Frequency asymmetry of sleep spindles associated with focal pathology

Frequency asymmetry of sleep spindles associated with focal pathology

Electroencephalography and clinical Neurophysiology 106 (1998) 84–86 Case report Frequency asymmetry of sleep spindles associated with focal patholo...

79KB Sizes 3 Downloads 79 Views

Electroencephalography and clinical Neurophysiology 106 (1998) 84–86

Case report

Frequency asymmetry of sleep spindles associated with focal pathology Andrew L. Reeves1, Donald W. Klass* Department of Neurology, Mayo Clinic and Mayo Foundation, Rochester, MN, USA Accepted for publication: 9 September 1997

Abstract Focal cerebral lesions are often associated with voltage asymmetry of sleep spindles, usually with depressed voltage on the side of the lesion. In this report, we document a case in which a brain tumor was associated with a frequency asymmetry in addition to a voltage asymmetry of sleep spindles. The slower frequency spindles occurred on the side of the lesion.  1998 Elsevier Science Ireland Ltd. Keywords: Electroencephalography; Frequency asymmetry; Sleep spindles; Tumor

1. Introduction Sleep spindles have long been known to constitute an essential feature of normal non-rapid eye movement (NREM) sleep in humans (Loomis et al., 1935, 1938; Davis et al., 1939). Gibbs and Gibbs (1950) divided sleep spindles into three types according to predominant frequency (14 Hz, 12 Hz, and 10 Hz) and analyzed each type according to its topography, age distribution, and level of sleep in which it appears. Sleep spindles first appear at 6–8 weeks post-term, and after about age 2, they are bilaterally synchronous and symmetrical (Kellaway, 1979). Abnormalities in spindle activity may assume several forms. Complete absence of spindle activity suggests bilateral hemispheric or diffuse cerebral disease (Kodama et al., 1979; Wiegand et al., 1991). High-voltage and prolonged spindles are usually the result of medications (Hirshkowitz et al., 1982; Johnson et al., 1983; Jobert et al., 1992a,b), but they also may be associated with mental retardation (Gibbs and Gibbs, 1962). Focal hemispheric lesions may cause voltage asymmetry of spindle activity, usually with depressed voltage on the side of the lesion (Gibbs and

* Corresponding author. Mayo Clinic, 200 First Street SW, Rochester, MN 55905, USA. 1 Present address: Department of Neurology, Ohio State University, 1654 Upham Drive, Columbus, OH 43210, USA.

0013-4694/98/$19.00  1998 Elsevier Science Ireland Ltd. All rights reserved PII S0013-4694 (97 )0 0131-4

Gibbs, 1967; Daly, 1968). Such asymmetries in voltage, or even unilateral absence, of spindles have been described in focal disorders involving the cerebral cortex, subcortical white matter, and deep gray matter structures such as the thalamus and basal ganglia (Cress and Gibbs, 1948; Silverman and Groff, 1957; Jankel and Niedermeyer, 1985; Ganji et al., 1988). In this report, we document the case of a patient in whom a hemispheric lesion produced not only voltage asymmetry but also frequency asymmetry of sleep spindles. To our knowledge, an asymmetry of spindle frequency associated with a focal lesion has not been previously described. 2. Report of case A 12 year old boy was referred for evaluation of a suspected brain tumor. He had a 1 month history of generalized headaches and partial motor seizures involving the left leg. Neurologic examination revealed a mild left hemiparesis. A computerized tomographic scan of the brain showed a contrast-enhancing infiltrating mass in the right frontal lobe involving the cerebral cortex and the subjacent white matter. Stereotactic biopsy revealed a grade 3 astrocytoma. Phenytoin and dexamethasone were administered. Before biopsy, electroencephalography (EEG) was performed with the standard 10–20 system of electrode placement. During wakefulness, the EEG contained alpha activity of 10 Hz predominant frequency, which was bilat-

