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Experimental studies of spinal mechanisms associated with muscle fatigue
Umeå University, Faculty of Medicine, Department of Surgical and Perioperative Sciences, Sports Medicine.
2004 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Muscle fatigue is ubiquitous in every day life.Muscle fatigue might be considered as an altered state of motor behaviour, which impairs motor performance. By contrast, muscle fatigue could also be considered a positive phenomenon, which protects muscle tissue from damage that might be incurred to it by overuse.

The principal aim of the thesis was to explore some of the mechanisms of muscle fatigue at the spinal level in animal models.The activation of multiple motor units of a single calf muscle may influence contractile properties of its neighbouring, otherwise inactive units, providing evidence for spatial spreading of fatigue between different muscle parts. The release of metabolites, their action on inactive muscle units and the effects of local hypoxia are the most likely causes. Fatigue-induced metabolite shift in the interstitium provokes excitation and/or sensitisation of high-threshold afferent fibers, with complex effects on the spinal premotoneuronal network involved in the modulation of motoneuronal output. This was examined by studing the intrasegmental lamellar distribution of the lumbar spinal interneurons following fatiguing contractions of the triceps surae muscle. Furthermore, fatigue of calf muscles enhanced the activity of fusimotor neurons to these muscles irrespective of the regime of muscle activity (isometric vs. lengthening) in conditions that simulate locomotion. Altered fusimotor activity, through increased or maintained muscle spindle afferent responsiveness may be advantageous, providing support to the skeletomotor activity and enhanced information about muscle periphery to higher nervous centres. The particular effects of interneuronal network at motor input (presynaptic inhibition system) and output (recurrent inhibition system) stages were then addressed. Fatigue of triceps surae muscle induced a suppression of the monosynaptic reflex. The intensity of presynaptic inhibition increased, while the intensity of recurrent inhibition decreased. Post fatigue-evoked changes in monosynaptic reflexes and presynaptic inhibition indicate the possibility that high-threshold afferents inhibit group Ia terminals pre-synaptically, which would allow fatigue-induced signals from the muscle to reduce the relevance of proprioceptive feedback. Besides intrasegmental, intersegmental spreading of nociceptive signals was explored. Activation of sensory afferents from dorsal neck muscles by capsaicin induces powerful activation of interneurons located in the cervical spinal cord, as well as a widespread activation of cells in lumbar spinal cord segments.

The results confirm the pivotal role of small diameter muscle afferents in the orchestration of segmental responses to fatigue and show complex interactions that may lead to limited accuracy of motor output. They also depict processes that may be related to, and even become precursors of chronic muscle pain.

Place, publisher, year, edition, pages
2004.
Series
Umeå University medical dissertations, ISSN 0346-6612 ; 910
Keyword [en]
muscle fatigue, monosynaptic reflex, presynaptic inhibition, recurrent inhibition, fusimotor system, Fos-immunoreactivity, referral pain
Research subject
Surgery
Identifiers
URN: urn:nbn:se:umu:diva-332ISBN: 91-7305-703-7 (print)OAI: oai:DiVA.org:umu-332DiVA: diva2:143137
Public defence
2004-11-12, Stora salen, Arbetslivsinstitutet, 13:00
Opponent
Available from: 2004-10-08 Created: 2004-10-08 Last updated: 2010-06-28Bibliographically approved
List of papers
1. Spreading of fatigue-related effects from active to inactive parts in the medial gastrocnemius muscle of the cat
Open this publication in new window or tab >>Spreading of fatigue-related effects from active to inactive parts in the medial gastrocnemius muscle of the cat
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2002 (English)In: European Journal of Applied Physiology, ISSN 1439-6319, E-ISSN 1439-6327, Vol. 86, no 4, 295-307 p.Article in journal (Refereed) Published
Abstract [en]

In the medial gastrocnemius muscle of the decerebrate cat, the spatial spread of fatigue between active and inactive muscle parts was studied. Conditioning fatiguing stimulation (CFS) was applied to a part of the muscle to test whether it had an effect on the contraction efficiency in an unstimulated part. To exclude somato-sympathetic reflexes during CFS, a full rhizotomy of the lumbo-sacral spinal cord was performed. The same ipsilateral ventral root, either L7 or S1, was divided into seven filaments, one of which was used for the test stimulation, and four or five for CFS. The CFS consisted of 12 s sessions of distributed stimulation of five (or four) filaments at a rate of 40 s(-1), the sessions were repeated, every 40 s, 15 or more times. The test consisted of 12 s of regular stimulation at a rate of 10 s(-1), preceded and followed by a single stimulus. The tests applied just after CFS showed a strong decline of both tension and electromyogram (EMG), amounting to only [mean (SD)] 0.45 (0.18) and 0.51 (0.19) (n = 15), respectively, of the corresponding values in the tests before CFS. It thus turned out that depressive fatigue-related effects could spread within the muscle. At the same time, control reactions recorded in the lateral gastrocnemius during stimulation of its cut nerve did not change. Subsequent repetitions of the tests usually revealed a tendency towards restoration. The EMG reactions recovered more quickly than tension. The depression of EMG after CFS was accompanied by a slowing of the constituent M-waves; their latencies decreased during restoration. Distinct changes in the systemic blood pressure were observed during CFS. These changes were usually correlated well with muscle tension changes. The factors possibly underlying the observed effects may include diffusion of metabolites from active to inactive muscle fibres, lowering of the efficiency of neuro-muscular transmission due to squeezing of efferent motor terminals and changes in outer metabolite content, as well as local hypoxia due to increases in intramuscular pressure.

