated distortion of the background activity. The discharges had a widespread distribution within the cerebral hemispheres, including the temporal, frontal, and parietal lobes in both patients and the occipital lobe in patient 2. The SSS were recorded predominantly from deep intracerebral structures. The topography of the spikes in the depth recordings of the two patients which were associated with SSS on the surface is shown in the composite diagram in Fig. 5 . The distributions were very similar in both cases. In the patient with bilateral implantation of the depth leads the SSS often appeared to be bilaterally synchronous in the scalp leads over the two hemispheres (although predominating on one side), but the
SMALL SHARP SPIKES IN DEEG
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Right -
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47-50
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FIG. 3. Example of SSS in bipolar recording from patient I in the right- and left-sided depth leads and in scalp leads. LF, left frontal; RF, right frontal; LAT, left anterior temporal; RAT, right anterior temporal; LPT, left posterior temporal; RPT, right posterior temporal.
B
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-
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FIG. 4. Examples of SSS (A) and temporal sharp wave (B)recorded simultaneously from scalp and left-sided depth leads in patient 2. Epilepsia, Vol. 20, December 1979
B . F. WESTMORELAND ET A L .
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JZ$Ef
sss
........ a ~iiiiiii
Area covered by depth leads
FIG. 5. Composite diagram of distribution of SSS in depth leads in the 2 patients. The dotted area represents the overlapping areas covered by the depth leads from both sides of patient 1 and the left side of patient 2. The wavy-lined area represents the overlapping areas of distribution of the SSS in the 2 patients.
corresponding spikes within the depth leads usually occurred independently on the two sides. In the recordings of our 2 patients, SSS were recognizable in the scalp leads only during drowsiness and light sleep. However, once the concomitant spikes in the depth recordings were identified, these could also be detected in the DEEG during wakefulness, but usually with a less widespread distribution. Electrical stimulation through the depth leads did not induce or accentuate SSS in the scalp EEG or DEEG. Regions that gave rise to SSS as the only paroxysmal discharge did not exhibit a decreased threshold for electrically induced afterdischarge and were not involved in the genesis of spontaneous or electrically induced seizures. In contrast to the waveforms associated with the SSS, the discharges in the DEEG associated with the surface anterior temporal sharp waves were higher in amplitude, longer in duration, and more complex (Fig. 4B). The spike or sharp wave component was polyphasic, and the subsequent slow-wave component was prominent. These discharges were often associated ,with slowing of the background
Epilepsia, Vol. 20, December. 1979
activity, and abnormal slow waves in the same areas occurred in brief irregular groups or serial rhythmic trains. The discharges were more closely confined to the temporal region (Figs. 1 and 2) and were maximal in the inferomesial temporal leads. Their locations coincided with areas that gave rise to spontaneous or electrically induced seizure discharges in both patients. Electrical stimulation through the depth leads frequently elicited prolonged afterdischarges from these same areas. Ocular, glossokinetic, myogenic, and electrocardiographic activities were noted in recordings from leads on the scalp or earlobes but not from intracerebral leads. The small sharp spikes in the DEEG were not confined to single leads, and their morphologic features and distribution were distinctly different from pulsation artifacts and from electrostatic discharges. In the first patient, DEEG demonstrated that focal epileptiform abnormalities and seizures arose independently from the right and left temporal regions, and therefore the patient was not considered to be a candidate for surgery. She has continued to be treated medically for her seizures. In the second patient, DEEG demonstrated that the seizures arose from a well-
SMALL SHARP SPIKES IN DEEG
