The neural response to deep brain stimulation of the anterior nucleus of the thalamus: A MEMRI and c-Fos study

Gimenes, Christiane; Malheiros, Jackeline Moraes; Battapady, Harsha; Tannús, Alberto; Hamani, Clement; Covolan, Luciene

doi:10.1016/j.brainresbull.2019.01.011

Cited by 17 publications

(10 citation statements)

References 42 publications

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“…This new DBS apparatus allows unrestricted moving and feeding of experimental animals and delivers long-term chronic stimulation (at the effective voltage for over 3 months), which is more advantageous than the majority of previous DBS devices used for rodent models ( 32 , 33 ). We have observed that HF-DBS increases the expression of activity-dependent genes c-fos and Npas4 in the AI, which suggests our stimulation protocol modulates AI cellular activity and is in line with previous DBS studies ( 34 – 37 ).…”

Section: Discussionsupporting

confidence: 91%

Continuous High Frequency Deep Brain Stimulation of the Rat Anterior Insula Attenuates the Relapse Post Withdrawal and Strengthens the Extinction of Morphine Seeking

et al. 2020

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Deep brain stimulation (DBS) modulates the neuronal activity in specific brain circuits and has been recently considered as a promising intervention for refractory addiction. The insula cortex is the hub of interoception and is known to be involved in different aspects of substance use disorder. In the present study, we investigate the effects of continuous high frequency DBS in the anterior insula (AI) on drug-seeking behaviors and examined the molecular mechanisms of DBS action in morphine-addicted rats. Sprague-Dawley rats were trained to the morphine-conditioned place preference (CPP, day 1–8) followed by bilaterally implanted with DBS electrodes in the AI (Day 10) and recovery (Day 10–15). Continuous high-frequency (HF) -DBS (130 Hz, 150 μA, 90 μs) was applied during withdrawal (Day 16–30) or extinction sessions. CPP tests were conducted on days 16, 30, 40 during withdrawal session and several rats were used for proteomic analysis on day 30. Following the complete extinction, morphine-CPP was reinstated by a priming dose of morphine infusion (2 mg/kg). The open field and novel objective recognition tests were also performed to evaluate the DBS side effect on the locomotion and recognition memory. Continuous HF-DBS in the AI attenuated the expression of morphine-CPP post-withdrawal (Day 30), but morphine addictive behavior relapsed 10 days after the cessation of DBS (Day 40). Continuous HF-DBS reduced the period to full extinction of morphine-CPP and blocked morphine priming-induced recurrence of morphine addiction. HF-DBS in the AI had no obvious effect on the locomotor activity and novel objective recognition and did not cause anxiety-like behavior. In addition, our proteomic analysis identified eight morphine-regulated proteins in the AI and their expression levels were reversely changed by HF-DBS. Continuous HF-DBS in the bilateral anterior insula prevents the relapse of morphine place preference after withdrawal, facilitates its extinction, blocks the reinstatement induced by morphine priming and reverses the expression of morphine-regulated proteins. Our findings suggest that manipulation of insular activity by DBS could be a potential intervention to treat substance use disorder, although future research is warranted.

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Section: Discussionsupporting

confidence: 91%

Continuous High Frequency Deep Brain Stimulation of the Rat Anterior Insula Attenuates the Relapse Post Withdrawal and Strengthens the Extinction of Morphine Seeking

et al. 2020

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“…To investigate the pattern of cellular activation following CFA injection, all animals in the treated and control groups (not the Naïve group) received a single injection of CFA (25 µl) in the left hind paw 12 hr after Mn 2+ chloride injection and 2 hr before MRI brain scanning. These time points were chosen because (a) 12 hr after systemic injection, the manganese chloride solution is already reaching deep structures in the central nervous system and (b) the MEMRI signal is capable to differentially measure the tissue‐specific activation within 1 hr after the stimulus, as previously showed (Gimenes et al., 2019). MRIs were obtained in a 2 Tesla/30 cm horizontal superconducting magnet 85310HR (Oxford Instruments) interfaced to a Bruker Avance AVIII console (Bruker‐Biospin, Ettlingen, GE) running Paravision 5.1 software (Bruker, Ettlingen, GE).…”

