Shedding light on interictal epileptic spikes: An in vivo study using fast optical signal and electrocorticography

Summary Objective Interictal epileptic spikes (IESs), apart from being a key marker of epileptic neuronal networks, constitute a nice model of the widespread endogenous phenomenon of neuronal hypersynchronization. Many questions concerning the mechanisms that drive neurons to hypersynchronize remain unresolved, but synaptic as well as nonsynaptic events are likely to be involved. In this study, changes in optical properties of neural tissues were observed in rats with penicillin‐induced IES using fast optical signal (FOS) concomitantly with electrocorticography (ECoG). Methods In this study, near‐infrared optical imaging was used with ECoG to investigate variations in the optical properties of cortical tissue directly associated with neuronal activity in 15 rats. FOS changes correspond to variations of scattered light from neuronal tissue when neurons are activated. To independently evaluate our method, a control experiment on somatosensory was designed and applied to seven different rats. Time‐frequency analysis was also used to track variations of (de)synchronization concomitantly with changes in optical signals during IES. Results FOS responses revealed that changes in optical signals occurred 320 msec before to 370 msec after the IES peak. These changes started before any changes in ECoG signal. In addition, time‐frequency domain electrocorticography revealed an alternating decrease‐increase‐decrease in the ECoG spectral power (pointing to desynchronization‐synchronization‐desynchronization), which occurred concomitantly with an increase‐decrease‐increase in relative optical signal during the IES. These results suggest a relationship between (de)synchronization and optical changes. Significance These changes in the neuronal environment around IESs raise new questions about the mechanisms that induce changes in optical properties of neural tissues before the IES, which may provide suitable conditions for neuronal synchronization during IESs. FOS‐ECoG constitutes a multimodal approach and opens new avenues to study the mechanisms of neuronal synchronization in the pathologic brain, which has clinical implications, at least in epilepsy.