delineated portion of the left inferomesial anterior temporal region (corresponding to the distribution of the anterior temporal sharp waves) that did not involve language function. A block resection of the anterior portion of the left temporal lobe was performed. Postoperative scalp EEGs continued to show bilateral SSS. He has remained free of seizures for 9 years since the operation. DISCUSSION The results of simultaneous scalp EEG and DEEG recordings indicate conclusively that SSS have an intracerebral origin. In extensive recordings of our 2 patients, every SSS that could be detected by scalp leads was associated with a concurrent spike arising from within the cerebrum, and the DEEG was virtually uncontaminated by the numerous artifacts to which the scalp EEG was subject. As compared with SSS in the surface EEG, SSS in the DEEG are similar in several respects: The SSS in each situation have a widespread distribution and a similar and rather simple morphologic appearance. They occur as single sporadic transients and do not disrupt the ongoing background activity from which they arise. However, as expected, the amplitude of the spikes is higher in the depth recording than in the surface EEG. In DEEG, SSS can be distinguished from discharges associated with anterior temporal sharp waves on the surface. The temporal sharp waves are more complex morphologically; they often occur in repetitive clusters and often are associated with prominent abnormal slow waves and with disruption of background rhythms. Also, in contrast to the SSS, the temporal sharp waves occur in areas from which prolonged afterdischarges and seizures can be elicited by electrical stimulation and from which spontaneous seizures arise. We found no evidence that SSS were involved in the process of seizure generation
605
in our 2 patients. The SSS occurred in areas that were independent of those involved in generating spontaneous seizure discharges and electrically induced afterdischarges, and electrical stimulation did not induce or enhance the SSS. DEEG supports the findings from the scalp EEG (Reiher and Klass, 1968; Klass, 1975; White et al., 1977; Lebel et al., 1977, 1978) that SSS are widely distributed throughout both cerebral hemispheres. However, because of the widespread distribution of these spikes and the limited amount of brain sampled by the depth leads, we were unable to determine precisely the anatomic structures responsible for their generation. DEEG contributed information about SSS that is not apparent in the standard EEG. Discharges that are identical to those accompanying SSS in the scalp EEG during drowsiness or light sleep can be detected in the DEEG during wakefulness. Failure to detect SSS in the scalp EEG during wakefulness may be due to masking by background rhythms and the more limited size or synchronization of the neuronal populations that act as generators. Studies of SSS in scalp EEGs have shown that SSS occur as frequently in patients without seizures as in patients who have epileptic seizures (Lebel et al., 1977, 1978) and slightly more frequently in normal subjects than in patients who have temporal lobe seizures (White et al., 1977). The electroencephalographer needs to carefully distinguish SSS from epileptiform discharges in the scalp EEG, which have greater significance for the diagnosis of seizures. A similar distinction needs to be drawn in the DEEG; otherwise, SSS could provide misleading information about the location, laterality, and extent of the epileptogenic areas. The results of DEEG in our 2 epileptic patients lend support to the conclusion that SSS should be considered merely as incidental findings. Because SSS are common in the EEGs of
Epilepsia, Vol. 20, December 1979
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adults (20 to 26%) (White et al., 1977; Lebel et al., 1977,1978), we suspect that they may be seen in DEEGs more frequently if their characteristics are recognized. ACKNOWLEDGMENT The implantation of depth leads in both patients and the left temporal lobectomy in the second patient were performed by Dr. Albert L. Rhoton, Jr. REFERENCES Chatrian GE, Bergamini L, Dondey M, Klass DW, Lennox-Buchthal M, and Petersen I. Appendix B: A glossary of terms most commonly used by clinical electroencephalographers. Electroencephalogr Clin Neurophysiul 37538-548, 1974. Gibbs FA and Gibbs EL. Atlas of Electruencephalography, Vul 2. second edition, Addison-Wesley, Reading, Mass, 1952. Klass DW. Electroencephalographic manifestations of complex partial seizures. Adv Neurol 11: 113- 140, 1975. Lebel M, Reiher J, and Klass D. Small sharp spikes (SSS): Reassessment of electroencephalographic and clinical significance. Electruencephalugr CIin Neuruphysiol 43:463, 1977 (abstract). Lebel M,Reiher J, and Klass DW: Small sharp spikes (SSS): ElectroenCephalographic characteristics and clinical significance. Electruencephalugr CIin Neurophysiul43:463, 1977 (abstract). Reiher J and Klass DW. Two common EEG patterns of doubtful clinical significance. Med Clin North Am 52933-940,1968. Reiher J and Klass DW. "Small sharp spikes" (SSS): Electroencephalographic characteristics and clinical significance. Electroencephalogr CIin Neuruphysiol 2 8 9 , 1970 (abstract). Small JG. Small sharp spikes in a psychiatric population. Arch Gen Psychiatry 22:277-284, 1970. Small JG, Sharpley P, and Small IF. Positive spikes, spike-wave phantoms, and psychomotor variants: A survey of these EEG patterns in psychiatric patients. Arch Gen Psychiatry 18:232-238, 1968.