Keyword
Muscle fatigue, Electromyography, Blood pressure, Interstitium, Ischaemia
National Category
Medical and Health Sciences
Identifiers
urn:nbn:se:umu:diva-4149 (URN)10.1007/s00421-001-0550-8 (DOI)11990742 (PubMedID)
Available from: 2004-10-08 Created: 2004-10-08 Last updated: 2010-06-28Bibliographically approved
2. c-fos expression and NADPH-d reactivity in spinal neurons after fatiguing stimulation of hindlimb muscles in the rat
Open this publication in new window or tab >>c-fos expression and NADPH-d reactivity in spinal neurons after fatiguing stimulation of hindlimb muscles in the rat
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2001 (English)In: Brain Research, ISSN 0006-8993, E-ISSN 1872-6240, Vol. 923, no 1-2, 91-102 p.Article in journal (Refereed) Published
Abstract [en]

The distribution of Fos-immunoreactive (Fos-ir) and nicotinamide adenine dinucleotide phosphate-diaphorase (NADPH-d)-reactive neurons in the rat lumbar spinal cord was examined following muscle fatigue caused by intermittent high-rate (100 s(-1)) electrical stimulation of the triceps surae muscle or the ventral root L5 (VRL5) for 30 min. Following both types of stimulation, the fatigue-related c-fos gene expression was more extensive in the L2-L5 segments on the stimulated side, and the majority of Fos-ir neurons were concentrated in the dorsal horn. After direct muscle stimulation, the highest number of Fos-ir neurons were detected in two regions: layer 5, and superficial layers (1 and 2(o)), although many labeled cells were also found in layers 3, 4, 6, and 7. In response to VRL5 stimulation, the maximal density of Fos-ir neurons was detected in the middle and lateral parts of layers 1 and 2(o), the zone of termination of high-threshold muscle afferents(.) Statistically significant prevalence of Fos-ir cell number was also found in layers 5 and 7 on the stimulated side. A few Fos-ir neurons were detected in the ventral horn (layer 8 and area 10) on both sides. The lamellar distribution of NADPH-d-reactive neurons was similar over all experimental groups of animals. In the L3-L6 segments, such reactive cells were arranged in two distinct regions: dorsal horn (layers 2(i), 3, and 5) and area 10; in the L1 and L2 segments, an additional cluster of NADPH-d positive cells was found in the intermediolateral cell column (IML). Double-labeled cells were not detected. We suggest that c-fos expression in response to muscle fatigue reveals activity of functionally different types of spinal neurons which could operate together with NOS-containing cells in pre-motoneuronal networks to modulate the motoneuron output.

National Category
Medical and Health Sciences
Identifiers
urn:nbn:se:umu:diva-4150 (URN)10.1016/S0006-8993(01)03049-9 (DOI)11743976 (PubMedID)
Available from: 2004-10-08 Created: 2004-10-08 Last updated: 2010-06-28Bibliographically approved
3. Changes in fusimotor activity during repetitive lengthening muscle contractions in decerebrate cats
Open this publication in new window or tab >>Changes in fusimotor activity during repetitive lengthening muscle contractions in decerebrate cats
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1998 (English)In: Neuroscience, ISSN 0306-4522, E-ISSN 1873-7544, Vol. 86, no 4, 1337-1342 p.Article in journal (Refereed) Published
Abstract [en]

Responses of fusimotor neurons to lengthening vs isometric contractions have been studied in decerebrate cats. Spike discharges of fusimotor neurons to the medial gastrocnemius muscle were recorded from this muscle nerve filament during sequences of contractions and/or stretches of the lateral gastrocnemius and soleus muscles. The sequences lasted for 250-450s (duty cycle 4:2 s). Isometric contractions were elicited by electrical stimulation (40 Hz, 1.3 times motor threshold) of the muscle nerves. Lengthening contractions were elicited in the same way while the muscles were stretched by 4 mm at a velocity of 1 mm/s. Of 25 fusimotor neurons studied, 23 responded to muscle contractions with an increase in firing rate, subsiding towards the end of the sequence. The increase was either modulated with each subsequent contraction or smooth throughout the sequence. Approximately 64% of fusimotor neurons, responding to muscle contractions, responded in a similar way to the sequences of muscle stretches, applied alone. Responses to sequences of the lengthening contractions were significantly larger, on average, than those to the isometric ones, but smaller than the sum of the responses to the contractions and stretches applied separately. On the other hand, they were also larger in fusimotor units, showing no overt responses to muscle stretches alone.

