Studies of the EEG activity of limbic structures in man

doi:10.1016/0013-4694(68)90171-5

Electroencephalography and Clinical Neurophysiology

Volume 25, Issue 4, October 1968, Pages 309-318

https://doi.org/10.1016/0013-4694(68)90171-5 Get rights and content

Abstract

1.
1. Studies have been made of the on-going EEG activity of amygdala, hippocampus and hippocampal gyrus as recorded by implanted electrodes together with surface recordings in twenty-eight cases of temporal lobe epilepsy and two non-epileptic patients.
2.
2. A computer program has been used to determine the frequencies present in these limbic structures and elsewhere and to explore whether their wave processes share any common features.
3.
3. Strong correlations in several frequency bands were usually found between the hippocampus, hippocampal gyrus and ipsilateral amygdala. No contralateral coherences were found.
4.
4. These correlations were disrupted in stages of sleep which show slow wave or low voltage fast activity at the scalp. The wave characteristics of the limbic structures differ fundamentally in sleep from those of the scalp recordings.
5.
5. There is a stage of sleep in which marked spindling occurs in the limbic system without any representation of it at the convexity.
6.
6. Two conditions in which correlation, not usually present, are found to develop are during electrical seizure discharge in the limbic structures and after a pre-narcotic dose of barbiturates.

Résumé

1.
1. Cette étude porte sur l'activité EEG continue de l;amygdale, de l'hippocampe et de la circonvulution hippocampiqye, telle qu'elle est enregistrée par électrodes implantées simultanément á des enrigistrements en surface dans vingt-huit cas d'épilepsie du lobe temporal et chez deux patients non-épileptiques.
2.
2. Un programme d'ordinateur a été utilisé pour établir les fréquences présentes dans ces structures limbiques et ailleurs, et pour déterminer si les ondes ont des caractères communs.
3.
3. De fortes corrélations dans plusieurs bandes de fréquence ont été communément trouvées entre l'hippocampe, la circonvulution hippocampique et l'amygdale ipsilatérale. Des cohérences entre structures contralatérales ne sont pas apparues.
4.
4. Ces corrélations disparaissaient dans les stades de sommeil accompagnés par des ondes lentes ou par une activit'e rapide de bas voltage sur le scalp. Les caractérisiques des structures limbiques différent fondamentalement de celles des enrigistrement de surface au cours du sommeil.
5.
5. Il y a un stade de sommeil dans lequel des fuseaux marqués apparaissent dans le système limbique sans contrepartie équivalente sur la convexité des hémispheres.
6.
6. Deux conditions dans lesquelles des corrélations, non existantes habituellement, se développent sont: durant les décharges électroques convulsives dans les structures limbiques et après l'administration d'une dose pré-narcotique de barbiturates.

