Inactivation of the Somatosensory Cortex Prevents Paroxysmal Oscillations in Cortical and Related Thalamic Neurons in a Genetic Model of Absence Epilepsy

Polack, Pierre-Olivier; Mahon, Séverine; Chávez, Mario; Charpier, Stéphane

doi:10.1093/cercor/bhn237

Cited by 110 publications

(129 citation statements)

References 61 publications

(112 reference statements)

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“…However, oscillations may be initiated in the cortex and propagated to the thalamus, which then sends oscillations back to the cortex, thus increasing the cortico-thalamo-cortical resonance (36). This is in agreement with findings in rats, which have spike-and-wave discharges originating from SIo, and then propagating to the thalamus (37). Alternatively, our results may instead represent a direct interaction between MIo and SIo.…”

Section: Discussionsupporting

confidence: 91%

Primary motor and sensory cortical areas communicate via spatiotemporally coordinated networks at multiple frequencies

Arce-McShane

Ross

Takahashi

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Skilled movements rely on sensory information to shape optimal motor responses, for which the sensory and motor cortical areas are critical. How these areas interact to mediate sensorimotor integration is largely unknown. Here, we measure intercortical coherence between the orofacial motor (MIo) and somatosensory (SIo) areas of cortex as monkeys learn to generate tongue-protrusive force. We report that coherence between MIo and SIo is reciprocal and that neuroplastic changes in coherence gradually emerge over a few days. These functional networks of coherent spiking and local field potentials exhibit frequency-specific spatiotemporal properties. During force generation, theta coherence (2-6 Hz) is prominent and exhibited by numerous paired signals; before or after force generation, coherence is evident in alpha (6-13 Hz), beta (15-30 Hz), and gamma (30-50 Hz) bands, but the functional networks are smaller and weaker. Unlike coherence in the higher frequency bands, the distribution of the phase at peak theta coherence is bimodal with peaks near 0°and ±180°, suggesting that communication between somatosensory and motor areas is coordinated temporally by the phase of theta coherence. Time-sensitive sensorimotor integration and plasticity may rely on coherence of local and large-scale functional networks for cortical processes to operate at multiple temporal and spatial scales.S ynchrony between cortical areas has been implicated in neuronal communication and plasticity (1-4). Sensorimotor integration and formation of motor memories during learning are examples wherein effective communication between sensory and motor areas of the cerebral cortex is critical. However, very few studies have investigated coherence between the somatosensory and motor pathways in primates (5-7). These past studies have been confined to upper limb tasks, and none of them looked at changes in coherence during learning. Here, we investigated the synchronous activity between the orofacial primary motor (MIo) and somatosensory (SIo) cortical areas that play important roles in the control of orofacial behaviors (8-10). Sensorimotor control of oral behaviors is complex, involving the integration of afferent information for moving the tongue and facial muscles. Anatomical connections between MIo and SIo are dense and both areas have bilateral orofacial representations and project to brainstem cranial nerve motor nuclei containing the motoneurons projecting to jaw, facial, and tongue muscles (11,12). These connections provide a substrate for interareal communication between MIo and SIo for the control and learning of orofacial behaviors. To investigate cortico-cortical interactions between these areas, we measured coherence of spiking and local field potentials (LFPs) recorded simultaneously from MIo and SIo of the left hemisphere as monkeys learned a simple and controlled tongue protrusion task. Several studies using this behavioral paradigm have reported neuroplasticity and modulation of neuronal activity related to tongue protrusion separatel...

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Section: Discussionsupporting

confidence: 91%

Primary motor and sensory cortical areas communicate via spatiotemporally coordinated networks at multiple frequencies

Arce-McShane

Ross

Takahashi

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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“…In two genetic models of absence seizure -WAG/Rij and GAERS rats -SWD generation was found to start from the deep layers of the neocortex, specifically the somatosensory cortex (Meeren et al, 2002(Meeren et al, , 2005Polack et al, 2007). Inactivation of the somatosensory cortex abolished SWDs in GAERS rats (Polack et al, 2009). Magnetoencephalogram and functional magnetic resonance imaging support a cortical rather than thalamic initiation of SWDs in patients with absence seizures (Bai et al, 2010;Westmijse et al, 2009).…”