Section: Methodsmentioning

confidence: 99%

Adult brain activation in response to pain is changed by neonatal painful stimulation according to sex: A manganese‐enhanced MRI study

Malheiros

Andreeta

Polli

et al. 2020

Eur J of Neuroscience

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Although it is known that nociceptive stimulation in the first postnatal week in rats is useful to model preterm pain, resulting in activation of specific brain areas, as assessed in vivo using manganese‐enhanced magnetic resonance imaging (MEMRI), little is known about its long‐term effects and sex specificity. Here we aimed to investigate whether inflammatory pain induced in male and female adult rats modify the pattern of brain activation between animals subjected or not to neonatal pain. For this, Complete Freund's adjuvant (CFA) was injected into the left hind paw of rat pups on postnatal day 1 (P1) or P8 to induce inflammatory response. During adulthood, CFA‐treated and control animals were injected with CFA 1 hr prior MRI. MEMRI has the ability to enhance the contrast of selective brain structures in response to a specific stimulus, as the pain. MEMRI responses were consistent with activation of nociceptive pathways and these responses were reduced in animals treated with CFA on P1, but increased in animals treated on P8, mainly in the female group. In agreement, P8 female group showed exacerbated responses in the thermal nociceptive test. Using MEMRI, we conclude that the natural ability of adult rats to recognize and react to pain exposition is modified by neonatal painful exposition, mainly among females.

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“…Furthermore, chronic electrical stimulation also leads to an elevation in Janus kinase-signal transducer and activator of transcription (JAK/STAT) signaling, which is critical for cytokine/chemokine signaling ( Zareen et al, 2018 ). Another study demonstrated increased c-Fos in brain regions including cingulate cortex, posterior hypothalamus, and subiculum following DBS ( Gimenes et al, 2019 ). Microstimulation of sensorimotor cortex also leads to the expression of c-Fos and c-Jun in the striatum ( Parthasarathy and Graybiel, 1997 ).…”

Section: Response Of Neurons and Non-neuronal Cell Types To Electrica...mentioning

confidence: 99%

Effects of central nervous system electrical stimulation on non-neuronal cells

Williams

Kushwah²,

Dhawan³

et al. 2022

Front. Neurosci.

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Over the past few decades, much progress has been made in the clinical use of electrical stimulation of the central nervous system (CNS) to treat an ever-growing number of conditions from Parkinson’s disease (PD) to epilepsy as well as for sensory restoration and many other applications. However, little is known about the effects of microstimulation at the cellular level. Most of the existing research focuses on the effects of electrical stimulation on neurons. Other cells of the CNS such as microglia, astrocytes, oligodendrocytes, and vascular endothelial cells have been understudied in terms of their response to stimulation. The varied and critical functions of these cell types are now beginning to be better understood, and their vital roles in brain function in both health and disease are becoming better appreciated. To shed light on the importance of the way electrical stimulation as distinct from device implantation impacts non-neuronal cell types, this review will first summarize common stimulation modalities from the perspective of device design and stimulation parameters and how these different parameters have an impact on the physiological response. Following this, what is known about the responses of different cell types to different stimulation modalities will be summarized, drawing on findings from both clinical studies as well as clinically relevant animal models and in vitro systems.

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The neural response to deep brain stimulation of the anterior nucleus of the thalamus: A MEMRI and c-Fos study

Cited by 17 publications

References 42 publications

Continuous High Frequency Deep Brain Stimulation of the Rat Anterior Insula Attenuates the Relapse Post Withdrawal and Strengthens the Extinction of Morphine Seeking

Continuous High Frequency Deep Brain Stimulation of the Rat Anterior Insula Attenuates the Relapse Post Withdrawal and Strengthens the Extinction of Morphine Seeking

Adult brain activation in response to pain is changed by neonatal painful stimulation according to sex: A manganese‐enhanced MRI study

Effects of central nervous system electrical stimulation on non-neuronal cells

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