Epilepsia, Vol. 20, December 1979
Westmoreland BF and Klass DW. Studies of "small spikes" with depth electrography. Epilcpsio 13:346- 347, I972 (abstract). White JC, Langston JW, and Pedley TA. Benign epileptiform transients of sleep: Clarification of the small sharp spike controversy. Neurolugy f Minm a p ) 27:1061 - 1068, 1977. Zivin L and Ajmone Marsan C. Incidence and prognostic significance of "epileptiform" activity in the EEG of non-epileptic subjects. Brtiiti 91:751-778, 1%8.
RESUME Chez deux malades souffrant de crises d'kpilepsie incontrblables et prksentant un foyer de pointes lentes temporal, les E.E.G. de surface montraient aussi I'existence de pointes ackrkes de faible amplitude. Des enregistrements en profondeur ont permis de verifier I'origine intrackrkbrale de ces petites pointes et de les diffkrencier d'anomalies kpileptiformes plus significatives. (J.-L. Gastaut, Marseilles)
RESUMEN Dos pacientes con crisis incontrolables y ondas agudas temporales presentaron, tambikn, de un modo incidental, pequerias puntas agudas en el electroencefalograma. Registros usando electrodos profundos establecieron el origen intracerebral de las pequenas puntas agudas y establecieron la diferencia entre ellas y las anomalias epileptiformes miis significativas. (A. Portera Sanchez, Modrid)
ZUSAMMENFASSUNG 2 Patienten mit therapieresistenten Anfgllen und fokalen temporalen sharp-waves hatten auch gelegentlich kleine "scharfe spikes" im EEG. Tiefenelektroden verifizierten den intracerebralen Ursprung der kleinen "scharfen spikes" und differenzierten sie von den stark ins Auge fallenden epileptischen Abnormitiiten. (D. Scheffner, Heidelher#)
Raven Press, New York
Recording Small Sharp Spikes with Depth Electroencephalography Barbara F. Westmoreland, Jean Reiher, and Donald W . Klass Mayo Clinic and Mayo Foundation, Rochester. Minnesota 55901
Summary: Two patients with intractable seizures and focal temporal sharp waves also had small sharp spikes as incidental findings in their scalp electroencephalograms. Depth electroencephalography verified the intracerebral origin of the small sharp spikes and differentiated them from the more significant epileptiform abnormalities.
Spikes and sharp waves are important diagnostic features of the electroencephalogram (EEG). These transients in the interictal EEG frequently denote a propensity for the generation of epileptic seizures (Zivin and Ajmone’ Marsan, 1968). However, many different types of spike and sharp wave activity exist, and not all of these types indicate the likelihood of clinical seizures with the same probability. One type of spike activity, named small sharp spikes (SSS) by Gibbs and Gibbs (1952), frequently encountered in EEGs of adults has little importance for the diagnosis or localization of seizures (Small et al., 1968; Reiher and Klass, 1968, 1970; Small, 1970; Westmoreland and Klass, 1972; Klass, 1975; White et al., 1977; Lebel et al., 1977, 1978). Although the name small sharp spikes is unsatisfactory (Reiher and Klass, 1970; Chatrian et al., 1974), the term has achieved widespread use. The name benign epileptiform transients of sleep (BETS) (White et al., 1977) has been suggested as an alternative, but this has not yet been universally accepted.
