Thalamocortical theta coherence in neurological patients at rest and during a working memory task

https://doi.org/10.1016/j.ijpsycho.2005.03.015Get rights and content

Abstract

We simultaneously recorded the local field potential (LFP) in the thalamus and the electroencephalogram (EEG) on the scalp of 5 patients suffering from neurogenic pain, epilepsy and movement disorders. In an earlier study [Sarnthein, J., Morel, A., von Stein, A., Jeanmonod, D., 2003. Thalamic theta field potentials and EEG: high thalamocortical coherence in patients with neurogenic pain, epilepsy and movement disorders. Thalamus Related Syst. 2, 231–238], we have investigated the slowing of EEG and the high thalamocortical coherence in the framework of thalamocortical dysrhythmia, the common underlying pathophysiology. The current study focuses on the effects of different cognitive conditions. When patients rested with eyes closed, a theta peak dominated the EEG spectra. The peak height was reduced upon opening the eyes, reminiscent of the classical alpha blocking. This peak reduction also appeared in the thalamic LFP recording. When patients activated their working memory by counting backwards, the theta peak increased in scalp EEG or in the LFP recorded in thalamic nuclei VA/VL. The coherence estimates between EEG and LFP ranged between 21% and 76% for different patients and cognitive conditions (mean: 50%). The involvement of both cortex and thalamus in working memory and the high thalamocortical coherence underline, in addition to cortico-cortical interactions, the importance of thalamocortical modules in the generation of higher cognitive functions.

Introduction

Thalamic and cortical areas are densely and reciprocally interconnected (Steriade et al., 1997, Jones, 2001) and extensive studies by in vivo techniques, in anaesthetized preparations and in awake animals have investigated the functional roles of the thalamocortical system (Llinás and Jahnsen, 1982, Steriade, 2001). At the thalamic cellular level, ionic channel properties are at the base of the appearance of specific discharge patterns. In particular, low-threshold calcium spike (LTS) bursts have been described intracellularly in in vitro and in vivo experiments and related to a state of membrane hyperpolarization (Llinás and Jahnsen, 1982, Steriade, 2001). At the network level, temporal and spatial patterns of activity in cortical and thalamic areas demonstrate wide variability, suggesting that the reverberating thalamocortical circuit supports a wide range of dynamic interactions necessary for input analysis, motor programming and cognitive functions (Llinás and Ribary, 1993, Steriade et al., 1997, Steriade, 2001, Alitto and Usrey, 2003).

Based on the above physiological evidence as well as on human thalamic unit recordings (Jeanmonod et al., 1996) and magnetoencephalographic (MEG) measurements (Llinás et al., 1999), it was proposed that a single global mechanism involving the thalamocortical reentry loop is responsible for the generation of the five domains of positive symptoms that clinically characterize the so-called thalamocortical dysrhythmia (TCD) (Llinás et al., 1999, Llinás et al., 2001, Jeanmonod et al., 2001). These domains include neurogenic pain and tinnitus, epilepsy, movement and neuropsychiatric disorders. The present study focuses on the theta activity in thalamus and cortex during cognitive tasks and the coherence between the two. In the course of surgical interventions we simultaneously measured EEG on the scalp and local field potentials (LFP) in the thalamus of patients suffering from neurogenic pain, epilepsy and movement disorders. Patients were awake and were asked either to rest with eyes open or eyes closed or to count backwards to activate their working memory (WM). In a previous publication (Sarnthein et al., 2003) we averaged over cognitive conditions and found: (1) high power in the theta frequency range of the EEG and thalamic LFP, (2) high coherence between EEG and LFP most markedly in the theta band and (3) a strong interaction between LFP theta and beta frequency bands in the bicoherence.

The present study extends those results by analyzing the cognitive conditions separately. Patients were selected from the previous group along the following criteria: (1) theta power in EEG or LFP was reduced upon opening the eyes and (2) theta power increased during WM task in EEG or LFP. These cognitive effects indicate, first, that the alpha blocking expected from the EEG of healthy subjects with eyes open (Berger, 1930) was shifted to theta frequencies in our patients. We consider this shift to be a sign of the TCD pathophysiology (Llinás et al., 1999). Second, the theta increase during WM activation occurred at the same frequency as the pathological theta. Third, the effects of cognitive condition on the LFP and the high thalamocortical coherence support an involvement of thalamic nuclei in memory functions which may also be extended to healthy subjects.

Section snippets

Patients

We analyzed spontaneous brain activity from 5 male patients suffering from chronic, severe neurological disorders, all displaying resistance to classically recognized drug treatments. Patients ranged between 22 and 68 years old. The patient group included two patients diagnosed with neurogenic pain, two patients with epilepsy and one with parkinsonian rest tremor (Table 1). Surgical procedures were described elsewhere (Jeanmonod et al., 2001). All patients gave informed consent to the

Theta dominance in power and coherence spectra

The EEG of the patients in all cognitive conditions differed from that of healthy subjects (Nunez et al., 2001) in that the dominant peak was shifted down to the theta range. EEG peak frequencies in the ec condition are given in Table 1. The LFP spectra showed a strong theta peak but they differed from EEG spectra at higher frequencies. The estimated coherence between EEG and LFP were also dominated by theta, peak values varied between 21% and 76% with a mean of 50%. Only in patient 3 were

Thalamocortical dysrhythmia

A common pathophysiology for sensory, motor and limbic positive symptoms was first evidenced in the thalamus with single unit recordings (Jeanmonod et al., 1996) and extended to the cortical level by MEG recordings (Llinás et al., 1999). On these bases the concept of thalamocortical dysrhythmia (TCD) was introduced (Llinás et al., 1999). As an anatomical basis, a thalamocortical module is sketched in Fig. 8. The specific pathway to cortical layer IV activates the apical dendrites of layer V and

Acknowledgements

We thank Universität Zürich for financial support, Paul Nunez and Hans-Georg Geissler for comments on an earlier version of the manuscript, and James Dodd for technical assistance during surgery.

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