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Electroencephalography and clinical Neurophysiology 95 (1995) 71-76

The significance of the phi rhythm

Peter L. Silbert \ Kurupath Radhakrishnan 2, Judy Johnson, Donald W. Klass *

Section of Electroencephalography, Mayo Clinic and Mayo Foundation, 200 First Street Sw, Rochester, MN 55905, USA Accepted for publication: 1 April 1995

Abstract

We reviewed two series of patients with the phi rhythm (posterior rhythmic slow waves occurring after eye closure) to determine its characteristics and clinical significance. Phi rhythm was defined as a minimum of three consecutive monomorphic posterior delta waves occurring within 2 sec of eye closure on at least two occasions during electroencephalography. Group 1 consisted of 30 patients (16 male and 14 female) with a mean age of 11.6 ± 8.4 years (range, 3 to 46 years) who were evaluated between 1978 and 1993. Phi rhythm most commonly occurred when the patient was alert and after concentrated visual attention, such as reading or picture or pattern scanning. Seventeen of these patients had epilepsy (11 generalized, 3 focal, 1 both, and 2 unclassified). The frequency of epilepsy was not significantly different from that of a control group of 60 patients matched for age and sex; however, generalized epilepsies were more common in the phi group (P = 0.008). Group 2 consisted of a previously unreported series of 121 patients evaluated between 1960 and 1962. A diverse range of underlying clinical diagnoses was evident in both groups. The mechanism of the phi rhythm is unknown, but the findings suggest that the origin is subcortical and that the presence of this activity should not be considered diagnostic of a seizure disorder.

Keywords: Electroencephalography; Delta activity; Posterior; Phi rhythm

The Greek letter 7T (pi) has been used in the past to refer to any posterior slow waves or rhythms of 3 to 4 Hz in the electroencephalogram (EEG) which are not harmonically related to alpha activity (Dutertre, 1977). In 1959, while working at the Mayo Clinic with one of us (D.W.K.), Dr. David D. Daly proposed the Greek letter 4> (phi) to designate a particular type of posterior rhythmic delta activity that occurred after eye closure, in order to distinguish this type of activity from other types of posterior slow waves that occur while the eyes are closed but are not consistently related to the act of eye closure (Naquet et al., 1976). Although this appellation has been used infrequently (Naquet et al., 1976; PeBenito et al., 1983; Westmoreland and Klass, 1990), a few authors have called attention to phi rhythm in reports of small numbers of cases (Crighel, 1963; Johnson et al., 1964; Rossler and Spic3kova, 1966; Belsh et al., 1983; PeBenito et al., 1983). These studies have concluded that the phi rhythm occurs exclusively during childhood and adolescence and that it is found predominantly in patients who have epilepsy

• Corresponding author. Tel.: 1 507-284-3335; Fax: 1-507-284-2107. 1 Royal Perth Hospital, Perth, Australia.

2 SREE Chitra Medical Institute, Trivandrum, Kerala, India.

0013-4694/95/$09.50 © 1995 Elsevier Science Ireland Ltd. All rights reserved SSDI 0013-4694(95)00076-3

(Crighel, 1963; Rossler and Spicakova, 1966; Belsh et al., 1983; PeBenito et al., 1983), although it has also been found in patients who have nonepileptic conditions (Johnson et al., 1964).

The current study was undertaken to review the characteristics of the phi rhythm in a larger number of cases in an effort to further illuminate its electrographic characteristics and clinical significance.

1. Method

1.1. Phi rhythm

Phi rhythm was defined as the presence of a minimum of three consecutive monomorphic, bilaterally synchronous slow waves (less than 4 Hz) arising from the occipitoparietal regions, distinct from the background, and occurring within 2 sec of eye closure on at least two occasions during EEG. An arbitrary maximal duration of 4 sec was chosen to avoid overlap with other types of posterior rhythmic slow waves. Two groups of patients were studied.

