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

J Neurosci. 2021 Apr 28;41(17):3870-3878. doi: 10.1523/JNEUROSCI.2785-20.2021. Epub 2021 Mar 16.

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.SIGNIFICANCE STATEMENT Periventricular heterotopias (PVH) are developmentally abnormal brain tissues that frequently cause epileptic seizures. In a rare opportunity to obtain direct electrophysiological recordings from PVH, we were able to show that, contrary to common assumptions, PVH functional activity is similar to healthy cortical sites during a well-established cognitive task and exhibits clear resting state connectivity with the responsive cortical regions.

Keywords: high-frequency broadband; intracranial electroencephalography; intrinsic connectivity; periventricular heterotopia; sustained attention.

Publication types

  • Case Reports
  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adolescent
  • Adult
  • Attention
  • Brain Mapping
  • Cognition*
  • Electrocorticography / methods*
  • Electrophysiological Phenomena
  • Female
  • Humans
  • Magnetic Resonance Imaging
  • Male
  • Nerve Net / physiopathology
  • Neuroimaging
  • Periventricular Nodular Heterotopia / diagnostic imaging
  • Periventricular Nodular Heterotopia / physiopathology*
  • Periventricular Nodular Heterotopia / psychology
  • Psychomotor Performance
  • Young Adult