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Hippocampal spindles and barques are normal intracranial electroencephalographic entities
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Citation Excerpt :
However scalp and intracranial spindles are independent, as scalp sleep spindles are not synchronous with intracranial sigma band oscillations from various cortical and subcortical structures (Frauscher et al., 2015a). The intracranial presence of spindle activity was first identified in the human hippocampus over 50 years ago (Brazier, 1968, 1970, 1972). Although counterintuitive, the hippocampal spindles are not temporally correlated to the occurrence of scalp sleep spindles (Nakabayashi et al., 2001; Frauscher et al., 2015a), despite the fact that their morphological features of waxing and waning sinusoidal oscillation are indistinguishable.
To assess whether hippocampal spindles and barques are markers of epileptogenicity.
Focal epilepsy patients that underwent stereo-electroencephalography implantation with at least one electrode in their hippocampus were selected (n = 75). The occurrence of spindles and barques in the hippocampus was evaluated in each patient. We created pairs of pathologic and pathology-free groups according to two sets of criteria: 1. Non-invasive diagnostic criteria (patients grouped according to focal epilepsy classification). 2. Intracranial neurophysiological criteria (patient’s hippocampi grouped according to their seizure onset involvement).
Hippocampal spindles and barques appear equally often in both pathologic and pathology-free groups, both for non-invasive (P_spindles = 0.73; P_barques = 0.46) and intracranial criteria (P_spindles = 0.08; P_barques = 0.26). In Engel Class I patients, spindles occurred with similar incidence both within the non-invasive (P = 0.67) and the intracranial criteria group (P = 0.20). Barques were significantly more frequent in extra-temporal lobe epilepsy defined by either non-invasive (P = 0.01) or intracranial (P = 0.01) criteria.
Both spindles and barques are normal entities of the hippocampal intracranial electroencephalogram. The presence of barques may also signify lack of epileptogenic properties in the hippocampus.
Understanding that hippocampal spindles and barques do not reflect epileptogenicity is critical for correct interpretation of epilepsy surgery evaluations and appropriate surgical treatment selection.
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Vagal nerve stimulation (VNS) is known as an effective method of treatment in a number of neurological disorders. The low risk of side effects also makes it useful in clinical trials in other diseases. Branches of the vagal nerve innervate the anatomical structures known to be involved in memory processing. That is why it seems justified that several studies emphasize the impact of VNS on the cognitive and memory function in both healthy volunteers and patients with epilepsy and Alzheimer’s disease. Results have shown that VNS can modulate different types of memory depending the protocol of stimulation in non-demented patients after both short term and chronic VNS application. Transcutaneous vagal nerve stimulation (tVNS), which is a non-invasive method of VNS, opens up new perspectives for different clinical applications.
Multifaceted roles for low-frequency oscillations in bottom-up and top-down processing during navigation and memory
2014, NeuroImage
Citation Excerpt :
Using this method, we determined that rodent movement-related oscillations typically peaked at around 8 Hz and lasted about 4.3 cycles while those from humans peaked around 3.4 Hz and lasted typically about 2.7 cycles (Watrous et al., in press). These quantitative findings mirror previous qualitative observations in the literature suggesting human low-frequency oscillations are more transient and may peak at a lower frequency than that characterized in the rodent (Arnolds et al., 1980; Bodizs et al., 2001; Brazier, 1968; Cantero et al., 2003; Kahana et al., 1999; Lega et al., 2012). Based on these findings, we suggest several possible reasons why primate low-frequency oscillations may have been elusive in the past.
A prominent and replicated finding is the correlation between running speed and increases in low-frequency oscillatory activity in the hippocampal local field potential. A more recent finding concerns low-frequency oscillations that increase in coherence between the hippocampus and neocortical brain areas such as prefrontal cortex during memory-related behaviors (i.e., remembering the correct location to visit). In this review, we tie together movement-related and memory-related low-frequency oscillations in the rodent with similar findings in humans. We argue that although movement-related low-frequency oscillations, in particular, may have slightly different characteristics in humans than rodents, placing important constraints on our thinking about this issue, both phenomena have similar functional foundations. We review four prominent theoretical models that provide partially conflicting accounts of movement-related low-frequency oscillations. We attempt to tie together these theoretical proposals, and existing data in rodents and humans, with memory-related low-frequency oscillations. We propose that movement-related low-frequency oscillations and memory-related low-frequency oscillatory activity, both of which show significant coherence with oscillations in other brain regions, represent different facets of “spectral fingerprints,” or different resonant frequencies within the same brain networks underlying different cognitive processes. Together, movement-related and memory-related low-frequency oscillatory coupling may be linked by their distinct contributions to bottom-up, sensorimotor driven processing and top-down, controlled processing characterizing aspects of memory encoding and retrieval.