EEG 94195

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P.L. Silbert et al. / Electroencephalography and clinical Neurophysiology 95 (1995) 71-76

1.2. Study groups

Group 1 comprised all patients who underwent EEG between January 1978 and October 1993 and who had a phi rhythm recorded. The patients were identified from the Mayo Clinic EEG database. This study period was chosen to correspond with the availability of modern neuroimaging procedures. The presence of the phi rhythm was confirmed on the basis of the descriptive EEG reports and the actual EEG tracings, whenever available. In patients who had EEG more than once during the study period, the first EEG showing the phi rhythm was considered the index EEG. In all cases, EEG was performed with the 10/20 system of electrode placement, a paper speed of 30 mmysec, a low linear frequency setting of 1.0 Hz, and standard sensitivity settings of 5 /-LV /mm for recordings in adults and 10 to 20 /-LV /mm for recordings in children. Bipolar and referential montages were used during wakefulness, and most of the patients also had recordings during sleep. Eye opening and eye closure were performed during each montage in wakefulness. Additional procedures performed in all patients included reading, scanning a standard picture and a standard geometric pattern, and mental arithmetic (or counting, depending on the patient's age). Eye closure was performed after each type of activity. Hyperventilation was performed with the eyes closed,

Table 1

Clinical diagnoses of patients with phi rhythm

Group 1 (1978-1993) a

Group 2 (1960-1962) a

Patients with epilepsy
Idiopathic epilepsy 15 (2P, lOG, 2U, IB) 37 (5P, 27G, 5U)
Cerebral palsy/mental 1 (G) 5 (2P, 2G, IV)
retardation
Head injury 4 (p)
Phakomatoses l(P) 1 (P)
CNS b tumors 1 (P)
Stroke 1 (P)
Hydrocephalus 1 (G)
Total 17 (3P, llG, 2U, IB) 50 (14P, 30G, 6U)
Patients without epilepsy
Headache 3 20
Cerebral palsy/mental 9
retardation
Behavioral problems 10
Spells/syncope 5 7
Sydenham's chorea 4
Encephalitis/meningitis 1 3
Posterior fossa tumors 3
Phakomatoses 2
Other 3 13
Total 13 71
Total patients 30 121 a P, partial; G, generalized; U, unclassified; B, both generalized and partial.

b CNS, central nervous system.

and a lO-sec period of eye opening followed the cessation of hyperventilation. Photic stimulation was performed with the eyes open, at selected flash frequencies between 1 and 30 Hz, and then with the eyes closed.

The medical records were reviewed for information pertaining to the clinical history, neurologic examination, family history, medications, results of neuroimaging investigations, and the indications for referral for EEG. The EEGs were reviewed (when available) for the characteristics of the phi rhythm, including its latency after eye closure, frequency, duration, voltage, symmetry, distribution, persistence, and relationship to state and activating procedures. Other characteristics of the EEG, including response to photic stimulation, were also noted. For patients who had a history of epilepsy, the type of epilepsy was classified as partial (focal), generalized, or uncertain. Patients with a remote history of only febrile seizures were not classified as epileptic.

A control group of 60 cases without phi rhythm was randomly selected from the files of the EEG laboratory and was matched with group 1 for year of EEG, age, and sex. Phi rhythm was excluded on the basis of the descriptive reports. The relative frequencies of seizure disorders in the control and study groups were compared.

Group 2 comprised a previously unreported series of patients with the phi rhythm evaluated between 1960 and 1962 by one of the authors (D.W.K.). The medical records of these patients and the associated EEG findings were reviewed.

1.3. Statistical analysis

Standard deviations were used to define the dispersion.

The statistical significance between different groups was assessed with Student's t test and X2 analysis.

2. Results

2.1. Group 1

Thirty patients with posterior phi rhythm were identified from a total of 224,198 EEGs obtained at the Mayo Clinic during the study period. Of the 30 patients, 16 were male and 14 were female; their mean age at the time of the index EEG was 11.6 ± 8.4 years (median, 9.5 years; range, 3 to 46 years).

