Brain Topography

, Volume 30, Issue 3, pp 390–407 | Cite as

Hemodynamic Changes Associated with Interictal Spikes Induced by Acute Models of Focal Epilepsy in Rats: A Simultaneous Electrocorticography and Near-Infrared Spectroscopy Study

  • Viktoriya Osharina
  • Ardalan Aarabi
  • Mana Manoochehri
  • Mahdi Mahmoudzadeh
  • Fabrice Wallois
Original Paper

Abstract

Interictal spikes can be generated by blocking GABAA receptor-mediated inhibition. The nature of the hemodynamic activities associated with interictal spikes in acute models of focal epilepsy based on GABA deactivation has not been determined. We analyzed systemic changes in hemodynamic signals associated with interictal spikes generated by acute models of focal epilepsy. Simultaneous ElectroCorticoGraphy (ECoG) and Near-InfraRed Spectroscopy (NIRS) recordings were obtained in vivo from adult Sprague–Dawley rat brain during semi-periodic focal interictal spikes induced by local cortical application of low doses of Penicillin G (PG) and Bicuculline Methiodide (BM) as GABA deactivation agents. The Finite Impulse Response deconvolution technique was used to estimate the profile of hemodynamic changes in oxyhemoglobin (HbO) and deoxyhemoglobin (HbR) concentrations associated with interictal ECoG spikes in each rat. Our results show that, in both acute models of focal epilepsy, the hemodynamic changes associated with interictal spikes were characterized by pre-spike and post-spike primary NIRS responses, and recovery periods with slight differences in amplitude and latency. The pre-spike period starting at least 2 s prior to the onset of ECoG spikes was characterized by a significant decrease in HbO concomitant with an increase in HbR with respect to baseline. The post-spike primary NIRS response exhibited the expected changes described according to the classical view of neurovascular coupling, i.e., a significant increase in HbO and a significant decrease in HbR in response to interictal spikes. The recovery period was characterized by a decreased HbO signal and an increased HbR signal, followed by a return to baseline. Compared to the BM epilepsy model, the PG model was more stable and showed lower variability in the shape, amplitude and latency of the components of spike-related hemodynamic changes. Our findings support a prominent role for pre-spike hemodynamic changes in the initiation of interictal spikes. The mechanism of interactions between neuronal and vascular networks during the pre-spike period constitutes a complex process, resulting in increased sensitivity of the epileptogenic focus to induce neuronal spiking.

Keywords

Electrocorticography Near-infrared spectroscopy Epilepsy Interictal spike Rats Neurovascular coupling GABA deactivation 

Abbreviations

ECoG

ElectroCorticoGraphy

NIRS

Near-InfraRed Spectroscopy

HbO

Oxyhemoglobin

HbR

Deoxyhemoglobin

HbT

Total hemoglobin

BM

Bicuculline Methiodide

PG

Penicillin G sodium

Notes

Acknowledgements

The Project was funded by the Picardy regional council and the European Regional Development Fund (ERDF). We thank Dr. Saul for his assistance in reviewing the paper.

Compliance with Ethical Standards

Conflict of interest

None of the authors have any conflicts of interest to disclose. We confirm that we have read the Journal’s position on issues involved in ethical publication and affirm that this report is consistent with those guidelines.

Supplementary material

10548_2016_541_MOESM1_ESM.docx (272 kb)
Figure S1. Examples of ECoG/NIRS data. Forty seconds of ECoG data with spikes (channel C3, ipsilateral, filtered between 0.5 Hz – 100 Hz) and the corresponding NIRS signals (HbO/HbR, filtered between 0.001 Hz – 78 Hz) collected from rat 1 in the BM model. Data were low-pass filtered below the Nyquist frequency (78 Hz, half of the sampling frequency). HbO: oxyhemoglobin, HbR: deoxyhemoglobin (DOCX 271 KB)
10548_2016_541_MOESM2_ESM.docx (4 mb)
Figure S2. Time-course of ECoG spikes and their corresponding HbO and HbR on the ipsilateral and contralateral sides for Rats 1-8 included in the BM model. Spike amplitudes and their corresponding HbO and HbR changes have been normalized to their maximum values on the ipsilateral side. HbO: oxyhemoglobin, HbR: deoxyhemoglobin (DOCX 4078 KB)
10548_2016_541_MOESM3_ESM.docx (7.2 mb)
Figure S3. Time-course of ECoG spikes and their corresponding HbO and HbR on the ipsilateral and contralateral sides for Rats 1-13 included in the PM model. Spike amplitudes and their corresponding HbO and HbR changes have been normalized to their maximum values on the ipsilateral side. HbO: oxyhemoglobin, HbR: deoxyhemoglobin (DOCX 7322 KB)
10548_2016_541_MOESM4_ESM.docx (24 kb)
(DOCX 24 KB)
10548_2016_541_MOESM5_ESM.docx (29 kb)
(DOCX 29 KB)

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Copyright information

© Springer Science+Business Media New York 2017

Authors and Affiliations

  • Viktoriya Osharina
    • 1
    • 4
  • Ardalan Aarabi
    • 1
    • 3
  • Mana Manoochehri
    • 1
  • Mahdi Mahmoudzadeh
    • 1
    • 2
  • Fabrice Wallois
    • 1
    • 2
  1. 1.GRAMFC-Inserm U1105University Research Center (CURS), CHU SITE SUDAmiensFrance
  2. 2.EFSN Pediatric (Pediatric Nervous System Functional Investigations Unit), CHU AMIENS - SITE SUDAmiensFrance
  3. 3.Faculty of MedicineUniversity of Picardie Jules VerneAmiensFrance
  4. 4.GRAMFC, Inserm U 1105Centre Universitaire de Recherches en Santé (CURS) CHU AMIENS - SITE SUDAmiensFrance

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