Single-pulse electrical stimulation methodology in freely moving rat

Gronlier, Eloïse; Vendramini, Estelle; Volle, Julien; Woźniak-Kwaśniewska, Agata; Santos, Noelia Antón; Coizet, Véronique; Duveau, Venceslas; David, Olivier

doi:10.1016/j.jneumeth.2021.109092

Cited by 6 publications

(11 citation statements)

References 33 publications

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“…We know that 6-OHDA animals already produce aberrant beta oscillations in the cortical basal ganglia loop (Mallet et al 2008;Avila et al 2010;Beck et al 2016;. Additionally, our stimulation methodology induced evoked oscillations mainly in the beta band in control animals (Gronlier et al 2021). We hypothesize that brain oscillations of 6-OHDA animals are exacerbated in this frequency band, mimicking the clinical observations (Kuhn et al 2006;Kuhn et al 2009).…”

Section: Injection-free Recordingsmentioning

confidence: 83%

“…First, we wanted to detect the differences of evoked responses in injection-free condition between the 6-OHDA and sham animals from a two-level random-effect analysis of timefrequency of SPES power. To do so, the specific LFP spectral response for each stimulated structure was identified at the group level using a tailored statistical analysis, which implemented a random-effect group analysis as previously described in (Gronlier et al 2021).…”

Section: Injection-free Recordingsmentioning

confidence: 99%

“…Neurophysiological procedures are shortly presented here (see Supplementary Information for details). We used the same approach that we detailed in a previous methodological report (Gronlier et al 2021). DES was performed alternatively for each intracerebral site by stimulating between the intracerebral electrode and the ground located over the cerebellum.…”

Section: Des and Lfp Recordingsmentioning

confidence: 99%

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Evoked responses to single pulse electrical stimulation demonstrate impaired striatal excitability in a rodent model of Parkinson’s disease

Gronlier

Volle²,

Coizet

et al. 2022

Preprint

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Background: Sensorimotor beta oscillations are increased in Parkinson’s disease (PD) due to the alteration of dopaminergic transmission. This electrophysiological read-out is reported both in patients and in animal models such as the 6-OHDA rat model obtained with unilateral nigral injection of 6-hydroxydopamine (6-OHDA). Current treatments, based on dopaminergic replacement, transiently normalize this pathological beta activity and improve patients’ quality of life. Objectives: We wanted to assess in vivo whether the abnormal beta oscillations can be directly linked to the striato-cortical excitability of the sensorimotor system and whether it is modulated by the pharmacological manipulation of the dopaminergic system. Methods: In the unilateral 6-OHDA rat model and control animals, we used intra-striatal and intra-cortical single-pulse electrical stimulation (SPES) and concurrent local field potentials (LFP) recordings. In the two groups, we quantified basal cortico-striatal excitability from time-resolved spectral analyses of LFP evoked responses induced remotely by intracerebral stimulations. The temporal dependance of cortico-striatal excitability to dopaminergic transmission was further tested using electrophysiological recordings combined with levodopa injection. Results: LFP evoked responses after striatal stimulation showed a transient reduction of power in a large time-frequency domain in the 6-OHDA group compared to the sham group. This observation is specific to the striatum, as no significant difference was observed in cortical LFP evoked responses between the two groups, and corresponds to an impaired striatal excitability in the 6-OHDA group compared to the controls. This PD-specific effect was observed in the striatum at least during the first 3 months after the lesion. In addition, the striatum responses to SPES during a levodopa challenge showed a transient potentiation of the decrease of responsiveness in frequencies below 40 Hz. Conclusion: The spectral properties of striatal responses to SPES show high sensitivity to dopaminergic transmission in the unilateral 6-OHDA rat model. We thus propose that this approach could be used in preclinical models as a time-resolved biomarker of impaired dopaminergic transmission capable of monitoring progressive neurodegeneration and/or challenges to drug intake.

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Section: Injection-free Recordingsmentioning

confidence: 83%

Section: Injection-free Recordingsmentioning

confidence: 99%

Section: Des and Lfp Recordingsmentioning

confidence: 99%

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Evoked responses to single pulse electrical stimulation demonstrate impaired striatal excitability in a rodent model of Parkinson’s disease

Gronlier

Volle²,

Coizet

et al. 2022

Preprint

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“…Because the sensitivity of measurements is critical for monitoring early brain changes induced by PD, as well as brain responses to medication, we wanted here to evaluate whether the responses to direct electrical stimulations (DES) could bring new insights for the preclinical screening of drug effects. To this end, we used a methodology we recently developed that demonstrated very high signal to noise ratio and interindividual reproducibility ( Gronlier et al, 2021 ). This approach is very similar to the stimulation protocol used during presurgical evaluations in patients with refractory epilepsy ( David et al, 2010 ).…”

Section: Introductionmentioning

confidence: 99%

Evoked responses to single pulse electrical stimulation reveal impaired striatal excitability in a rat model of Parkinson's disease

Gronlier,

Volle,

Coizet

et al. 2023

Neurobiology of Disease

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“…Single pulse electrical stimulation (SPES) often evokes negative electrical potential responses in directly connected regions within 50 ms (N1), which has been related to direct cortico-cortical projections (Keller et al, 2014). Recent work has highlighted how the focus on early responses has left out components with different timescales and morphologies (Gronlier et al, 2021;Miller et al, 2021), crucial to unriddling complex cortico-subcortical pathways. Given the important role of the limbic system in neurological diseases, understanding its stimulation-driven features can help advance technologies that target this system.…”

Section: Introductionmentioning

confidence: 99%

Signatures of electrical stimulation driven network interactions in the human limbic system

Valencia

Gregg

Worrell

et al. 2022

Preprint

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Stimulation-evoked signals are starting to be used as biomarkers to indicate the state and health of brain networks. The human limbic network, often targeted for brain stimulation therapy, is involved in emotion and memory processing. Previous anatomical, neurophysiological, and functional studies suggest distinct subsystems within the limbic network (Rolls, 2015). Previous studies using intracranial electrical stimulation, however, have emphasized the similarities of the evoked waveforms across the limbic network. We test whether these subsystems have distinct stimulation-driven signatures. In seven patients with drug-resistant epilepsy, we stimulated the limbic system with single-pulse electrical stimulation (SPES). Reliable cortico-cortical evoked potentials (CCEPs) were measured between the hippocampus and the posterior cingulate cortex (PCC) and between the amygdala and the anterior cingulate cortex (ACC). However, the CCEP waveform in the PCC after hippocampal stimulation showed a unique and reliable morphology, which we term the limbic H-wave. This limbic H-wave was visually distinct and separately decoded from the amygdala to ACC waveform. Diffusion MRI data show that the measured endpoints in the PCC overlap with the endpoints of the parolfactory cingulum bundle rather than the parahippocampal cingulum, suggesting that the limbic H-wave may travel through the fornix, mammillary bodies, and the anterior nucleus of the thalamus (ANT). This was further confirmed by stimulating the ANT, which evoked the same limbic H-wave but with a shorter latency. Limbic subsystems have unique stimulation-evoked signatures that may be used in the future to help develop stimulation therapies.

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Single-pulse electrical stimulation methodology in freely moving rat

Cited by 6 publications

References 33 publications

Evoked responses to single pulse electrical stimulation demonstrate impaired striatal excitability in a rodent model of Parkinson’s disease

Evoked responses to single pulse electrical stimulation demonstrate impaired striatal excitability in a rodent model of Parkinson’s disease

Evoked responses to single pulse electrical stimulation reveal impaired striatal excitability in a rat model of Parkinson's disease

Signatures of electrical stimulation driven network interactions in the human limbic system

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