Clinical diagnosis

The clinical diagnoses are given in Table 1. Seventeen patients had a current history of epilepsy, and one patient with meningitis had a remote history of febrile seizures. Additional clinical diagnoses in the patients with epilepsy included mild cerebral palsy in one patient with absence seizures and Klippel- Trenaunay syndrome in one patient with a focal seizure disorder. The epilepsy was partial in 3

P.L. Silbert et al. / Electroencephalography and clinical Neurophysiology 95 (]995) 71-76

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Fig. L Phi rhythm after eye closure in an 8-year-old girl with nonepileptic "spells."

patients, generalized in 11, and unclassifiable in 3, including 1 patient with generalized tonic-clonic seizures and both focal and generalized epileptiform activity on the EEG. That patient had EEGs performed multiple times between the ages of 3 and 12 years; the most recent EEG showed generalized spike-and-wave activity, and previous

Table 2

Electroencephalographic characteristics of phi rhythm in 16 patients

EEGs showed clearly focal epileptiform activity arising from the occipital region, central region, frontal region, and the right anterior temporal region. In the five patients with nonepileptic spells, the results of awake and sleep EEGs were normal, apart from the presence of the phi rhythm, and the clinical suspicion of epilepsy was low.

Age / sex Presence of phi after procedure

Pattern Picture Reading Other
13/F ++ + Photic, hv
13/M + ++ ++ hv
7/M Drowsy b
8/M + ++ +
l1/F ++
l1/M ++ +
8/F ++ + Photic, hv
46/F ++ hv
13/M ++ ++ ++ Mental concentration, hv
5/M Drowsy a
l1/M ++ Photic, hv
9/F ++ Mental concentration
13/F ++ ++
7/M Drowsy a
17/F + ++
8/M ++ ++ ++ Mental concentration, hv Epileptiform activity

GSW GSW No GATSW cr su

Multifocal spikes, GSW No

No

GSW

GATSW (maximal R) No

No

GSW

GSW

GATSW

GATSW

Clinical diagnosis

Primary generalized epilepsy (GTCS) Primary generalized epilepsy (GTCS) Primary generalized epilepsy (Abs) Primary generalized epilepsy (Abs) BREC

Focal and generalized epilepsy (GTCS) Spells

Spells

Primary generalized epilepsy (GTCS) Unclassified GTCS

Headaches

TIAs

Primary generalized epilepsy (GTCS) Hyperactive/tremor b

Primary generalized epilepsy (Abs/GTCS) Narcolepsy C

a Patient was drowsy at time of activation procedures. b No personal or family history of epilepsy.

C No personal history of epilepsy (positive family history).

Abbreviations: Abs, absence seizure; BREC, benign rolandic epilepsy of childhood; cr sh, centrotemporal sharp wave; GATSW, generalized atypical spike-and-wave activity; GSW, generalized 3-Hz spike-and-wave activity; GTCS, generalized tonic-clonic seizure; hv, hyperventilation.

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Follow-up information in three of these patients, obtained during 9, 6, and 3 years, revealed no evidence of epilepsy.

EEG findings

Original EEGs were available for review in 16 of the 30 patients; 10 patients had a diagnosis of epilepsy, and 6 patients had no evidence of epilepsy.

Phi characteristics (Fig. 1). The median latency before onset of the phi rhythm after eye closure was 450 msec (range, 100-1000 msec), and the median frequency was 3 Hz (range, 2.5-4.0 Hz). The median number of waves after eye closure was 6 (range, 3-9), and the median total duration of the phi rhythm after eye closure was 2 sec (range, 1.0-3.0 sec). The phi rhythm occurred after eye closure 20% of the time (median) that eye closure was performed (range, 5-30%). The mean voltage (in bipolar derivations) was 60 ± 22 IL V for the alpha rhythm and 136 ± 47 ILV for the phi rhythm. The median amplitude ratio of phi: alpha rhythm was 2:1 (range, 1.7-4). The voltage and distribution were usually symmetrical on the two sides of the head.

