Intracranial Electroencephalography Reveals Selective Responses to Cognitive Stimuli in the Periventricular Heterotopias

Abstract

Our recent work suggests that non-lesional epileptic brain tissue is capable of generating normal neurophysiological responses during cognitive tasks, which are then seized by ongoing pathologic epileptic activity. Here, we aim to extend the scope of our work to epileptic periventricular heterotopias (PVH) and examine whether the PVH tissue also exhibits normal neurophysiological responses and network-level integration with other non-lesional cortical regions. As part of routine clinical assessment, three adult patients with PVH underwent implantation of intracranial electrodes and participated in experimental cognitive tasks. We obtained simultaneous recordings from PVH and remote cortical sites during rest as well as controlled experimental conditions. In all three subjects (two females), cognitive experimental conditions evoked significant electrophysiological responses in discrete locations within the PVH tissue that were correlated with responses seen in non-epileptic cortical sites. Moreover, the responsive PVH sites exhibited correlated electrophysiological activity with responsive, non-lesional cortical sites during rest conditions. Taken together, our work clearly demonstrates that the PVH tissue may be functionally organized and it may be functionally integrated within cognitively engaged cortical networks despite its anatomic displacement during neurodevelopment.

Periventricular nodular heterotopia is functionally coupled with the neocortex during resting and task states

“…non-epileptic tissues) during a cognitive task. 17 In the current study, we further confirm their findings by revealing that the PVNH tissue shows visual evoked responses as well as inter-areal coupling with neocortex during the visual task state .…”

“…This assumption is supported by subsequent fMRI and sEEG studies which reveal that the PVNH tissue is activated during multiple cognitive tasks. 12,17 In the current study, we additionally probed the relationship between the activities in the PVNH tissue and visual cortex by measuring the peak latencies. Interestingly, no significant difference between the two response latencies was found, in neither the MEG nor the sEEG visual experiment.…”

“…11,31 However, a recent perspective suggested that there may exist two PVNH-cortical networks, where epileptic tissues in PVNH are connected to epileptic cortical areas, 7,32 while non-epileptic tissues in PVNH are connected to cognitive cortical networks. 17 Using sEEG recordings, it was shown that only a portion of recording sites within PVNH tissues generated normal physiological responses and connected to the neocortex (i.e. non-epileptic tissues) during a cognitive task.…”

“…In a recent study, using stereo-electroencephalography (sEEG) recordings, it was shown that PVNH tissues not only exhibited spontaneous activities which were correlated to the neocortex, but also generated normal physiological responses during a cognitive task in three patients. 17 Although this landmark study suggested a functional involvement of the PVNH tissue, due to the sparseness of sEEG sampling, we are still unclear whether and how neurons in the PVNH tissue functionally communicate with neurons in the neocortex over a wide spatial range, which limits our understanding of the potential cognitive relevance of PVNH neurons.…”

BrainQuake: An Open-Source Python Toolbox for the Stereoelectroencephalography Spatiotemporal Analysis

“…Neural activities before the resection surgery are recorded with SEEG electrodes for EZ localization and lesion analysis, usually lasting for 2 weeks. The neural activity acquired during the 2-week SEEG recording is vital to the presurgical planning (Cossu et al, 2015) and of great value to brain research (Zhang et al, 2019;Akkol et al, 2021). However, exploiting the large number of multimodal neurodata and managing them effectively remain a problem to be solved.…”