HYPOTHESIS
The EEG Spike: Signal of Information Transmission? Janice R. Stevens, MD
Enhanced neuronal excitability or coherence, leading to a rapid-bursting m o d e of u n i t discharge or to synchronous polarization, underlies t h e electroencephalographic spike. The propensity for EEG spike activity to occur i n relation to events that require absolute command of neural circuitry suggests that the EEG spike represents a mode of discharge of underlying neural elements which is employed for communication of imperative messages. N o r m a l when confined to certain axial nuclei of the brain d u r i n g sleep or d u r i n g p h o t i c or sexual excitation, compensatory i n response to deafferentation or hypoxia, this powerful transmission m o d e must have certain advantages to have persisted t h r o u g h o u t evolutionary history. Stevens JR: The EEG spike: signal of information transmission! Ann Neurol 1:309-314, 1977
Spike activity in the electroencephalogram of man is usually considered a sign of abnormal neuronal activity characteristic of epilepsy and other pathological cerebral states. There are several situations, however, in which spike activity appears normally from the surface and depth electroencephalogram in both animals and man. Among these are the sharp, spikelike transients commonly superimposed on K complexes and delta waves of the slow-wave sleep of normal children, the 14 and 6 per second positive spikes recorded over temporal regions during light sleep in adolescents and young adults, and paroxysmal spikewave response to intense photic stimulation, found not only in patients with epilepsy but also in a small percentage of normal girls and young women. A striking feature of each of these various “normal spikes” is their relationship to chronological age, with a remarkable predilection for the periadolescent period. Desynchronized (rapid eye movement) sleep-and thus by inference the monophasic sharp waves in the EEG known as ponto-geniculateoccipital (PGO) spikes associated with this state-is also strikingly related to ontogeny and brain maturation, declining steadily from birth t o around 12 years of age in humans and similarly associated with maturation in animals [ 1, 21. The EEG spike, defined as a transient potential with rapid rise and fall over a period of 50 to 75 msec, is generally considered to represent the envelope of temporally and spatially summed synaptic events that result from synchronous activation of numerous synapses on the same neuron or group of neurons [31. The outstanding characteristic of the epileptic spike is From the Departments of Neurology and Psychiatry, University of Oregon Health Sciences Center, Portland, OR. Adapted from t h e Presidential Address to the American bhG Society, Seattle, 1973
its capacity for propagation from a primary focus to distant cortical and subcortical sites. In cbntrast, spikes associated with the physiological states of sleep do not propagate over increasingly wider areas of cerebrum but, like the single spikes of sensory evoked potentials, may reflect signal transmission by physiological synchronizatbn limited to closely associated neurons.
The Photoconvulsive Response As is evident from the occurrence ofvisually evoked potentials and photic driving in the EEG, the waking brain normally is excitable to photic stimuli. Augmentation of the photic driving response, including elicitation of paroxysmal high-voltage spike or spike-wave activity in response to regular light flashes, occurs in nearly 50% of patients with bilateral spike-wave epilepsy [4, 51. Less well known are reports from a number ofworkers that 10 to 15% ofnormal girls between the ages of 10 and 16 years, but only 1 to 2% of boys, display the photoconvulsive response (PCR) [6131. The age distribution and genetic characteristics of the PCR in the nonepileptic population are similar to those in petit ma1 epilepsy, a disorder in which the PCR is found not only in nearly 50%) of probands, but also in parents and siblings who never manifest clinical seizures. In contrast, only 3rT of patients with focal epilepsy demonstrate a paroxysmal EEG response to intermittent photic stimulation. As in the general population, age-related susceptibility is notable, with the incidence of spike-wave trait among seizure-free siblings ofpatients with petit ma1 epilepsy rising to nearly 509; between the ages of 4 5 and 16Y2 years and falling to less than 10%)by age 30 1141 (Fig 1). The remarkable susceptibility to PCR among females in early adolescence and throughout the reproductive period may relate to a sex-linked genetic trait, to sexually diAccepted for publication Oct 4. 1976. Address reprint requests to Dr Stevens, University of Oregon Health Sciences Center, Portland, OR 97201