Activating procedures. Phi rhythm was most common when the patient was alert, and it was often particularly evident after procedures that involved concentrated visual attention (Table 2). All three patients who did not demonstrate phi rhythm after reading or looking at the picture or pattern were drowsy at the time.

Persistence of posterior phi rhythm. Five patients had 17 additional EEG recordings obtained more than 12 months from the index EEG. Of these, four had phi rhythm persisting at 1, 4, 6, and 10 years; the patient who had phi rhythm 10 years after index EEG was 23 years old at the time of his most recent recording. One patient had no evidence of phi rhythm on four recordings obtained during a 5-year period before the index EEG (obtained at age 11 years) or during a follow-up recording obtained 2 years after the index EEG.

Intervening posterior delta activity. Ten of the 16 patients with EEGs available for review had phi rhythm without intervening posterior delta activity during resting wakefulness. In three of these, posterior delta activity (of a different configuration to the posterior phi activity) developed during hyperventilation. Six patients had additional intervening posterior delta activity during alertness, and in two patients this activity was of a configuration similar to the phi rhythm. Posterior delta activity was also present during hyperventilation in four of these six patients.

Epileptiform activity. Generalized epileptiform activity was present in the recordings of nine patients, focal changes in three, and both focal and generalized epileptiform activity in one (Table 2).

Photo paroxysmal response. Three patients had a photoparoxysmal response.

Neuroimaging findings

Computed tomography was performed in nine patients, and magnetic resonance imaging was done in six other patients. No patient had a structural lesion or other abnormality demonstrated by these procedures.

Comparison of group 1 with control group

Of the 60 control patients, 33 had a history of epilepsy; the proportion of control patients with epilepsy was not significantly different from the proportion in the phi group (X2 = 0.006, degree of freedom = 1, P = 0.936). The epilepsy in the control patients was partial in 20, generalized in 11, and unclassified generalized tonic-clonic seizures in 2. One patient had no history of seizures, but his EEG showed centrotemporal spikes, and another patient had a history of febrile seizures only. A history of generalized epilepsy was more common in the patients with phi rhythm (X2 = 7.166, degree of freedom = 1, P = 0.008).

2.2. Group 2

During a 2-year study period from 1960 to 1962, 121 patients with phi rhythm were identified. During this study period, 22,522 EEGs were obtained in the Mayo Clinic EEG department. Of the 121 patients, 62 were male and 59 were female; their mean age was 13.1 ± 12 years (median, 10 years; range, 3 to 65 years).

Clinical diagnosis

The clinical diagnoses are given in Table 1. Fifty patients had epilepsy, 3 patients had febrile seizures, and the remaining 68 patients had no history of epileptic seizures. The mean age of the patients with epilepsy did not differ significantly from that in patients without epilepsy (p = 0.269). (In the epilepsy group, the mean age was 11.8 ± 9.0 years, the median was 10 years, and the range was 3 to 64 years. In the group without epilepsy, the mean age was 14.0 ± 13.4 years, the median was 10 years, and the range was 3 to 65 years.)

Epilepsy was generalized in 30 patients, focal in 14, and unclassified in 6. Nine patients had a photoparoxysmal response, including eight with a diagnosis of a generalized seizure disorder and one patient with no history of epilepsy.

Comparison of groups 1 and 2

There was no significant difference between groups 1 and 2 for age at the time of the index EEG (p = 0.428) or for the proportion of patients with a diagnosis of epilepsy (X2 = 2.293, degree of freedom = 1, P = 0.131).

3. Discussion

In previous reports of activity most likely identical to the phi rhythm, epilepsy was reported in 71 % to 100% of

PL. Silbert et al. / Electroencephalography and clinical Neurophysiology 95 (]995) 71-76

the patients (Crighel, 1963; Rossler and Spicakova, 1966; Belsh et al., 1983; PeBenito et al., 1983), although one report noted its presence in Sydenham's chorea (Johnson et al., 1964). Belsh et al. (1983) suggested that the presence of epilepsy was most probably related to the referral bias in patients selected for EEG. In our series of patients, the phi rhythm was found in patients with varied clinical diagnoses (Table 1), and the case-control study provides further evidence that in this population the diagnosis of epilepsy is not significantly different between patients with and those without phi rhythm; however, generalized epilepsies were more prevalent in the phi group. The prevalence of phi rhythm was higher in group 2 (patients evaluated from 1960 to 1962). The reasons for this difference are not completely clear, but they may include more diverse indications for EEG referrals in earlier years of the study, a greater proportion of children in the earlier years (28% were younger than 16 years in group 2, and 18% were younger than 16 years in group 1), and less attention to the phenomenon by a more varied group of interpreters in the later years of the study.