In this report we propose to verify the cerebral origin of SSS, describe the characteristics of S S S in depth electroencephalographic (DEEG) recordings, compare the characteristics of the SSS in scalp EEG recordings with those occurring in DEEG, and contrast the characteristics of SSS with temporal sharp waves recorded during DEEG. PATIENTS AND METHODS Our observations are based on EEG and DEEG studies of 2 patients who were being evaluated as possible candidates for surgical treatment of intractable seizures. The preoperative EEGs of both patients contained bilateral SSS during drowsiness and light sleep, as well as focal temporal sharp waves that were predominantly unilateral. Patient 1 was an 18-year-old woman who began having brief seizures at the age of 13 years. The seizures were characterized by feelings “as if this had happened before” or “as if I had been here before and heard these same things before.” At first, the sei-
Received December 5, 1978. Key words: Epileptiform activitySpikesSmal1 sharp spikes4EG-Depth electroencephalography. Dr. Reiher’s present address is Centre Hospitalier, Universitaire, Sherbrooke. Quebec, Canada. Resented in part at the meeting of the American Epilepsy Society, New York, N.Y., December 2, 1971.
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zures occurred about once a month and were unaccompanied by other symptoms. At 15 years of age, she began to have episodes of feeling “detached,” followed by unawareness; and after these seizures, she felt an urge to sleep. During the seizures, observers described her as appearing to be dazed, speaking in syllables that were slurred and incoherent, and hanging her head down as if tired. Subsequently, most of her seizures, which were occurring daily, were characterized by a feeling “as if I were going to lose my mind,” difficulty in speaking, and brief unawareness of her surroundings. According to her mother, the patient would say irrelevant and nonsense words and would pick at her clothes and laugh. The seizures lasted from 30 sec to 3 min and were followed by a stuporous state that lasted 20 to 30 min. The patient also had generalized tonic-clonic seizures during the night. Many different anticonvulsant medications had failed to control her seizures. The patient was right-handed. The results of neurologic examination were normal. Radiologic examination of the head, including stereoscopic views and tomograms, revealed a small area of calcification that, to some observers, appeared to be in the right petroclinoid ligament, but to other observers it appeared to be in the mesial aspect of the right temporal lobe. The results of an angiogram, a pneumoencephalogram, and a cerebrospinal fluid examination were normal. On the Wechsler Adult Intelligence Scale the patient attained a verbal IQ of 95, a performance IQ of 107, and a full-scale IQ of 100. The clinical psychologist believed that the patient exhibited a pattern of language difficulty of the type observed among some patients who have lesions of their left temporal lobes. Multiple EEGs recorded with scalp and nasopharyngeal leads during wakefulness and during sleep contained interictal focal sharp waves arising from the right anterior temporal region. Also, the EEGs during light levels of sleep contained bilateral SSS. Epilepsia, Vol. 20, December 1979
On two separate occasions the patient’s typical seizures were induced by pentylenetetrazol administered intravenously. The EEG at the onset of each seizure contained right anterior temporal sharp waves. DEEG was undertaken because of the evidence of right temporal abnormality in the EEG and left temporal abnormality in the psychometric tests. Patient 2 was a 47-year-old man from Iran. At the age of 5 years he had fallen off a donkey and lacerated his left temporal region, but he had not lost consciousness. At the age of 12 years he had his first seizure, which was characterized by staring and loss of awareness for less than a minute. At the age of 17 years he began having repeated seizures manifested as an undefinable generalized strange sensation and the hearing of a sound like the dial tone of a telephone, followed by staring, inability to speak, loss of awareness, and some automatic movements of the right upper extremity. These became more frequent, and at the age of 25 years he began having major motor seizures in addition to the minor spells. The seizures were often followed by long periods of postictal dysphasia that lasted up to 2 days. He was incapacitated by the seizures, which had been refractory to all anticonvulsants. The patient was right-handed. Neurologic examination revealed ataxia and slowed mentation resulting from the toxic effects of anticonvulsant medications. Plain roentgenograms of the skull and a left carotid arteriogram showed no abnormalities. A pneumoencephalogram showed that the left temporal horn of the lateral ventricle was somewhat larger than the right, and this was believed to be caused by localized atrophy. Psychological tests revealed no significant impairment of mental function. Injection of amobarbital into the left carotid artery produced no impairment of memory function. Multiple scalp EEG recordings showed frequent interictal focal sharp wave discharges over the left anterior temporal re-
SMALL SHARP SPIKES IN DEEG
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gion. A recorded seizure consisted initially of a generalized decrement of the ongoing EEG activity, maximal on the left, followed by bilateral rhythmic 7-Hz activity that was maximal over the left anterior temporal region. DEEG was undertaken to determine if the seizures were arising in a resectable region of the left temporal lobe.