Section: Introductionmentioning

confidence: 87%

The hippocampus participates in a pharmacological rat model of absence seizures

Arcaro

Chu

et al. 2016

Epilepsy Research

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SUMMARYObjective-Using the gamma-butyrolactone (GBL) model of absence seizures in Long-Evans rats, this study investigated if 2.5-6 Hz paroxysmal discharges (PDs) induced by GBL were synchronized among the thalamocortical system and the hippocampus, and whether inactivation of the hippocampus affected PDs.Methods-Local field potentials were recorded by chronically implanted depth electrodes in the neocortex (frontal, parietal, visual), ventrolateral thalamus and dorsal hippocampal CA1 area. In separate experiments, multiple unit recordings were made at the hippocampal CA1 pyramidal cell layer, or the mid-septotemporal hippocampus was inactivated by local infusion of GABA A receptor agonist muscimol.Results-As PDs developed following GBL injection, coherence of local field potentials at 2.5-6 Hz increased between the hippocampus and thalamus, and between the hippocampus and the neocortex. Hippocampal theta rhythm was disrupted when GBL induced immobility in the rats. The probability of hippocampal multiple unit firing significantly increased at 40 -80 ms prior to the negative peak of thalamic PDs. Coherence between hippocampal multiple unit activity and thalamic field potentials at 2.5-6 Hz was significantly increased after GBL injection. Muscimol infusion to inactivate the mid-septotemporal hippocampus, as compared to saline infusion, significantly decreased the peak frequency of the PDs induced by GBL, decreased 30-120 Hz hippocampal gamma power, and hastened the transition of PDs to 1-2 Hz slow waves.Significance-During GBL induced 2.5-6 Hz PDs, a hallmark of absence seizure, increased synchronization between the hippocampus and the thalamocortical network was indicated by frequency and temporal correlation analysis. These results suggest that the hippocampus was entrained by thalamocortical activity in the present model of absence seizures. Prolonged synchronization of the hippocampus may result in synaptic alterations that may explain the

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“…As a result of this hyperpolarization, TC neurons of the VPM and Po respond in a burst-like pattern towards the cortical input (Crunelli and Leresche, 2002;McCormick and Bal, 1997;(Polack et al, 2009). Since TC neurons of the VPM and Po project to the somatosensory cortex, their activity "reactivates" the cortical focus and via these nuclei, provides a reverberation circuit, the cortico-thalamo-cortical network, relevant for SWD generation and maintenance.…”

Section: Brain Regions Of Interestmentioning

confidence: 99%

Upholding WAG/Rij rats as a model of absence epileptogenesis: Hidden mechanisms and a new theory on seizure development

Russo

Citraro

Constanti³

et al. 2016

Neuroscience & Biobehavioral Reviews

128

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Upholding WAG/Rij rats as a model of absence epileptogenesis: Hidden mechanisms and a new theory on seizure development.Neuroscience and Biobehavioral Reviews http://dx.doi.org/10. 1016/j.neubiorev.2016.09.017 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. AbstractThe WAG/Rij rat model has recently gathered attention as a suitable animal model of absence epileptogenesis. This latter term has a broad definition encompassing any possible cause that determines the development of spontaneous seizures; however, most of, if not all, preclinical knowledge on epileptogenesis is confined to the study of post-brain insult models such as traumatic brain injury or post-status epilepticus models. WAG/Rij rats, but also synapsin 2 knockout, Kv7 current-deficient mice represent the first examples of genetic models where an efficacious antiepileptogenic treatment (ethosuximide) was started before seizure onset. In this review, we have critically reconsidered all articles published regarding WAG/Rij rats, from the perspective that the period before SWD onset is considered as the latent period. In our new theory on seizure development, it is proposed that genes might be considered as the initial "insult" responsible for all plastic changes underpinning the development of spontaneous seizures. According to this idea, in WAG/Rij rats, genetic predisposition would lead to the development of abnormal bilateral cortical epileptic foci, which would then nongenetically stimulate the rest of the brain to rearrange networks in order to phenotypically develop seizures similarly to what happens during electrical kindling.

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Inactivation of the Somatosensory Cortex Prevents Paroxysmal Oscillations in Cortical and Related Thalamic Neurons in a Genetic Model of Absence Epilepsy

Cited by 110 publications

References 61 publications

Primary motor and sensory cortical areas communicate via spatiotemporally coordinated networks at multiple frequencies

Primary motor and sensory cortical areas communicate via spatiotemporally coordinated networks at multiple frequencies

The hippocampus participates in a pharmacological rat model of absence seizures

Upholding WAG/Rij rats as a model of absence epileptogenesis: Hidden mechanisms and a new theory on seizure development

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