The diverse clinical associations suggest that the cause of phi rhythm is nonspecific and that it should be distinguished from epileptiform activity on eye closure with spike or spike-wave accompaniments (Newmark and Penry, 1979) and from other types of posterior slow wave activity. Of the four main types of slow waves described by Aird and Gastaut (1959), the phi rhythm most closely resembles the "slow posterior rhythm associated with petit mal" (Kellaway, 1979; PeBenito et al., 1983; Holmes et al., 1987). The distinctive features of the "slow posterior rhythm associated with petit mal" described by Aird and Gastaut (1959) included the predominant frequency of 3 Hz, high amplitude, sinusoidal morphology, posterior location, bilateral symmetry and synchrony of bursts, attenuation with eye opening, and accentuation with hyperventilation. Although Fig. 8 A in their report depicts a burst of such activity occurring after eye closure, no mention was made of a consistent relationship with that action as opposed to eyelid position. The "slow posterior rhythm associated with petit mal" was not found in any of 500 normal control subjects during rested wakefulness, but the controls were not matched for age.

PeBenito et al. (1983) described 28 children with paroxysmal rhythmic posterior slow wave patterns. They distinguished 15 patients who had "posterior slow associated with petit mal," all of whom had seizures, from 13 patients with phi rhythm (seen only after eye closure), 10 of whom had seizures. They found that both patterns were frequently associated with other EEG abnormalities but that EEG and neurologic abnormalities were more common in the group with "posterior slow associated with petit mal.'

In our study, six patients had intervening posterior delta activity in addition to the phi rhythm, two of whom had a generalized seizure disorder, manifested. clinically by gen-

75

eralized tonic-clonic seizures in one patient and absence seizures in the other. In our later series (group 1), 2 of the 16 patients with recordings available for review had associated epileptiform abnormalities but no clinical seizures. One was an 8-year-old boy with narcolepsy and a positive family history of epilepsy, and the other was a 7-year-old boy with hyperactivity and an atypical tremor. A photoparoxysmal response was present in 8 of the 30 patients from the initial series who had a generalized seizure disorder and in 3 of the 11 patients from the current series. Overall, this frequency is consistent with the expected frequency of a photoparoxysmal response in a patient group with generalized seizure disorders (Gastaut et al., 1958; Stevens, 1962; Newmark and Penry, 1979).

Phi rhythm does not seem to be simply an enhancement of coexisting posterior nonrhythmic delta activity. Of the 16 patients whose records were available for review, 10 did not have prominent posterior delta activity, although isolated nonrepetitive "posterior slow waves of youth" were not uncommon. The phi rhythm is not a variant of drowsy activity because it occurred primarily when the patients were alert and usually occurred after concentrated visual attention (Table 2, Fig. 1). It was distinguishable from the increase of slow waves which often occurred during hyperventilation, although in 7 of the 16 patients it occurred after hyperventilation.

Slow posterior waves of 2.5 to 4.5 Hz are commonly observed in children and peak at age 5 to 7 years; they are present in approximately 25% of normal children at this age. They are often accentuated by drowsiness and hyperventilation and attenuated by eye opening, and they become less prevalent and less prominent with increasing age (Wiener et al., 1966; Eeg-Olofsson, 1971; Eeg-Olofsson et al., 1971; Kellaway, 1979; Kellaway, 1990). They do not, however, typically occur in bilaterally synchronous rhythmic trains.