was inserted through a right frontal burr hole and was directed posteriorly, with the tip residing in the paramedial frontal area. Leads VI and VII were inserted through a left temporal burr hole: lead VI (contacts 38-43) was directed anteriorly, with the tip residing in the inferior medial portion of the left temporal lobe; lead VII (contacts 45-50) was directed posteriorly, with the tip residing in the parietal lobe. DEEG In the second patient, seven depth leads In the first patient, five depth leads were were implanted in the left hemisphere inserted into the right frontotemporal lobe, within the left frontal, temporal, parietal, and two depth leads were inserted within and occipital lobes (Fig. 2). Electrode Q the left temporal region (Fig. 1). Leads I, 11, (contacts 1-6) was inserted through a left and I11 were inserted through a right an- frontal burr hole and was directed posteriterior temporal burr hole: lead I (contacts orly and medially, with the tip residing in 1-6) was directed medially and superiorly, the mesial portion of the frontal lobe. Elecwith the tip residing in the thalamus; lead I1 trodes R (contacts 7-12), S (contacts (contacts 8- 13) was directed anteriorly, 13-18), and T (contacts 19-24) were inwith the tip residing near the medial surface serted through a left midtemporal burr hole: of the temporal pole; lead I11 (contacts electrode R was directed anteriorly and 15-20) was directed posteriorly and in- medially, with the tip residing in the inferior feriorly, with the tip residing in the poste- medial portion of the frontal lobe; electrode rior temporal lbbe. Lead IV (contacts S was directed superiorly and medially, 22-27) was inserted through a right poste- with the tip near the left pulvinar; electrode rior temporal burr hole in a mesial direc- T was inserted horizontally and medially, tion, with the tip residing near the with the tip located in the posterior medial thalamus. Electrode V (contacts 3 1-36) portion of the left temporal lobe near the
I -
i
Med Temp f f - 6 J Ant Temp ( 8 - 1 3 ) Post Tamp lf5-201 LV - Mid Temp P2-271 Z - Frontol (31-36) - - - - - + Indicates drrection of inseriion
ll Ill -
Right
-----+ Indicotes direction of insertion
FIG. 1. Diagrams showing location of depth leads in patient 1. A: Segment shows right-sided leads (I-V). B Segment shows left-sided leads (VI and VII). The lowest contact number on each lead is located at the tip. Dotted area represents distribution of SSS. Cross-hatched area represents distribution of temporal sharp waves. Epilepsie, Vol. 20, December 7979
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followed by a low-voltage slow-wave component), and the depth recordings were scanned for concurrent events. Thirty-two channels were used to record the activity from the intracerebral and scalp leads during wakefulness and spontaneous sleep.
Left
I R S T U V X
-
Fronta-Temp Temp I n f Temp Supm-insular Inf rSmp Occipital
I 7-VI (i3-rBI (19-241 (25-301 (3i-361 (37-421
FIG. 2. Diagram showing location of seven depth leads (Q-X) inserted on the left side in patient 2. Dotted area indicates distribution of SSS. Cross-hatched area indicates distribution of temporal sharp waves.
