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Brain processing of experimental muscle pain and its interrelation with proprioception and muscle fatigue: positron emission tomography study
Umeå University, Faculty of Medicine, Surgical and Perioperative Sciences, Sports Medicine.
2005 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Chronic muscle pain is a significant medical and social problem and better understanding of the pathophysiological mechanisms involved is an important requirement for further development of diagnostics, treatment and rehabilitation methods. Experimental imaging studies have investigated functional neuroanatomy of different pain components. However, several aspects of brain mechanisms underlying brain processing of muscle pain remain unclear.

The general goal of the present thesis was to study functional brain anatomy of systems underlying perception of muscle pain, processing of proprioceptive information and maintenance of fatiguing muscle contractions with an emphasize on their possible interrelations.

Four series of experiment were carried out. Using an injection of hypertonic saline (HS) into the m. triceps to induce pain comparable with clinical muscle pain a significant activation of insula and putamen as well as decrease of activity in the temporal and occipital cortex in comparison with control stimulation were revealed. An advanced model of prolonged muscle pain were provided by the infusion of the HS during 20 minutes into m. erector spinae A complex dynamics of brain activity during the habituation to nociceptive stimulation was shown: initial activation of insula changed to decrease of activity in this and several other cortical areas. A conjunction analysis identified activations jointly significant in both experiments (despite localization of HS nociceptive stimulation) in the right insula, occipital and left parietal cortical areas. The study of brain activity in response to different modalities of prorioceptive inputs – passive movements, kinesthetic illusions and muscle vibration showed corresponding different patterns of activation in motor and somatosenory areas and temporal areas. Finally, the study of sustained isometric muscle contractions of various force levels and durations revealed that muscle fatigue is associated with contralateral activation of the motor and somatosensory areas and temporal areas and bilateral activation in the supplementary motor areas and cingular cortex, indicating that increased efforts needed to maintain required force and its eventual breakdown with fatigue might induce activation of additional cortical areas. Analysis of data obtained in all experimental series revealed that insula, secondary somatosensory and auditory areas are activated during both perception of muscle pain and processing of somatosensory afferentation.

In conclusion, this thesis has elucidated brain processing of muscle pain showing distributed, bilateral patterns comprised of activated structures predominantly attributed to the medial pain system and deactivated structures. Furthermore, initial and late phases of tonic muscle pain are associated with different brain reactions, namely initial activation of the insula followed by a significant bilateral decrease of activity at the late stage. Area of brain cortex located near lateral sulcus and comprised of secondary somatosensory cortex, posterior part of the insula and adjacent auditory cortex is engaged in the perception of muscle pain and processing of somatosensory afferentation as well as maintenance of fatiguing muscle contractions.

Place, publisher, year, edition, pages
2005. , 72 p.
Keyword [en]
Experimental muscle pain, Hypertonic saline, Kinesthesia, Proprioception, Movement, Vibration, Muscle fatigue, Brain, Imaging, Positron emission tomography, Regional cerebral blood flow
Identifiers
URN: urn:nbn:se:umu:diva-570OAI: oai:DiVA.org:umu-570DiVA: diva2:143826
Public defence
2005-09-09, Stora föreläsningssalen, Arbetslivsinstitutet Umeå, 10:00 (English)
Opponent
Available from: 2005-08-23 Created: 2005-08-23 Last updated: 2009-11-18Bibliographically approved
List of papers
1. Changes in human regional cerebral blood flow following hypertonic saline induced experimental muscle pain: a positron emission tomography study
Open this publication in new window or tab >>Changes in human regional cerebral blood flow following hypertonic saline induced experimental muscle pain: a positron emission tomography study
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2002 (English)In: Neuroscience Letters, ISSN 0304-3940, E-ISSN 1872-7972, Vol. 335, no 2, 119-123 p.Article in journal (Refereed) Published
Abstract [en]

A positron emission tomography imaging study was performed on 16 healthy volunteers to reveal changes in cortical activation during acute muscle pain induced by intra-muscular injection of hypertonic saline into the left triceps brachii muscle. Changes in regional cerebral blood flow (rCBF) were measured with the use of [(15)O] labelled water during 'Rest1', 'Needle' (insertion of a needle without injection), 'Rest2' and 'Pain' conditions. Differences in rCBF were found in the comparison of Pain and Needle, and Pain and Rest2 conditions, revealing activation of the contralateral insula and putamen. The results are discussed with respect to possible differences in brain processing of muscle and cutaneous noxious inputs.