Previously reported series have found activity that corresponds to the phi rhythm only in patients younger than 16 years (Rossler and Spicakova, 1966; Belsh et al., 1983; PeBenito et al., 1983). We also found a definite age preponderance. The median ages in our series were 9.5 years in group 1 and 10.0 years in group 2. However, the phenomenon occasionally occurs in adults. It seems likely, however, that the phi rhythm in adults represents persistence from earlier in life rather than appearance de novo in adulthood. In one of our patients, the phi rhythm was first noted at age 13 years and persisted in the most recent follow-up recording at age 23 years.

The mechanism responsible for generating the phi rhythm is not evident from our study because gross pathologic lesions were uncommon and there was no common thread to link the varied clinical conditions that were associated with the phi rhythm. The close resemblance to the type of activity frequently encountered with deep-seated intracranial lesions suggests that subcortical nuclei are involved, and the slow waves resulting from such lesions

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are more likely to be posteriorly predominant in children (Goldensohn, 1979). The occipital intermittent delta activity is not usually limited to the act of eye closure. Aird and Gastaut (1959) proposed subcortical "pacemaker" mechanisms for the "slow posterior rhythm associated with petit mal," which the phi so closely resembles, and both of these rhythms are typically un associated with occipital cortical lesions. Gloor et al. (1968) found that intermittent bursts of slow wave activity are usually associated with conditions involving both cortical and subcortical gray matter. An important relationship of the phi rhythm to ascending brain stem reticular and thalamocortical projection systems is suggested by the prevalence during wakefulness, the frequent occurrence after hyperventilation, which is a nonspecific activator primarily at the subcortical level (Sherwin, 1984), and its propensity to occur in patients with generalized rather than partial epilepsy. The relationship with concentrated visual attention, however, supports the importance of central vision, the occipital regions and visual association areas, and subcortical structures in its pathogenesis. The act of eye closure involves complex mechanisms, including change in illumination, pattern withdrawal, and motor activity (Naquet et aI., 1976; Newmark and Penry, 1979). The macula has a large cortical representation, and its cortical input is known to be of importance in scotosensitivity epilepsy (Panayiotopoulos, 1981; Lugaresi et aI., 1984) and in eyelid closure (fixation-off-sensitive) epilepsy (Panayiotopoulos, 1987). In these cases, it is the visual input to the macula region which creates the effect, rather than the act of fixation or eye movement (Panayiotopoulos, 1987). In other patients, however, the triggering of spikes by blinking (in the light or dark) supports motor pathway involvement in some patients (Nadkarni et aI., 1994). In view of the importance of visual attention in our patients, the visual pathways are likely to be the most important for the generation of the phi rhythm.

Finally, although the exact generating mechanisms are uncertain, we can conclude that the phi rhythm is an unusual age-related phenomenon that has no significance for the diagnosis of structural cerebral lesions or the diagnosis of epilepsy. In patients with the phi rhythm who have epilepsy, the seizure disorder is more likely to be generalized than partial.

References

Aird, RB. and Gastaut, Y. (1959) Occipital and posterior electroencephalographic rhythms. Electroenceph. clin. Neurophysiol., 11: 637- 656.

Belsh, I.M., Chokroverty, S. and Barabas, G. (1983) Posterior rhythmic slow activity in EEG after eye closure. Electroenceph. clin. Neurophysiol., 56: 562-568.

Crighel, E. (1963) The EEG activating phenomenon on closing the eyes (abstract). Electroenceph. c1in. Neurophysio!., 15: 531.

Dutertre, F. (1977) Catalogue of the main EEG patterns. In: A. Remand (Ed.), Handbook of Electroencephalography and Clinical Neurophysiology, Vol. 2, Part A. Elsevier Scientific Publishing Company, Amsterdam, p. 65.

Eeg-Olofsson, O. (1971) The development of the electroencephalogram in normal adolescents from the age of 16 through 21 years. Neuropadiatrie, 3: 11-45.

