Learned expectations and uncertainty facilitate pain during classical conditioning

Taylor, Véronique A.; Chang, Luke J.; Rainville, Pierre; Roy, Mathieu

doi:10.1097/j.pain.0000000000000948

Cited by 21 publications

(23 citation statements)

References 34 publications

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“…Excessive anxiety can lead to increased catecholamine secretion that may enhance nociceptive stimuli from the pelvis and increase the perception of these stimuli at the cortical level ( 52 ). Pain has been shown to be under the constant influence of learning processes affecting the anticipation of, and responses to future pain, as temporary periods of conditioned hyperalgesia were induced by both the predictability and uncertainty of pain from an electric shock ( 53 ). This has interesting implications for the perception of farrowing pain in primiparous and multiparous sows.…”

Section: Discussionmentioning

confidence: 99%

Periparturient Behavior and Physiology: Further Insight Into the Farrowing Process for Primiparous and Multiparous Sows

Ison

Jarvis

et al. 2018

Front. Vet. Sci.

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Giving birth is a critical time for many species and is often the most painful event ever experienced by females. In domestic species, like the pig, pain associated with parturition represents a potential welfare concern, and the consequences of pain can cause economic losses (e.g., by indirectly contributing to piglet mortality as pain could slow post-farrowing recovery, reduce food and water intake, reducing milk let-down). This study investigated pain assessment and its management in primiparous (gilts) and multiparous (sows) breeding pigs, including the provision of a non-steroidal anti-inflammatory drug (NSAID) post-parturition. Individuals were randomly allocated to receive the NSAID ketoprofen (3 mg/kg bodyweight) (n = 11 gilts, 16 sows) or the equivalent volume of saline (n = 13 gilts, 16 sows) by intramuscular injection 1.5 h after the birth of the last piglet. Data collected included putative behavioral indicators of pain (back leg forward, tremble, back arch), salivary cortisol concentrations pre-farrowing and up to 7 days post-injection. In addition, post-partum biomarkers of inflammation, including the acute phase protein C-reactive protein (CRP) and 3 porcine cytokines [interleukin-1 β (IL1 β), interleukin-6 (IL6), and tumor necrosis factor α (TNF α)] were measured in plasma collected 6 h following the injection. Behaviors were analyzed using generalized linear mixed models, and physiological variables with linear mixed models. No difference in putative pain behaviors, salivary cortisol, CRP, or cytokines were found between individuals treated with ketoprofen or those administered the saline control. However, there were some differences between gilts and sows, as sows exhibited more putative pain behavior than gilts, had higher salivary cortisol on the day of farrowing and had higher plasma TNF α. Conversely, gilts had higher salivary cortisol than sows on day 3 post-farrowing and had higher CRP. This indicates that, like human females, multiparous sows experience more pain from uterine activity following birth than primiparas. This study provides useful information for developing management practices relating to post-farrowing care for breeding pigs.

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Section: Discussionmentioning

confidence: 99%

Periparturient Behavior and Physiology: Further Insight Into the Farrowing Process for Primiparous and Multiparous Sows

Ison

Jarvis

et al. 2018

Front. Vet. Sci.

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“…The fact that attention and controllability reliably modulate pain (Eccleston and Crombez, 1999;Wiech et al, 2006;Yoshida et al, 2013;Salomons et al, 2007Salomons et al, , 2015Taylor et al, 2017;Br€ ascher et al, 2016), beyond that which can be explained by mechanisms above, suggests that factors intrinsic to learning and control specifically modulate pain. Although the goal of RL is to learn to minimize pain as an objective function, performance can be enhanced by intrinsically modulating pain according to its informational value in learning.…”

