Abstract
While it is known that cortical sensory dysfunction may occur in focal neocortical epilepsy, it is unknown whether sensory-evoked neurovascular coupling is also disrupted during epileptiform activity. Addressing this open question may help to elucidate both the effects of focal neocortical epilepsy on sensory responses and the neurovascular characteristics of epileptogenic regions in sensory cortex. We therefore examined bilateral sensory-evoked neurovascular responses before, during, and after 4-aminopyridine (4-AP, 15 mmol/L, 1 μL) induced focal neocortical seizures in right vibrissal cortex of the rat. Stimulation consisted of electrical pulse trains (16 seconds, 5 Hz, 1.2 mA) presented to the mystacial pad. Consequent current-source density neural responses and epileptic activity in both cortices and across laminae were recorded via two 16-channel microelectrodes bilaterally implanted in vibrissal cortices. Concurrent two-dimensional optical imaging spectroscopy was used to produce spatiotemporal maps of total, oxy-, and deoxy-hemoglobin concentration. Compared with control, sensory-evoked neurovascular coupling was altered during ictal activity, but conserved postictally in both ipsilateral and contralateral vibrissal cortices, despite neurovascular responses being significantly reduced in the former, and enhanced in the latter. Our results provide insights into sensory-evoked neurovascular dynamics and coupling in epilepsy, and may have implications for the localization of epileptogenic foci and neighboring eloquent cortex.
Highlights
Cortical responses to sensory stimuli may be altered in focal neocortical epilepsy.[1,2] In occipital lobe epilepsy, regions of visual cortical dysfunction ipsilateral to the epileptogenic region can be identified using functional magnetic resonance imaging.[3]
The key findings of this study were the following: (1) sensoryevoked neurovascular coupling in the seizure onset zone (SOZ) is modified during focal ictal-like discharges, (2) induction and persistence of seizure activity after injection of 4-AP produces marked increases in Hbt, HbO, and a decrease in Hbr concentration, in addition to polyphasic alterations underlying each ictal event, (3) sensory-evoked neurovascular responses are significantly reduced in vibrissal cortex ipsilateral to SOZ, and reciprocally enhanced in contralateral vibrissal cortex
We have shown there to be a divergence from linearity in the sensory-evoked neurovascular coupling relationship in the SOZ during 4-AP-induced ictal discharges
Summary
Cortical responses to sensory stimuli may be altered in focal neocortical epilepsy.[1,2] In occipital lobe epilepsy, regions of visual cortical dysfunction ipsilateral to the epileptogenic region can be identified using functional magnetic resonance imaging (fMRI).[3]. Whether debilitated sensory-evoked neurovascular coupling is a feature of epileptogenic zones in sensory regions, and whether recurrent seizure activity produces enduring effects on neurovascular responses, both ipsilateral and contralateral to the SOZ, remain unexplored. Evaluation of sensory-evoked neurovascular responses in anesthetizedrodent models can offer valuable insights into the nature of neurovascular coupling, and guide refinement of mathematical models that enable interpretation of perfusion-based imaging signals in terms of underlying neuronal activity.[5,6,7,8,9,10,11] Assessment of neural and hemodynamic responses to sensory stimulation before, during, and after epileptiform activity can interrogate the stability of neurovascular coupling mechanisms in epilepsy, which have been recently suggested to be altered in acute models.[12,13] This remains an important question, as a detailed understanding of neurovascular coupling is crucial to the correct interpretation of perfusion-related imaging signals in epilepsy, such as blood oxygen level-dependent (BOLD) fMRI, that are increasingly used during presurgical evaluation of intractable epilepsy, and which typically assume linearity in neurovascular coupling.[14]
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