Impaired consciousness during temporal lobe seizures is related to increased long-distance cortical–subcortical synchronization

Abstract

Loss of consciousness (LOC) is a dramatic clinical manifestation of temporal lobe seizures. Its underlying mechanism could involve altered coordinated neuronal activity between the brain regions that support conscious information processing. The consciousness access hypothesis assumes the existence of a global workspace in which information becomes available via synchronized activity within neuronal modules, often widely distributed throughout the brain. Re-entry loops and, in particular, thalamo-cortical communication would be crucial to functionally bind different modules together. In the present investigation, we used intracranial recordings of cortical and subcortical structures in 12 patients, with intractable temporal lobe epilepsy (TLE), as part of their presurgical evaluation to investigate the relationship between states of consciousness and neuronal activity within the brain. The synchronization of electroencephalography signals between distant regions was estimated as a function of time by using non-linear regression analysis. We report that LOC occurring during temporal lobe seizures is characterized by increased long-distance synchronization between structures that are critical in processing awareness, including thalamus (Th) and parietal cortices. The degree of LOC was found to correlate with the amount of synchronization in thalamo-cortical systems. We suggest that excessive synchronization overloads the structures involved in consciousness processing, preventing them from treating incoming information, thus resulting in LOC.

Functional Networks in Temporal-Lobe Epilepsy: A Voxel-Wise Study of Resting-State Functional Connectivity and Gray-Matter Concentration

“…There is a large body of evidence supporting the role of the thalamus in TLE, specifically in the secondary generalization of seizures Englot et al, 2010;Norden and Blumenfeld, 2002;Yu and Blumenfeld, 2009). Synchronous electrical activity in the thalamus and temporal lobes during temporal lobe seizures were found using intracerebral electrical recordings (Arthuis et al, 2009;Guye et al, 2006). The degree of synchrony was related to the loss of consciousness and inversely related to better surgical outcome (Guye et al, 2006).…”

“…Wholebrain connectivity to the left hippocampus (LH) was chosen, as this structure is highly implicated in the origination of seizure activity in patients with LTLE. Whole-brain connectivity to the left thalamus (Lthal) was also considered, as it is highly implicated as a component of the epileptogenic network; studies across several imaging modalities have observed abnormal activity in the thalamus during seizures and loss of consciousness in patients with TLE (Arthuis et al, 2009;Blumenfeld et al, 2004;Henry et al, 1993;Morgan et al, 2010;Newberg et al, 2000;Yune et al, 1998). We hypothesized that within the LTLE patient group, decreases in GMC would be associated with changes in functional connectivity from both the hippocampus and the thalamus to affected regions in the epileptic network.…”

Permittivity Coupling across Brain Regions Determines Seizure Recruitment in Partial Epilepsy

“…1A; Talairach and Bancaud, 1966;Spencer, 2002). Partial seizures can be asymptomatic (Cook et al, 2013), and their spread to downstream brain regions is often linked to the emergence of clinical symptoms (Bonini et al, 2014), including cognitive impairment and loss of consciousness (Arthuis et al, 2009;Bartolomei and Naccache, 2011). How brain areas are recruited during seizure propagation is not well understood.…”

Altered thalamocortical rhythmicity and connectivity in mice lacking Ca V 3.1 T-type Ca 2+ channels in unconsciousness

“…From a functional perspective, abnormal slow cortical rhythms and their synchronized network dynamics are omnipresent correlates of unconscious states, such as coma and general anesthesia (3,4). Moreover, a dynamic alteration of coherence as well as coupling/uncoupling in thalamocortical circuits also can be characterized as likely correlates of unconsciousness (3)(4)(5).…”