Section: Modulation By Informational Valuementioning

confidence: 99%

Pain: A Precision Signal for Reinforcement Learning and Control

Seymour

2019

Neuron

110

104

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Since noxious stimulation usually leads to the perception of pain, pain has traditionally been considered sensory nociception. But its variability and sensitivity to a broad array of cognitive and motivational factors have meant it is commonly viewed as inherently imprecise and intangibly subjective. However, the core function of pain is motivational-to direct both short-and long-term behavior away from harm. Here, we illustrate that a reinforcement learning model of pain offers a mechanistic understanding of how the brain supports this, illustrating the underlying computational architecture of the pain system. Importantly, it explains why pain is tuned by multiple factors and necessarily supported by a distributed network of brain regions, recasting pain as a precise and objectifiable control signal.Despite the advent of brain imaging, a clear picture of how pain is processed in the brain has been much harder to unravel than anticipated, being beset by three problems. First, pain is associated with robust responses in multiple and diverse brain regions, most of which are not specific to pain (at least on a macroscopic scale), and so it has been hard to ''pin down'' the pain system to any specific brain region. Second, pain is an inherently private percept, but an individual's self-reports of pain can vary widely from moment to moment, and it has remained unclear whether this fluctuation represents irreducible noise and subjectivity or a precise tuning of pain based on hidden factors. Third, pain is exquisitely sensitive to a broad range of emotional, environmental, and cognitive factors-a phenomenon called endogenous modulation. Although this has led to an appreciation that pain is more than a simple readout of nociceptive input, it has not led to any satisfactory unified explanation as to what pain really is. This has left the view that pain is simply a highly variable and malleable representation of assumed actual or potential tissue damage.In this review, we propose a model of pain that centralizes its role as a learning and control signal and argue that this can solve these problems. We begin with a perspective of how theories of pain have evolved over recent decades, and how insights have emerged that have moved thinking beyond purely sensory accounts of pain. We then argue that current accounts still don't fully capture how pain controls behavior to minimize harm, which is its primary function. Importantly, although this is often achieved by immediate nocifensive responses, a substantial part of this comes from learning-allowing an animal to mitigate or avoid predictable harm long into the future. The foundations of a learning account of pain are rooted in psychological models of animal learning, and we describe how these can be developed in computational terms to provide a mechanistic model of the architecture of the pain system. Critically, we argue that this requires pain to be shaped by a set of factors to optimize its role as a learning and control signal and review evidence that suggests that a great...

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“…A priori expectancies strongly correlate with CPM-induced analgesia, such that expectancies of hyperalgesia verbally induced through suggestions can enhance the nociceptive reflex amplitude and shock pain (thus blocking the analgesia normally activated by CPM), while suggestions of analgesia enhance the decrease in nociceptive reflex amplitude (Cormier et al, 2013). Changes in expected pain predict changes in pain outcomes mediated by descending pain modulation affecting spinal processes (Taylor, Chang, Rainville, & Roy, 2017). Findings suggest that while positive expectancies (analgesia) and lower stress are related to a greater pain reduction induced by CPM, negative expectancies (e.g., expectation of enhanced pain, hyperalgesia) enhance pain intensity.…”

Section: Role and Manipulation Of Expectanciesmentioning

confidence: 99%

Pain Modulation: From Conditioned Pain Modulation to Placebo and Nocebo Effects in Experimental and Clinical Pain

Damien

Colloca

Belleï-Rodriguez

et al. 2018

International Review of Neurobiology

106

107

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Accumulating evidence reveal important applications of endogenous pain modulation assessment in healthy controls and in patients in clinical settings, as dysregulations in the balance of pain modulatory circuits may facilitate pain and promote chronification of pain. This article reviews data on pain modulation, focusing on the mechanisms and translational aspects of pain modulation from conditioned pain modulation (CPM) to placebo and nocebo effects in experimental and clinical pain. The specific roles of expectations, learning, neural and neurophysiological mechanisms of the central nervous system are briefly reviewed herein. The interaction between CPM and placebo systems in pain inhibitory pathways is highly relevant in the clinic and in randomized controlled trials yet remains to be clarified. Examples of clinical implications of CPM and its relationship to placebo and nocebo effects are provided. A greater understanding of the role of pain modulation in various pain states can help characterize the manifestation and development of chronic pain and assist in predicting the response to pain-relieving treatments. Placebo and nocebo effects, intrinsic to every treatment, can be used to develop personalized therapeutic approaches that improve clinical outcomes while limiting unwanted effects.

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Learned expectations and uncertainty facilitate pain during classical conditioning

Cited by 21 publications

References 34 publications

Periparturient Behavior and Physiology: Further Insight Into the Farrowing Process for Primiparous and Multiparous Sows

Periparturient Behavior and Physiology: Further Insight Into the Farrowing Process for Primiparous and Multiparous Sows

Pain: A Precision Signal for Reinforcement Learning and Control

Pain Modulation: From Conditioned Pain Modulation to Placebo and Nocebo Effects in Experimental and Clinical Pain

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