The projections from the anterior cingulate cortex to the nucleus accumbens and ventral tegmental area contribute to neuropathic pain-evoked aversion in rats

Gao, Shi-Hao; Shen, Lin‐Lin; Han, Wen; Zhao, Yandong; Chen, Penghui; Ruan, Han‐Li

doi:10.1016/j.nbd.2020.104862

Cited by 46 publications

(50 citation statements)

References 70 publications

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“…S5 ). Consistent with our published data ( Tu et al, 2021 ), previous awake behavioral studies using the same DREADDs showed a comparable regional inhibition level between the V1 and ACC ( Gao et al, 2020 ; Wang et al, 2021 ).…”

Section: Resultssupporting

confidence: 92%

Brain network reorganization after targeted attack at a hub region

Zhang

2021

NeuroImage

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The architecture of brain networks has been extensively studied in multiple species. However, exactly how the brain network reconfigures when a local region, particularly a hub region, stops functioning remains elusive. By combining chemogenetics and resting-state functional magnetic resonance imaging (rsfMRI) in an awake rodent model, we investigated the causal impact of acutely inactivating a hub region (i.e. the dorsal anterior cingulate cortex) on brain network properties. We found that suppressing neural activity in a hub could have a ripple effect that went beyond the hub-related connections and propagated to other neural connections across multiple brain systems. In addition, hub dysfunction affected the topological architecture of the whole-brain network in terms of the network resilience and segregation. Selectively inhibiting excitatory neurons in the hub further changed network integration. None of these changes were observed in sham rats or when a non-hub region (i.e. the primary visual cortex) was perturbed. This study has established a system that allows for mechanistically dissecting the relationship between local regions and brain network properties. Our data provide direct evidence supporting the hypothesis that acute dysfunction of a brain hub can cause large-scale network changes. These results also provide a comprehensive framework documenting the differential impact of hub versus non-hub nodes on network dynamics.

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Section: Resultssupporting

confidence: 92%

Brain network reorganization after targeted attack at a hub region

Zhang

2021

NeuroImage

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“…Removal of an aversive state to evoke CPP has been observed in animals expressing chronic pain, in which pairing a pain-relieving drug with a context during conditioning elicits CPP for the drug-paired context (King et al, 2009 ; Cahill et al, 2013 ; Navratilova et al, 2013 ). Additionally, in animals expressing chronic pain, inhibiting the anterior cingulate cortex (ACC), a brain region involved in pain expression, during context pairing elicits CPP for the context paired with ACC inhibition (Gao et al, 2020 ). These findings suggest that the removal of an aversive state, such as pain, reinforces the animal’s behavioral response to prefer the drug-paired context.…”

Section: Factors To Consider When Interpreting Conditioned Place Prefmentioning

confidence: 99%

Drug-Induced Conditioned Place Preference and Its Practical Use in Substance Use Disorder Research

McKendrick

Graziane

2020

Front. Behav. Neurosci.

145

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The conditioned place preference (CPP) paradigm is a well-established model utilized to study the role of context associations in reward-related behaviors, including both natural rewards and drugs of abuse. In this review article, we discuss the basic history, various uses, and considerations that are tied to this technique. There are many potential takeaway implications of this model, including negative affective states, conditioned drug effects, memory, and motivation, which are all considered here. We also discuss the neurobiology of CPP including relevant brain regions, molecular signaling cascades, and neuromodulatory systems. We further examine some of our prior findings and how they integrate CPP with self-administration paradigms. Overall, by describing the fundamentals of CPP, findings from the past few decades, and implications of using CPP as a research paradigm, we have endeavored to support the case that the CPP method is specifically advantageous for studying the role of a form of Pavlovian learning that associates drug use with the surrounding environment.

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“…mPFC encompasses the infralimbic and prelimbic cortex (IL, PL), and the adjacent anterior cingulate cortex (ACC). These distinct parts of the mPFC play different roles in pain modulation: activation of the PL glutamatergic neurons reduces sensory and affective pain responses in neuropathic pain [81][82][83], whereas activation of the ACC exerts an opposite effect, particularly on the emotional aspect of pain, i.e., mediates or enhances its aversive quality [84][85][86][87]. According to most studies, the ACC does not modulate the sensory experience of pain; however, some results suggest that ACC stimulation may also enhance sensory sensitivity [84,85,88].…”

Section: Involvement Of Medial Prefrontal Cortex In Pain Processingmentioning

confidence: 99%

“…*-In contrast to some other studies, Ren et al [67] provide evidence of an increase in dopaminergic neurotransmission in the medial VTA-medial NAc shell projection in chronic pain. This scheme has been based on the studies by Schwartz et al [89], Lee et al [81], Ren et al [63,67], and Gao et al [85]. The nigrostriatal dopamine pathway has not been included in the figure due to the lack of corresponding studies on the dorsal striatum.…”

Section: Involvement Of Medial Prefrontal Cortex In Pain Processingmentioning

confidence: 99%

“…Pharmacological studies involving injections of dopamine receptor ligands into the dStr and NAc suggest that stimulation of the D2R exerts an analgesic effect, whereas the striatal D1R plays no role in pain (see Section 6). Moreover, numerous studies demonstrated that chronic pain selectively affects the D2-MSN's (but not D1-MSN's) dendrite morphology, excitability, and synaptic connectivity [63,67,85,89]. This implicates the indirect striatal output pathway, stemming from the D2R-containing MSN, rather than the direct pathway originating in D1-MSN, in pain processing.…”

Section: Medial Nac Shellmentioning

confidence: 99%

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The Role of Mesostriatal Dopamine System and Corticostriatal Glutamatergic Transmission in Chronic Pain

Ziółkowska

2021

Brain Sciences

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There is increasing recognition of the involvement of the nigrostriatal and mesolimbic dopamine systems in the modulation of chronic pain. The first part of the present article reviews the evidence indicating that dopamine exerts analgesic effects during persistent pain by stimulating the D2 receptors in the dorsal striatum and nucleus accumbens (NAc). Thereby, dopamine inhibits striatal output via the D2 receptor-expressing medium spiny neurons (D2-MSN). Dopaminergic neurotransmission in the mesostriatal pathways is hampered in chronic pain states and this alteration maintains and exacerbates pain. The second part of this article focuses on the glutamatergic inputs from the medial prefrontal cortex to the NAc, their activity changes in chronic pain, and their role in pain modulation. Finally, interactions between dopaminergic and glutamatergic inputs to the D2-MSN are considered in the context of persistent pain. Studies using novel techniques indicate that pain is regulated oppositely by two independent dopaminergic circuits linking separate parts of the ventral tegmental area and of the NAc, which also interact with distinct regions of the medial prefrontal cortex.

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The projections from the anterior cingulate cortex to the nucleus accumbens and ventral tegmental area contribute to neuropathic pain-evoked aversion in rats

Cited by 46 publications

References 70 publications

Brain network reorganization after targeted attack at a hub region

Brain network reorganization after targeted attack at a hub region

Drug-Induced Conditioned Place Preference and Its Practical Use in Substance Use Disorder Research

The Role of Mesostriatal Dopamine System and Corticostriatal Glutamatergic Transmission in Chronic Pain

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