hippocampus. Electrodes U (contacts 25-30), V (contacts 31-36), and X (contacts 37-42) were inserted through a left posterior temporal burr hole: electrode U was directed superiorly and medially, with the tip located in the anterior limb of the internal capsule; electrode V was directed inferiorly and medially, with the tip located in the medial aspect of the left temporal lobe near the amygdala; electrode X was directed posteriorly and superiorly, with the tip located in the anterior occipital lobe. The depth leads were composed of stainless-steel wires insulated with a thermoplastic resin (Formvar’?), except for a I-mm uninsulated portion at the tip of each wire. Each depth lead was constructed of six wires stranded together so that the recording contacts were spaced at 1-cm intervals. The locations of the contact points were determined from postoperative roentgenograms and the Yoss atlas and from measurements made during surgery. Twelve electrodes also were sutured in the scalp beneath the head bandage. SSS were identified by their characteristic appearance in the scalp recordings (short-duration low-voltage diphasic spikes with steep ascending and descending limbs, sometimes Epilepsia, VoL 20, December 1979
RESULTS In the EEGs of both patients, whenever an SSS occurred in the scalp recording, a spike or spike-wave discharge was invariably present also in the recording from intracerebral leads. The SSS were present in bipolar recordings from the depth leads, as well as in referential recordings to extracerebral leads consisting of ear, chin, central, or central vertex leads (Figs. 3 and 4A). The waveforms seen in the depth leads of the two patients corresponding to the SSS on the surface consisted of a very brief (< 50 msec) monophasic or diphasic initial spike that at times was followed by a monophasic component or a ‘diphasic slow-wave component of lower amplitude (Figs. 3 and 4A). The amplitude of the spike ranged from 50 to 250pV. The polarity at the peak was either negative or positive. The morphologic features of the spike discharges in the depth leads were similar to those seen in the surface recording. The SSS in the depth recording occurred singly and sporadically without an associated distortion of the background activity. The discharges had a widespread distribution within the cerebral hemispheres, including the temporal, frontal, and parietal lobes in both patients and the occipital lobe in patient 2. The SSS were recorded predominantly from deep intracerebral structures. The topography of the spikes in the depth recordings of the two patients which were associated with SSS on the surface is shown in the composite diagram in Fig. 5 . The distributions were very similar in both cases. In the patient with bilateral implantation of the depth leads the SSS often appeared to be bilaterally synchronous in the scalp leads over the two hemispheres (although predominating on one side), but the
SMALL SHARP SPIKES IN DEEG
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FIG. 3. Example of SSS in bipolar recording from patient I in the right- and left-sided depth leads and in scalp leads. LF, left frontal; RF, right frontal; LAT, left anterior temporal; RAT, right anterior temporal; LPT, left posterior temporal; RPT, right posterior temporal.
B
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S Post Temporal
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FIG. 4. Examples of SSS (A) and temporal sharp wave (B)recorded simultaneously from scalp and left-sided depth leads in patient 2. Epilepsia, Vol. 20, December 1979
B . F. WESTMORELAND ET A L .
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sss
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Area covered by depth leads
FIG. 5. Composite diagram of distribution of SSS in depth leads in the 2 patients. The dotted area represents the overlapping areas covered by the depth leads from both sides of patient 1 and the left side of patient 2. The wavy-lined area represents the overlapping areas of distribution of the SSS in the 2 patients.