Identifiers
urn:nbn:se:umu:diva-4635 (URN)10.1016/S0304-3940(02)01181-3 (DOI)12459513 (PubMedID)
Available from: 2005-08-23 Created: 2005-08-23 Last updated: 2017-12-14Bibliographically approved
2. Brain processing of tonic muscle pain induced by infusion of hypertonic saline.
Open this publication in new window or tab >>Brain processing of tonic muscle pain induced by infusion of hypertonic saline.
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2005 (English)In: European Journal of Pain, ISSN 1090-3801, E-ISSN 1532-2149, Vol. 9, no 2, 185-194 p.Article in journal (Refereed) Published
Abstract [en]

Most of the previous studies on the effects of pain on Regional Cerebral Blood Flow (rCBF) had been done with brief cutaneous or intramuscular painful stimuli. The aim of the present study was to investigate the effect on rCBF of long lasting tonic experimental muscle pain. To this end we performed PET investigations of rCBF following tonic experimental low back pain induced by continuous intramuscular infusion of hypertonic (5%) saline (HS) with computer controlled infusion pump into the right erector spinae on L(3) level in 19 healthy volunteers. Changes in rCBF were measured with the use of (15)O labelled water during four conditions: Baseline (before start of infusion), Early Pain (4 min after start of infusion), Late Pain (20 min after start of infusion) and Post-Pain (>15 min after stop of infusion) conditions. Results of SPM analysis showed relative rCBF increase in the right insula and bilateral decrease in the temporo-parieto-occipital cortex during initial phase of painful stimulation (Early Pain) followed by activation of the medial prefrontal region and bilateral inhibition of insula, anterior cingulate and dorso-lateral prefrontal cortex mainly in ipsilateral hemisphere during Late Pain conditions. The results show that longer lasting tonic experimental muscle pain elicited by i.m infusion of HS results in decreases rather than increases in rCBF. Possible explanations for differences found in rCBF during tonic hypertonic saline-induced experimental muscle pain as compared with previous findings are discussed.

Keyword
Adult, Brain/*physiopathology/*radionuclide imaging, Case-Control Studies, Cerebrovascular Circulation/*physiology, Humans, Infusions; Parenteral, Injections; Intramuscular, Male, Muscle Tonus/drug effects/physiology, Muscle; Skeletal/drug effects/physiopathology, Pain/chemically induced/*physiopathology/radionuclide imaging, Positron-Emission Tomography, Saline Solution; Hypertonic/administration & dosage
Identifiers
urn:nbn:se:umu:diva-16964 (URN)10.1016/j.ejpain.2004.05.003 (DOI)15737811 (PubMedID)
Available from: 2007-10-23 Created: 2007-10-23 Last updated: 2017-12-14Bibliographically approved
3. Comparison of brain activity during different types of proprioceptive inputs: a positron emission tomography study
Open this publication in new window or tab >>Comparison of brain activity during different types of proprioceptive inputs: a positron emission tomography study
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2002 (English)In: Experimental Brain Research, ISSN 0014-4819, E-ISSN 1432-1106, Vol. 143, no 3, 276-285 p.Article in journal (Refereed) Published
Abstract [en]

It has been shown that the primary and secondary somatosensory cortex, as well as the supplementary motor area (SMA), are involved in central processing of proprioceptive signals during passive and active arm movements. However, it is not clear whether different cortical areas are involved in processing of different proprioceptive inputs (skin, joint, muscle receptors), what their relative contributions might be, where kinesthetic sensations are formed within the CNS, and how they interact when the full peripheral proprioceptive machinery acts. In this study we investigated the representation of the brain structures involved in the perception of passive limb movement and illusory movement generated by muscle tendon vibration. Changes in cortical activity as indicated by changes in regional cerebral blood flow (rCBF) were measured using positron emission tomography (PET). Twelve subjects were studied under four conditions: (1) passive flexion-extension movement (PM) of the left forearm; (2) induced illusions of movements (VI) similar to the real PM, induced by alternating vibration of biceps and triceps tendons (70-80 Hz) at the elbow; (3) alternating vibration of biceps and triceps tendons (with 20-50 Hz) without induced kinesthetic illusions (VN); and (4) rest condition (RE). The results show different patterns of cortex activation. In general, the activation during passive movement was higher in comparison with both kinds of vibration, and activation during vibrations with induced illusions of movement was more prominent than during vibrations without induced illusions. When the PM condition was contrasted with the other conditions we found the following areas of activation -- the primary motor (MI) and somatosensory area (SI), the SMA and the supplementary somatosensory area (SSA). In conditions where passive movements and illusory movements were contrasted with rest, some temporal areas, namely primary and associative auditory cortex, were activated, as well as secondary somatosensory cortex (SII). Our data show that different proprioceptive inputs, which induce sensation of movement, are associated with differently located activation patterns in the SI/MI and SMA areas of the cortex. In general, the comparison of activation intensities under different functional conditions indicates the involvement of SII in stimulus perception generation and of the SI/MI and SMA areas in the processing of proprioceptive input. Activation of the primary and secondary auditory cortex might reflect the interaction between somatosensory and auditory systems in movement sense generation. SSA might also be involved in movement sense generation and/or maintenance.

