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Descending Control Mechanisms and Chronic Pain

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Descending Control Mechanisms and Chronic Pain Current Rheumatology Reports (2019) 21: 13 https://doi.org/10.1007/s11926-019-0813-1 CHRONIC PAIN (R STAUD, SECTION EDITOR) Descending Control Mechanisms and Chronic Pain QiLiang Chen1 & Mary M. Heinricher2,3 Published online: 4 March 2019 # Springer Science+Business Media, LLC, part of Springer Nature 2019 Abstract Purpose of Review The goal of the review was to highlight recent advances in our understanding of descending pain- modulating systems and how these contribute to persistent pain states, with an emphasis on the current state of knowledge around “bottom-up” (sensory) and “top-down” (higher structures mediating cognitive and emotional processing) influences on pain-modulating circuits. Recent Findings The connectivity, physiology, and function of these systems have been characterized extensively over the last 30 years. The field is now beginning to ask how and when these systems are engaged to modulate pain. A recent focus is on the parabrachial complex, now recognized as the major relay of nociceptive information to pain- modulating circuits, and plasticity in this circuit and its connections to the RVM is marked in persistent inflamma- tory pain. Top-down influences from higher structures, including hypothalamus, amygdala, and medial prefrontal areas, are also considered. Summary The challenge will be to tease out mechanisms through which a particular behavioral context engages distinct circuits to enhance or suppress pain, and to understand how these mechanisms contribute to chronic pain. Keywords Pain modulation . Brainstem . Persistent pain . Inflammation . Hypersensitivity Introduction physical injury, or develop after a primary injury has healed, making targeted treatments or surgical interventions difficult. Current pharmacological treatments for chronic pain Moreover, pharmacological therapies used for acute pain are have limited efficacy and undesirable side effects, par- generally less effective in chronic pain conditions. For exam- ticularlywhenusedlong-term[1]. Relief of acute pain ple, opioids, one of the most powerful classes of analgesics, is relatively straightforward, and pharmacological ap- become less effective over time, and the accompanying side proaches range from over-the-counter pain relievers such effects, such as constipation, respiratory depression, and de- as nonsteroidal anti-inflammatory drugs (NSAIDs), to pendence, become more severe. The risk of addiction is also a prescription drugs, such as opioids, which can provide factor. Alternatives, such as serotonin-norepinephrine reup- powerful pain control. Management of chronic pain condi- take inhibitors and anticonvulsants, act centrally, and show tions, on the other hand, is much more challenging. Many benefits in treating some pain conditions, although these ap- chronic pain conditions are without apparent underlying proaches themselves have undesirable side effects. These clinical challenges highlight the complexity of pain This article is part of the Topical Collection on Chronic Pain as a sensory experience, and argue for understanding the cir- cuitry underlying different persistent pain states as the basis * Mary M. Heinricher for therapeutics. The present review will discuss recent [email protected] findings related to the role of “descending control sys- tems” in persistent pain. These systems, with important 1 Department of Surgery, Stanford University, Stanford, CA 94305, links in the brainstem and descending projections to the USA dorsal horn, are known to modulate spinal nociceptive 2 Department of Neurological Surgery, Oregon Health & Science processing. “Bottom-up” and “top-down” inputs to the University, Portland, OR 97239, USA descending pain-modulating system allow sensory infor- 3 Department of Behavioral Neuroscience, Oregon Health & Science mation (bottom-up) and cognitive and emotional factors University, Portland, OR 97239, USA 13 Page 2 of 7 Curr Rheumatol Rep (2019) 21: 13 (top-down) to influence nociceptive processing and pain Physiology of Brainstem Circuits Mediating perception [2–4]. Descending Control Extensive work from numerous laboratories has gone into characterizing the connectivity, physiology, and function of Dysfunction in Descending Control descending pain control circuitry over the last 30 years. (See Contributes to Persistent Pain States Heinricher and Fields [2] for an overview of this circuitry.) It was recognized as early as 1969 that electrical stimulation of There is now increasing evidence that persistent pain states specific brainstem structures, such as the midbrain are, at least in part, a reflection of dysfunction in descending periaqueductal gray (PAG), produces analgesia and inhibits control systems [5, 6]. This is most amply documented using nociceptive neurons in the dorsal horn. This analgesic influ- the “conditioned pain modulation” (CPM) paradigm, in which ence of the PAG is not mediated by a direct projection from a painful stimulus delivered to one part of the body suppresses PAG to the dorsal horn, but through a relay referred to as the the pain resulting from a standardized noxious stimulus ap- “rostral ventromedial medulla” (RVM). The RVM, plied at a remote site. An impaired ability to mount a CPM encompassing the area of the raphe magus and surrounding response is a frequent characteristic of patient populations reticular region at the level of the facial nucleus, has been with chronic pain [6–8]. This concept is supported by com- established as the major output node in descending modula- plementary studies in animal models measuring “diffuse nox- tion of nociception. As with the PAG, electrical stimulation of ious inhibitory control” (DNIC), the phenomenon of descend- the RVM produces potent analgesia. The RVM receives a ing inhibition of the dorsal horn sensory neurons when a pain- dense input from the PAG, and sends diffuse bilateral projec- ful stimulus is applied to a remote body part outside of the tions to the dorsal horn with terminations at multiple levels. recorded neuron’s receptive field [9]. The mechanism of The PAG-RVM system remains the best-studied circuit for DNIC involves a complex brainstem circuit that includes both descending pain modulation, and there is every reason to think an ascending limb from the dorsal horn to caudal brainstem, that it is functionally the most significant. and a descending limb from both the caudal medulla and the Based on the early studies demonstrating the analgesic ef- rostral ventromedial medulla [10, 11]. A reduction in DNIC fects of electrical stimulation in both PAG and RVM, the hasbeendemonstratedtobeassociatedwithhyperalgesiain PAG-RVM circuit was initially viewed as an “analgesia sys- models of postsurgical pain, nerve injury, traumatic brain in- tem” [16–18]. However, subsequent studies revealed that jury, and opioid-induced sensitization [12–15](Fig.1). RVM modulates nociception in a bidirectional manner, and that it can facilitate as well as inhibit pain [19, 20]. The capac- ity for bidirectional control derives from two classes of RVM neurons referred to as “OFF-cells” and “ON-cells” [2], which are described in more detail below. Overwhelming evidence has demonstrated that OFF-cells exert a net inhibitory effect on nociceptive transmission, whilst ON-cells have a net pro- nociceptive action [3, 21]. The OFF- and ON-cell designations arise from the fact that OFF-cells cease firing, or “turn off” when an animal responds to a noxious stimulus, whereas ON-cells are activated or “turn on” in association with responses to noxious stimuli. Although non-selective activation of all RVM neurons produces analge- sia, selective activation of ON-cells results in hyperalgesia [22]. Exogenous activation of OFF-cells or elimination of the OFF- cell pause is sufficient to produce antinociception, and it has been estimated that activation of as few as 30 OFF-cells pro- duces behaviorally measurable analgesia [23, 24]. ON- and OFF-cell activity is usually antiphase-synchronized under unstimulated conditions, having alternating periods of silence and activity [25]. The nocifensor withdrawal–related ON-cell burst of activity and OFF-cell pause in firing are also antiphase- Fig. 1 The PAG-RVM descending pain-modulating pathway exerts synchronized [26]. Thus, output from the two cell classes mod- facilitatory and inhibitory drive on dorsal horn neurons. The output of this pathway can be influenced by higher structures, such as ulates nociceptive transmission at the level of spinal dorsal horn hypothalamus and limbic forebrain in a parallel fashion, where the withdrawal threshold for the Curr Rheumatol Rep (2019) 21: 13 Page 3 of 7 13 organism is in part determined by collective activity across the OFF-cell activity. Blocking ON-cell activation reduces two cell populations. hyperalgesia under these conditions [38–40]. Similarly, visceral One recurring question that has arisen in the study of the acute inflammation induced by application of capsaicin increases PAG-RVM system is whether this system truly modulates ON-cell ongoing activity, and decreases the threshold for pain, or whether it is instead simply controlling output of nociception-evoked hindpaw withdrawal [41]. Taken together, nocifensor reflex circuits. Multiple lines of evidence argue these results demonstrate the contribution of descending facilita- against this latter view. First, although RVM terminals are tion mediated by RVM ON-cells to acute inflammatory pain. not limited to the dorsal horn, projections of OFF- and ON- The situation becomes more complex as inflammation
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