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The EEG Spike: Signal of Information Transmission? Janice R. Stevens, MD
Enhanced neuronal excitability or coherence, leading to a rapid-bursting m o d e of u n i t discharge or to synchronous polarization, underlies t h e electroencephalographic spike. The propensity for EEG spike activity to occur i n relation to events that require absolute command of neural circuitry suggests that the EEG spike represents a mode of discharge of underlying neural elements which is employed for communication of imperative messages. N o r m a l when confined to certain axial nuclei of the brain d u r i n g sleep or d u r i n g p h o t i c or sexual excitation, compensatory i n response to deafferentation or hypoxia, this powerful transmission m o d e must have certain advantages to have persisted t h r o u g h o u t evolutionary history. Stevens JR: The EEG spike: signal of information transmission! Ann Neurol 1:309-314, 1977
Spike activity in the electroencephalogram of man is usually considered a sign of abnormal neuronal activity characteristic of epilepsy and other pathological cerebral states. There are several situations, however, in which spike activity appears normally from the surface and depth electroencephalogram in both animals and man. Among these are the sharp, spikelike transients commonly superimposed on K complexes and delta waves of the slow-wave sleep of normal children, the 14 and 6 per second positive spikes recorded over temporal regions during light sleep in adolescents and young adults, and paroxysmal spikewave response to intense photic stimulation, found not only in patients with epilepsy but also in a small percentage of normal girls and young women. A striking feature of each of these various “normal spikes” is their relationship to chronological age, with a remarkable predilection for the periadolescent period. Desynchronized (rapid eye movement) sleep-and thus by inference the monophasic sharp waves in the EEG known as ponto-geniculateoccipital (PGO) spikes associated with this state-is also strikingly related to ontogeny and brain maturation, declining steadily from birth t o around 12 years of age in humans and similarly associated with maturation in animals [ 1, 21. The EEG spike, defined as a transient potential with rapid rise and fall over a period of 50 to 75 msec, is generally considered to represent the envelope of temporally and spatially summed synaptic events that result from synchronous activation of numerous synapses on the same neuron or group of neurons [31. The outstanding characteristic of the epileptic spike is From the Departments of Neurology and Psychiatry, University of Oregon Health Sciences Center, Portland, OR. Adapted from t h e Presidential Address to the American bhG Society, Seattle, 1973
its capacity for propagation from a primary focus to distant cortical and subcortical sites. In cbntrast, spikes associated with the physiological states of sleep do not propagate over increasingly wider areas of cerebrum but, like the single spikes of sensory evoked potentials, may reflect signal transmission by physiological synchronizatbn limited to closely associated neurons.
The Photoconvulsive Response As is evident from the occurrence ofvisually evoked potentials and photic driving in the EEG, the waking brain normally is excitable to photic stimuli. Augmentation of the photic driving response, including elicitation of paroxysmal high-voltage spike or spike-wave activity in response to regular light flashes, occurs in nearly 50% of patients with bilateral spike-wave epilepsy [4, 51. Less well known are reports from a number ofworkers that 10 to 15% ofnormal girls between the ages of 10 and 16 years, but only 1 to 2% of boys, display the photoconvulsive response (PCR) [6131. The age distribution and genetic characteristics of the PCR in the nonepileptic population are similar to those in petit ma1 epilepsy, a disorder in which the PCR is found not only in nearly 50%) of probands, but also in parents and siblings who never manifest clinical seizures. In contrast, only 3rT of patients with focal epilepsy demonstrate a paroxysmal EEG response to intermittent photic stimulation. As in the general population, age-related susceptibility is notable, with the incidence of spike-wave trait among seizure-free siblings ofpatients with petit ma1 epilepsy rising to nearly 509; between the ages of 4 5 and 16Y2 years and falling to less than 10%)by age 30 1141 (Fig 1). The remarkable susceptibility to PCR among females in early adolescence and throughout the reproductive period may relate to a sex-linked genetic trait, to sexually diAccepted for publication Oct 4. 1976. Address reprint requests to Dr Stevens, University of Oregon Health Sciences Center, Portland, OR 97201
309
2o
h
8