EEG 97094

A.L. Reeves, D.W. Klass / Electroencephalography and clinical Neurophysiology 106 (1998) 84–86

erally symmetrical in voltage and reactivity to eye opening and mental activity. Superimposed on the alpha activity were intermittent occipital transients of 2 to 3 Hz frequency that were abolished by eye opening. Photic stimulation elicited bilateral driving responses of slightly higher amplitude on the right side. No focal epileptiform or slow-wave abnormalities were present during wakefulness. During sleep, the V waves were consistently lower in amplitude on the right side. During stage 2 sleep, the 14 Hz spindles were also reduced in voltage over the right side. In addition, 12 Hz spindles occurred over the right frontocentral region. No 12 Hz spindles were present on the left side (Fig. 1). The asymmetry of sleep spindle frequency was not present during deeper stages of NREM sleep. 3. Discussion Investigators have different opinions about the circuits that are primarily responsible for spindle activity. Some authors have found in animal experiments that spindle activity depends on intrinsic bursts of neuronal activity in the reticular nucleus of the thalamus and that severing connections between the reticular nucleus and the cerebral cortex abolishes spindle activity (Contreras et al., 1993; Contreras and Steriade, 1996). Others have suggested that the thalamocortical circuits may have a more active role in generation of spindles (Golomb et al., 1994) and that sleep spindle

85

synchrony depends on synchronous excitatory corticothalamic volleys to synchronize thalamic reticular cells within the frequency range of spindles (Steriade, 1997). Although the infiltrating nature of the lesion in our patient does not permit a precise determination of the anatomical structures involved, the findings would be consistent with a perturbation of thalamocortical and corticothalamic circuits. The voltage asymmetry of 14 Hz spindles and V waves in the sleep EEG of our patient is in accordance with the statement of Gibbs and Gibbs (1967) that a ‘difference in voltage of sleep patterns in the two hemispheres indicates damage on the side of lower voltage’. As in our patient, ipsilateral depression of spindles with cerebral lesions can occur without focal abnormalities in the waking EEG (Cress and Gibbs, 1948). Although augmentation of spindles can occur on the side of a hemispheric brain tumor, reduction of voltage is more common (Daly, 1968). One study of the EEG in patients with brain tumors found that unilateral spindle depression favored a superficial location of the tumor (Silverman and Groff, 1957). In this regard, it should be noted that the lesion in our patient was relatively superficial in the right hemisphere. However, Daly (1968) found that unilateral distortion of sleep spindles was not a reliable indicator of the cortical or subcortical location of a tumor. The frequency asymmetry of spindles in our patient is unique. The slower spindles occurred on the side of the structural lesion. In some ways, this finding is analogous to a frequency asymmetry of the alpha rhythm in which the slower frequency indicates the side of the lesion (Arfel and Fischgold, 1961; Van Huffelen et al., 1984; Markand, 1990). However, in our patient, the two frequencies of spindles occurred independently on the two sides. From the standpoint of diagnosis, if a frequency asymmetry of sleep spindles is encountered, even in the absence of other localizing or lateralizing EEG abnormality, search for a lateralized cerebral hemispheric lesion on the side of the slower frequency would be warranted.

References

Fig. 1. Frequency asymmetry of sleep spindles. EEG of a 12 year old boy during sleep showing 14 Hz frontocentral spindles on the left side and 12 Hz frontocentral spindles independently on the right side. The sharp potential in Fp2 is myogenic artifact.

Arfel, G. and Fischgold, H. EEG-signs in tumours of the brain. Electroenceph. clin. Neurophysiol., 1961, Suppl. 19: 36–50. Contreras, D. and Steriade, M. Spindle oscillation in cats: the role of corticothalamic feedback in a thalamically generated rhythm. J. Physiol. (Lond.), 1996, 490: 159–179. Contreras, D., Curro Dossi, R. and Steriade, M. Electrophysiological properties of cat reticular thalamic neurones in vivo. J. Physiol. (Lond.), 1993, 470: 273–294. Cress, C.H. and Gibbs, E.L. Electroencephalographic asymmetry during sleep (in patients with vascular and traumatic hemiplegia). Dis. Nerv. System, 1948, 9: 327–329. Daly, D.D. The effect of sleep upon the electroencephalogram in patients with brain tumors. Electroenceph. clin. Neurophysiol., 1968, 25: 521– 529. Davis, H., Davis, P.A., Loomis, A.L., Harvey, E.N. and Hobart, G. Elec-