corresponding spikes within the depth leads usually occurred independently on the two sides. In the recordings of our 2 patients, SSS were recognizable in the scalp leads only during drowsiness and light sleep. However, once the concomitant spikes in the depth recordings were identified, these could also be detected in the DEEG during wakefulness, but usually with a less widespread distribution. Electrical stimulation through the depth leads did not induce or accentuate SSS in the scalp EEG or DEEG. Regions that gave rise to SSS as the only paroxysmal discharge did not exhibit a decreased threshold for electrically induced afterdischarge and were not involved in the genesis of spontaneous or electrically induced seizures. In contrast to the waveforms associated with the SSS, the discharges in the DEEG associated with the surface anterior temporal sharp waves were higher in amplitude, longer in duration, and more complex (Fig. 4B). The spike or sharp wave component was polyphasic, and the subsequent slow-wave component was prominent. These discharges were often associated ,with slowing of the background
Epilepsia, Vol. 20, December. 1979
activity, and abnormal slow waves in the same areas occurred in brief irregular groups or serial rhythmic trains. The discharges were more closely confined to the temporal region (Figs. 1 and 2) and were maximal in the inferomesial temporal leads. Their locations coincided with areas that gave rise to spontaneous or electrically induced seizure discharges in both patients. Electrical stimulation through the depth leads frequently elicited prolonged afterdischarges from these same areas. Ocular, glossokinetic, myogenic, and electrocardiographic activities were noted in recordings from leads on the scalp or earlobes but not from intracerebral leads. The small sharp spikes in the DEEG were not confined to single leads, and their morphologic features and distribution were distinctly different from pulsation artifacts and from electrostatic discharges. In the first patient, DEEG demonstrated that focal epileptiform abnormalities and seizures arose independently from the right and left temporal regions, and therefore the patient was not considered to be a candidate for surgery. She has continued to be treated medically for her seizures. In the second patient, DEEG demonstrated that the seizures arose from a well-
SMALL SHARP SPIKES IN DEEG
delineated portion of the left inferomesial anterior temporal region (corresponding to the distribution of the anterior temporal sharp waves) that did not involve language function. A block resection of the anterior portion of the left temporal lobe was performed. Postoperative scalp EEGs continued to show bilateral SSS. He has remained free of seizures for 9 years since the operation. DISCUSSION The results of simultaneous scalp EEG and DEEG recordings indicate conclusively that SSS have an intracerebral origin. In extensive recordings of our 2 patients, every SSS that could be detected by scalp leads was associated with a concurrent spike arising from within the cerebrum, and the DEEG was virtually uncontaminated by the numerous artifacts to which the scalp EEG was subject. As compared with SSS in the surface EEG, SSS in the DEEG are similar in several respects: The SSS in each situation have a widespread distribution and a similar and rather simple morphologic appearance. They occur as single sporadic transients and do not disrupt the ongoing background activity from which they arise. However, as expected, the amplitude of the spikes is higher in the depth recording than in the surface EEG. In DEEG, SSS can be distinguished from discharges associated with anterior temporal sharp waves on the surface. The temporal sharp waves are more complex morphologically; they often occur in repetitive clusters and often are associated with prominent abnormal slow waves and with disruption of background rhythms. Also, in contrast to the SSS, the temporal sharp waves occur in areas from which prolonged afterdischarges and seizures can be elicited by electrical stimulation and from which spontaneous seizures arise. We found no evidence that SSS were involved in the process of seizure generation
605
