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      Orienting Attention Modulates Pain Perception: An ERP Study

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          Abstract

          Introduction

          Research has shown that people with chronic pain have difficulty directing their attention away from pain. A mental strategy that incorporates focused attention and distraction has been found to modulate the perception of pain intensity. That strategy involves placing attention on the nociceptive stimulus felt and shifting attention to a self-generated sub-nociceptive image and rehearsing it. Event-related potential was used to study the possible processes associated with the focus-then-orient strategy.

          Methods

          Eighteen pain-free participants received different levels of 50-ms nociceptive stimulations elicited by electric shocks at the right lateral malleolus (ankle). In perception trials, participants maintained the perceived nociceptive stimulus in working memory for 3,000 ms. In imagery trials, participants mentally generated and maintained the corresponding sub-nociceptive image they had learned previously. After both types of trials, participants evaluated the pain intensity of the incoming stimulus by recalling the feeling of the nociceptive stimulation at the beginning of the trial.

          Results

          Shifting attention from the incoming nociceptive to a self-generated sub-nociceptive image elicited central P2 and centro-parietal P3 waves, which were found to correlate with proportional scores on the Stroop Test. They were followed by a frontal N400 and a parietal P600, denoting generation of sub-nociceptive images in working memory. The voltages elicited in these potentials correlated moderately with attenuation of the pain ratings of the recalled nociceptive stimulations.

          Conclusions

          Focus-and-orient attention across nociceptive and sub-nociceptive images appears to be related to response inhibition. Mental rehearsal of the sub-nociceptive images was found to modulate the perception of the nociceptive sensation felt prior to the imagery. Such modulation seems to be mediated by generating and maintaining sub-nociceptive images in working memory. Future studies should explore the mental processes associated with orienting attention for pain modulation among people with pathological pain and frontal lobe dysfunction.

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          Most cited references53

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          Blind separation of auditory event-related brain responses into independent components.

          Averaged event-related potential (ERP) data recorded from the human scalp reveal electroencephalographic (EEG) activity that is reliably time-locked and phase-locked to experimental events. We report here the application of a method based on information theory that decomposes one or more ERPs recorded at multiple scalp sensors into a sum of components with fixed scalp distributions and sparsely activated, maximally independent time courses. Independent component analysis (ICA) decomposes ERP data into a number of components equal to the number of sensors. The derived components have distinct but not necessarily orthogonal scalp projections. Unlike dipole-fitting methods, the algorithm does not model the locations of their generators in the head. Unlike methods that remove second-order correlations, such as principal component analysis (PCA), ICA also minimizes higher-order dependencies. Applied to detected-and undetected-target ERPs from an auditory vigilance experiment, the algorithm derived ten components that decomposed each of the major response peaks into one or more ICA components with relatively simple scalp distributions. Three of these components were active only when the subject detected the targets, three other components only when the target went undetected, and one in both cases. Three additional components accounted for the steady-state brain response to a 39-Hz background click train. Major features of the decomposition proved robust across sessions and changes in sensor number and placement. This method of ERP analysis can be used to compare responses from multiple stimuli, task conditions, and subject states.
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            Towards a theory of chronic pain.

            In this review, we integrate recent human and animal studies from the viewpoint of chronic pain. First, we briefly review the impact of chronic pain on society and address current pitfalls of its definition and clinical management. Second, we examine pain mechanisms via nociceptive information transmission cephalad and its impact and interaction with the cortex. Third, we present recent discoveries on the active role of the cortex in chronic pain, with findings indicating that the human cortex continuously reorganizes as it lives in chronic pain. We also introduce data emphasizing that distinct chronic pain conditions impact on the cortex in unique patterns. Fourth, animal studies regarding nociceptive transmission, recent evidence for supraspinal reorganization during pain, the necessity of descending modulation for maintenance of neuropathic behavior, and the impact of cortical manipulations on neuropathic pain is also reviewed. We further expound on the notion that chronic pain can be reformulated within the context of learning and memory, and demonstrate the relevance of the idea in the design of novel pharmacotherapies. Lastly, we integrate the human and animal data into a unified working model outlining the mechanism by which acute pain transitions into a chronic state. It incorporates knowledge of underlying brain structures and their reorganization, and also includes specific variations as a function of pain persistence and injury type, thereby providing mechanistic descriptions of several unique chronic pain conditions within a single model.
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              The novelty P3: an event-related brain potential (ERP) sign of the brain's evaluation of novelty.

              A review of the literature that examines event-related brain potentials (ERPs) and novelty processing reveals that the orienting response engendered by deviant or unexpected events consists of a characteristic ERP pattern, comprised sequentially of the mismatch negativity (MMN) and the novelty P3 or P3a. A wide variety of evidence suggests that the MMN reflects the detection of deviant events, whereas the P3a is associated more with the evaluation of those events for subsequent behavioral action. On the scalp, the novelty P3a is comprised of at least two aspects, one frontal the other posterior, each with different cognitive (and presumably neurologic) correlates. Intracranial ERP investigations and studies of patients with localized brain lesions (and, to some extent, fMRI data) converge with the scalp-recorded data in suggesting a widespread neural network, the different aspects of which respond differentially to stimulus and task characteristics.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2012
                29 June 2012
                : 7
                : 6
                : e40215
                Affiliations
                [1 ]Applied Cognitive Neuroscience Laboratory, Department of Rehabilitation Sciences, The Hong Kong Polytechnic University, Hong Kong, China
                [2 ]Haven of Hope Hospital, Hospital Authority, Hong Kong, China
                [3 ]Department of Anaesthesiology, United Christian Hospital, Hospital Authority, Hong Kong, China
                University of Florida, United States of America
                Author notes

                Conceived and designed the experiments: SCCC CCHC ASKK TYC. Performed the experiments: SCCC CCHC KHT ASKK. Analyzed the data: SCCC KHT CCHC. Contributed reagents/materials/analysis tools: SCCC KHT CCHC. Wrote the paper: SCCC CCHC ASKK KHT TYC.

                Article
                PONE-D-11-18932
                10.1371/journal.pone.0040215
                3387012
                22768257
                fe83f9da-4dea-43df-b1d8-884e1acfa44f
                Chan et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                : 19 September 2011
                : 6 June 2012
                Page count
                Pages: 12
                Categories
                Research Article
                Biology
                Neuroscience
                Cognitive Neuroscience
                Pain
                Medicine
                Anesthesiology
                Pain Management
                Mental Health
                Psychology
                Behavior
                Attention (Behavior)
                Neurology
                Pain Management
                Physiotherapy and Rehabilitation
                Social and Behavioral Sciences
                Psychology
                Behavior
                Attention (Behavior)
                Clinical Psychology
                Cognitive Psychology
                Sensory Perception

                Uncategorized
                Uncategorized

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