Identifiers
urn:nbn:se:umu:diva-4637 (URN)10.1007/s00221-001-0994-4 (DOI)11889505 (PubMedID)
Available from: 2005-08-23 Created: 2005-08-23 Last updated: 2017-12-14Bibliographically approved
4. Comparison of brain activation after sustained non-fatiguing and fatiguing muscle contraction: a positron emission tomography study.
Open this publication in new window or tab >>Comparison of brain activation after sustained non-fatiguing and fatiguing muscle contraction: a positron emission tomography study.
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2005 (English)In: Experimental Brain Research, ISSN 0014-4819, E-ISSN 1432-1106, Vol. 163, no 1, 65-74 p.Article in journal (Refereed) Published
Abstract [en]

The concept of fatigue refers to a class of acute effects that can impair motor performance, and not to a single mechanism. A great deal is known about the peripheral mechanisms underlying the process of fatigue, but our knowledge of the roles of the central structures in that process is still very limited. During fatigue, it has been shown that peripheral apparatus is capable of generating adequate force while central structures become insufficient/sub-optimal in driving them. This is known as central fatigue, and it can vary between muscles and different tasks. Fatigue induced by submaximal isometric contraction may have a greater central component than fatigue induced by prolonged maximal efforts. We studied the changes in regional cerebral blood flow (rCBF) of brain structures after sustained isometric muscle contractions of different submaximal force levels and of different durations, and compared them with the conditions observed when the sustained muscle contraction becomes fatiguing. Changes in cortical activity, as indicated by changes in rCBF, were measured using positron emission tomography (PET). Twelve subjects were studied under four conditions: (1) rest condition; (2) contraction of the m. biceps brachii at 30% of MVC, sustained for 60 s; (3) contraction at 30% of MVC, sustained for 120 s, and; (4) contraction at 50% of MVC, sustained for 120 s. The level of rCBF in the activated cortical areas gradually increased with the level and duration of muscle contraction. The fatiguing condition was associated with predominantly contralateral activation of the primary motor (MI) and the primary and secondary somatosensory areas (SI and SII), the somatosensory association area (SAA), and the temporal areas AA and AI. The supplementary motor area (SMA) and the cingula were activated bilaterally. The results show increased cortical activation, confirming that increased effort aimed at maintaining force in muscle fatigue is associated with increased activation of cortical neurons. At the same time, the activation spread to several cortical areas and probably reflects changes in both excitatory and inhibitory cortical circuits. It is suggested that further studies aimed at controlling afferent input from the muscle during fatigue may allow a more precise examination of the roles of each particular region involved in the processing of muscle fatigue.

Keyword
Adult, Brain/blood supply/*physiology/radionuclide imaging, Cerebrovascular Circulation/physiology, Electromyography, Humans, Male, Muscle Contraction/*physiology, Muscle Fatigue/*physiology, Positron-Emission Tomography
Identifiers
urn:nbn:se:umu:diva-17015 (URN)10.1007/s00221-004-2141-5 (DOI)15645226 (PubMedID)
Available from: 2007-10-25 Created: 2007-10-25 Last updated: 2017-12-14Bibliographically approved
5. Eхperimental muscle pain induced by injection of hypertonic saline: Comparative analysis of two PET studies
Open this publication in new window or tab >>Eхperimental muscle pain induced by injection of hypertonic saline: Comparative analysis of two PET studies
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Manuscript (Other academic)
Identifiers
urn:nbn:se:umu:diva-4639 (URN)
Available from: 2005-08-23 Created: 2005-08-23 Last updated: 2010-01-13Bibliographically approved

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