Slow EEG rhythms and inter-hemispheric synchronization across sleep and wakefulness in the human hippocampus
2012, NeuroImage
Converging data that attribute a central role to sleep in memory consolidation have increased the interest to understand the characteristics of the hippocampal sleep and their relations with the processing of new information. Neural synchronization between different brain regions is thought to be implicated in long-term memory consolidation by facilitating neural communication and by promoting neural plasticity. However, the majority of studies have focused their interest on intra-hippocampal, rhinal–hippocampal or cortico-hippocampal synchronization, while inter-hemispheric synchronization has been so far neglected.
To clarify the features of spontaneous human hippocampal activity and to investigate inter-hemispheric hippocampal synchronization across vigilance states, pre-sleep wakefulness and nighttime sleep were recorded from right and left homologous hippocampal loci using stereo-EEG techniques. Hence, quantitative and inter-hemispheric coherence analyses of hippocampal activity across sleep and waking states were carried out.
The results showed the presence of delta activity in human hippocampal spontaneous EEG also during wakefulness. The activity in the delta range exhibited a peculiar bimodal distribution, namely a low frequency non-oscillatory activity (up to 2 Hz) synchronized between hemispheres mainly during wake and REM sleep, and a faster oscillatory rhythm (2–4 Hz). The latter was less synchronized between the hippocampi and seemed reminiscent of animal RSA (rhythmic slow activity). Notably, the low-delta activity showed high inter-hemispheric hippocampal coherence during REM sleep and, to a lesser extent, during wakefulness, paralleled by a (unexpected) decrease of coherence during NREM sleep.
Therefore, low-delta hippocampal state-dependent synchronization starkly contrasts with neocortical behavior in the same frequency range. Further studies might shed light on the role of these low frequency rhythms in the encoding processes during wakefulness and in the consolidation processes during subsequent sleep.
Effect of sleep on interictal spikes and distribution of sleep spindles on electrocorticography in children with focal epilepsy
2007, Clinical Neurophysiology
Citation Excerpt :
Previous studies of adults with uncontrolled focal epilepsy demonstrated that sleep spindles can be recorded intracranially (Brazier, 1968; Montplaisir et al., 1981) and that the amplitude of sleep spindles is highest in the frontal–central region (Caderas et al., 1982). Several studies in adults have documented that sleep spindles are also present in the medial temporal region predominantly during non-REM sleep (Brazier, 1968; Montplaisir et al., 1981; Malow et al., 1999). The nature of such medial temporal spindles has not been clearly understood, and its possible association with epileptic or physiological phenomenon has been proposed (Montplaisir et al., 1981; Malow et al., 1999).
To determine how sleep with central spindles alters the spatial distribution of interictal spike frequency in children with intractable focal seizures, and whether such children have spindles arising from the medial temporal region in addition to the frontal–central region.
Seventeen children (age: 7 months–17 years) were studied using extraoperative electrocorticography (ECoG).
Overall spike frequency across the subdural electrodes was greater during sleep with central spindles compared to wakefulness. In 13 children showing at least 1 spike/min in an electrode, the spatial distribution of spike frequency was similar during wakefulness and sleep; in addition, the spike frequency was greater in the seizure onset zones compared to the non-onset areas, regardless of wakefulness or sleep. Spindles were identified in the medial temporal region during sleep with central spindles in all 17 children.
Overall spike frequency may be increased by sleep with spindles, but the spatial distribution of spike frequency appears similar during wakefulness and sleep in children with intractable focal seizures.
Both awake and sleep ECoG may be useful to predict seizure onset zones in children with intractable focal epilepsy. Medial temporal spindles are present in some children with focal epilepsy.

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¹: The work of this investigator is supported by No. 5-K6-NB-18, 608 from the National Institutes of Health, Grant No. NB 04773 from the U.S. Public Health Service, Grant No. GP 6438 from tje National Science Foundation and Contract NR-233(69) from the U.S. Office of Naval Research.

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Studies of the EEG activity of limbic structures in manÉtudes de l'EEG des structures limbiques chez l'homme

Abstract

Résumé

Electroenceph. clin. Neurophysiol.

Exp. Neurol.

Thiopental effects on subcortical mechanisms in temporal lobe epilepsy

Anesthesiology

[Electrophysiological studies of the thalamus and hippocampus in man]

Sechenov physiol. J. U.S.S.R.

Electrical activity recorded simultaneously from the scalp and deep structures of the human brain: a computer study of their relationships

J. nerv. ment. Dis.