Eeg-Olofsson, 0., Petersen, I. and Sellden, U. (1971) The development of the electroencephalogram in normal children from the age of 1 through 15 years. Paroxysmal activity. Neuropadiatrie, 2: 375-404.

Gastaut, H., Trevisan, C. and Naquet, R (1958) Diagnostic value of electroencephalographic abnormalities provoked by intermittent photic stimulation (abstract). Electroenceph. c1in. Neurophysiol., 10: 194- 195.

Gloor, P., Kalabay, O. and Giard, N. (1968) The electroencephalogram in diffuse encephalopathies: electroencephalographic correlates of grey and white matter lesions. Brain, 91: 779-802.

Goldensohn, E.S. (1979) Use of the EEG for evaluation of focal intracraniallesions. In: D.W. Klass and D.D. Daly (Eds.), Current Practice of Clinical Electroencephalography. Raven Press, New York, pp. 307- 341.

Holmes, G.L., McKeever, M. and Adamson, M. (1987) Absence seizures in children: clinical and electroencephalographic features. Ann. Neurol., 21: 268-273.

Johnson, D.A., Klass, D.W. and Millichap, J.G. (1964) Electroencephalogram in Sydenham's chorea. Arch. Neurol., 10: 21-27.

Kellaway, P. (1979) An orderly approach to visual analysis: parameters of the normal EEG in adults and children. In: D.W. Klass and D.D. Daly (Eds.), Current Practice of Clinical Electroencephalography. Raven Press, New York, pp. 69-147.

Kellaway, P. (1990) An orderly approach to visual analysis. Characteristics of the normal EEG of adults and children. In: D.D. Daly and T.A. Pedley (Eds.), Current Practice of Clinical Electroencephalography (Znd Edn.). Raven Press, New York, pp. 139-199.

Lugaresi, E., Cirignotta, F. and Montagna, P. (1984) Occipital lobe epilepsy with scotosensitive seizures: the role of central vision. Epilepsia, 25: 115-120.

Nadkarni, M.A., Postolache, V., Gold, A. and Labar, D.R (1994) Central mid-temporal spikes triggered by blinking. Electroenceph. c1in. Neurophysiol., 90: 36-39.

Naquet, R, Bancaud, J., Bostem, F., Fischer-Williams, M., Gloor, P., Klass, D.W. and Kugler, J. (1976) Sensory stimulation, sleep and sleep deprivation. In: A. Remond (Ed.), Handbook of Electroencephalography and Clinical Neurophysiology, Vol. 3, Part D. Elsevier Scientific Publishing Company, Amsterdam, p. 21.

Newmark, M.E. and Penry, J.K. (1979) Photosensitivity and Epilepsy: A Review. Raven Press, New York, pp. 33-38.

Panayiotopoulos, c.P. (1981) Inhibitory effect of central vision on occipital lobe seizures. Neurology, 31: 1330-1333.

Panayiotopoulos, C.P. (1987) Fixation-oft-sensitive epilepsy in eyelid myoclonia with absence seizures. Ann. Neurol., 22: 87-89.

PeBenito, R., Cracco, J.B., Raymond, C.O. and Knobler, R (1983) The clinical significance of paroxysmal rhythmic posterior slow patterns (abstract). Electroenceph. c1in. Neurophysiol., 56: 1OP.

Rossler, M. and Spicakova, V. (1966) The phenomenon of episodic delta waves after closing the eyes (abstract). Electroenceph. c1in. Neurophysio!., 20: 282.

Sherwin, I. (1984) Hyperventilation: mode of action and application in electroencephalography. Am. J. EEG Techno!., 24: 201-211.

Stevens, J.R. (1962) Control and peripheral factors in epileptic discharge.

Clinical studies. Arch. Neurol., 7: 330-338.

Westmoreland, B.F. and Klass, D.W. (1990) Unusual EEG patterns. J.

Clin. Neurophysiol., 7: 209-228.

Wiener, J.M., Delano, J.G. and Klass, D.W. (1966) An EEG study of delinquent and nondelinquent adolescents. Arch. Gen. Psychiatry, 15: 144-150.