in our 2 patients. The SSS occurred in areas that were independent of those involved in generating spontaneous seizure discharges and electrically induced afterdischarges, and electrical stimulation did not induce or enhance the SSS. DEEG supports the findings from the scalp EEG (Reiher and Klass, 1968; Klass, 1975; White et al., 1977; Lebel et al., 1977, 1978) that SSS are widely distributed throughout both cerebral hemispheres. However, because of the widespread distribution of these spikes and the limited amount of brain sampled by the depth leads, we were unable to determine precisely the anatomic structures responsible for their generation. DEEG contributed information about SSS that is not apparent in the standard EEG. Discharges that are identical to those accompanying SSS in the scalp EEG during drowsiness or light sleep can be detected in the DEEG during wakefulness. Failure to detect SSS in the scalp EEG during wakefulness may be due to masking by background rhythms and the more limited size or synchronization of the neuronal populations that act as generators. Studies of SSS in scalp EEGs have shown that SSS occur as frequently in patients without seizures as in patients who have epileptic seizures (Lebel et al., 1977, 1978) and slightly more frequently in normal subjects than in patients who have temporal lobe seizures (White et al., 1977). The electroencephalographer needs to carefully distinguish SSS from epileptiform discharges in the scalp EEG, which have greater significance for the diagnosis of seizures. A similar distinction needs to be drawn in the DEEG; otherwise, SSS could provide misleading information about the location, laterality, and extent of the epileptogenic areas. The results of DEEG in our 2 epileptic patients lend support to the conclusion that SSS should be considered merely as incidental findings. Because SSS are common in the EEGs of
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adults (20 to 26%) (White et al., 1977; Lebel et al., 1977,1978), we suspect that they may be seen in DEEGs more frequently if their characteristics are recognized. ACKNOWLEDGMENT The implantation of depth leads in both patients and the left temporal lobectomy in the second patient were performed by Dr. Albert L. Rhoton, Jr. REFERENCES Chatrian GE, Bergamini L, Dondey M, Klass DW, Lennox-Buchthal M, and Petersen I. Appendix B: A glossary of terms most commonly used by clinical electroencephalographers. Electroencephalogr Clin Neurophysiul 37538-548, 1974. Gibbs FA and Gibbs EL. Atlas of Electruencephalography, Vul 2. second edition, Addison-Wesley, Reading, Mass, 1952. Klass DW. Electroencephalographic manifestations of complex partial seizures. Adv Neurol 11: 113- 140, 1975. Lebel M, Reiher J, and Klass D. Small sharp spikes (SSS): Reassessment of electroencephalographic and clinical significance. Electruencephalugr CIin Neuruphysiol 43:463, 1977 (abstract). Lebel M,Reiher J, and Klass DW: Small sharp spikes (SSS): ElectroenCephalographic characteristics and clinical significance. Electruencephalugr CIin Neurophysiul43:463, 1977 (abstract). Reiher J and Klass DW. Two common EEG patterns of doubtful clinical significance. Med Clin North Am 52933-940,1968. Reiher J and Klass DW. "Small sharp spikes" (SSS): Electroencephalographic characteristics and clinical significance. Electroencephalogr CIin Neuruphysiol 2 8 9 , 1970 (abstract). Small JG. Small sharp spikes in a psychiatric population. Arch Gen Psychiatry 22:277-284, 1970. Small JG, Sharpley P, and Small IF. Positive spikes, spike-wave phantoms, and psychomotor variants: A survey of these EEG patterns in psychiatric patients. Arch Gen Psychiatry 18:232-238, 1968.
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Westmoreland BF and Klass DW. Studies of "small spikes" with depth electrography. Epilcpsio 13:346- 347, I972 (abstract). White JC, Langston JW, and Pedley TA. Benign epileptiform transients of sleep: Clarification of the small sharp spike controversy. Neurolugy f Minm a p ) 27:1061 - 1068, 1977. Zivin L and Ajmone Marsan C. Incidence and prognostic significance of "epileptiform" activity in the EEG of non-epileptic subjects. Brtiiti 91:751-778, 1%8.
RESUME Chez deux malades souffrant de crises d'kpilepsie incontrblables et prksentant un foyer de pointes lentes temporal, les E.E.G. de surface montraient aussi I'existence de pointes ackrkes de faible amplitude. Des enregistrements en profondeur ont permis de verifier I'origine intrackrkbrale de ces petites pointes et de les diffkrencier d'anomalies kpileptiformes plus significatives. (J.-L. Gastaut, Marseilles)
RESUMEN Dos pacientes con crisis incontrolables y ondas agudas temporales presentaron, tambikn, de un modo incidental, pequerias puntas agudas en el electroencefalograma. Registros usando electrodos profundos establecieron el origen intracerebral de las pequenas puntas agudas y establecieron la diferencia entre ellas y las anomalias epileptiformes miis significativas. (A. Portera Sanchez, Modrid)
ZUSAMMENFASSUNG 2 Patienten mit therapieresistenten Anfgllen und fokalen temporalen sharp-waves hatten auch gelegentlich kleine "scharfe spikes" im EEG. Tiefenelektroden verifizierten den intracerebralen Ursprung der kleinen "scharfen spikes" und differenzierten sie von den stark ins Auge fallenden epileptischen Abnormitiiten. (D. Scheffner, Heidelher#)