86

A.L. Reeves, D.W. Klass / Electroencephalography and clinical Neurophysiology 106 (1998) 84–86

trical reactions of the human brain to auditory stimulation during sleep. J. Neurophysiol., 1939, 2: 500–514. Ganji, S., Duncan, M.C. and Frazier, E. Sydenham’s chorea: clinical, EEG, CT scan, and evoked potential studies. Clin. Electroencephalogr., 1988, 19: 114–122. Gibbs, F.A. and Gibbs, E.L. Atlas of Electroencephalography. Volume 1: Methodology and Controls, 2nd edn. Addison-Wesley, Cambridge, MA, 1950. Gibbs, E.L. and Gibbs, F.A. Extreme spindles: correlation of electroencephalographic sleep pattern with mental retardation. Science, 1962, 138: 1106–1107. Gibbs, F.A. and Gibbs, E.L. Medical Electroencephalography. AddisonWesley, Reading, MA, 1967. Golomb, D., Wang, X.J. and Rinzel, J. Synchronization properties of spindle oscillations in a thalamic reticular nucleus model. J. Neurophysiol., 1994, 72: 1109–1126. Hirshkowitz, M., Thornby, J.I. and Karacan, I. Sleep spindles: pharmacological effects in humans. Sleep, 1982, 5: 85–94. Jankel, W.R. and Niedermeyer, E. Sleep spindles. J. Clin. Neurophysiol., 1985, 2: 1–35. Jobert, M., Poiseau, E., Jahnig, P., Schulz, H. and Kubicki, S. Pattern recognition by matched filtering: an analysis of sleep spindle and Kcomplex density under the influence of lormetazepam and zopiclone. Neuropsychobiology, 1992a, 26: 100–107. Jobert, M., Poiseau, E., Jahnig, P., Schulz, H. and Kubicki, S. Topographical analysis of sleep spindle activity. Neuropsychobiology, 1992b, 26: 210–217. Johnson, L.C., Spinweber, C.L., Seidel, W.F. and Dement, W.C. Sleep

spindle and delta changes during chronic use of a short-acting and a long-acting benzodiazepine hypnotic. Electroencephalogr. clin. Neurophysiol., 1983, 55: 662–667. Kellaway, P. 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, 1979, pp. 69–147. Kodama, N., Aoki, Y., Hiraga, H., Wada, T. and Suzuki, J. Electroencephalographic findings in children with moyamoya disease. Arch. Neurol., 1979, 36: 16–19. Loomis, A.L., Harvey, E.N. and Hobart, G. Potential rhythms of cerebral cortex during sleep. Science, 1935, 81: 597–598. Loomis, A.L., Harvey, E.N. and Hobart, G.A. III Distribution of disturbance-patterns in human electroencephalogram, with special reference to sleep. J. Neurophysiol., 1938, 1: 413–430. Markand, O.N. Alpha rhythms. J. Clin. Neurophysiol., 1990, 7: 163–189. Silverman, D. and Groff, R.A. Brain tumor depth determination by electrographic recordings during sleep. Arch. Neurol. Psychiatr. (Chicago), 1957, 78: 15–28. Steriade, M. Neurobiologic mechanisms of sleep. In: Update on the Neurology of Sleep. American Academy of Neurology, 1997, 146-9-146-24. Van Huffelen, A.C., Poortvliet, D.C.J. and Van Der Wulp, C.J.M. Quantitative electroencephalography in cerebral ischemia. Detection of abnormalities in ‘normal’ EEGs. Prog. Brain Res., 1984, 62: 3–28. Wiegand, M., Moller, A.A., Schreiber, W., Krieg, J.C., Fuchs, D., Wachter, H. and Holsboer, F. Nocturnal sleep EEG in patients with HIV infection. Eur. Arch. Psychiatr. Clin. Neurosci., 1991, 240: 153– 158.