Keyword
fusimotor neurons, muscle contraction, muscle stretch
National Category
Medical and Health Sciences
Identifiers
urn:nbn:se:umu:diva-4151 (URN)10.1016/S0306-4522(98)00122-5 (DOI)9697137 (PubMedID)
Available from: 2004-10-08 Created: 2004-10-08 Last updated: 2010-06-29Bibliographically approved
4. Effects of cutaneous afferent input on fatigue-induced changes in fusimotor activity of decerebrate cats
Open this publication in new window or tab >>Effects of cutaneous afferent input on fatigue-induced changes in fusimotor activity of decerebrate cats
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1997 (English)In: Neuroscience, ISSN 0306-4522, E-ISSN 1873-7544, Vol. 79, no 3, 935-942 p.Article in journal (Refereed) Published
Abstract [en]

Interaction of cutaneous and small-diameter, primarily fatigue-induced, muscle afferent inputs on fusimotor neurons has been studied in decerebrate cats. Spike discharges of fusimotor neurons to medial gastrocnemius were recorded from filaments dissected free from this muscle nerve. Non-noxious mechanical stimuli (10 Hz, 2 mm vibration) were applied to the skin area on the lateral side of the heel, innervated by sural nerve, during long-lasting (250 s) fatiguing contraction of lateral gastrocnemius and soleus muscles, elicited by electrical stimulation (40 Hz, 1.3 x motor threshold) of the muscle nerves. In 15 units (58%) the pattern of responses to muscle contraction and/or fatigue (initial transient, and late long-lasting increase in firing rate, respectively) was preserved in the presence of skin vibration which, by itself, provoked either a slight increase or no changes in fusimotor discharge rate. Pattern of the response to skin vibration prevailed in the presence of muscle contraction and fatigue only if the vibration by itself induced marked increase in fusimotor discharge rate (three units). In the remaining eight units the responses to both stimuli applied simultaneously were dissimilar in pattern to the response to either stimulus applied alone: the initial, tension-related, increase in firing rate was prolonged, while the late, fatigue-induced one was attenuated and its post-contraction part almost abolished. Possible mechanisms and functional role of interaction between cutaneous and muscle afferent inflows are discussed.

Keyword
muscle fatigue, fusimotor neurons, cutaneous afferents
National Category
Medical and Health Sciences
Identifiers
urn:nbn:se:umu:diva-4152 (URN)10.1016/S0306-4522(97)00039-0 (DOI)9219956 (PubMedID)
Available from: 2004-10-08 Created: 2004-10-08 Last updated: 2010-06-29Bibliographically approved
5. Fatigue-related depression of the feline monosynaptic gastrocnemius-soleus reflex
Open this publication in new window or tab >>Fatigue-related depression of the feline monosynaptic gastrocnemius-soleus reflex
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2004 (English)In: Journal of Physiology, ISSN 0022-3751, E-ISSN 1469-7793, Vol. 556, no 1, 293-296 p.Article in journal (Refereed) Published
Abstract [en]

In decerebrate cats, changes in the monosynaptic reflex (MSR) of gastrocnemius-soleus (G-S) motoneurones were studied after fatiguing stimulation (FST) of the G-S muscles. Monosynaptic reflexes were evoked by stimulation of Ia fibres in the G-S nerve and recorded from a filament of ventral root (VR) L7. FST (intermittent 40 s(-1) stimulation for 10-12 min) was applied to the distal part of the cut VR S1. FST reduced MSR amplitudes to 0.64 +/- 0.04 (mean +/-s.e.m.) of the prefatigue values. The suppression remained stable for approximately 25 min and then MSR amplitudes gradually returned towards the normal. To test for the involvement of presynaptic and recurrent inhibition, MSRs were conditioned by stimulation of the nerve to the posterior biceps and semitendinosus (PBSt) muscles or a filament of VR L7, respectively. The intensity of presynaptic inhibition (reduction of the normalized value of MSR amplitude during conditioning) increased from 0.19 +/- 0.02 in prefatigue to 0.44 +/- 0.04 within a 5.3-18.2 min interval after FST, followed by a recovery. In contrast, the intensity of recurrent inhibition first diminished from 0.23 +/- 0.02 in prefatigue to 0.15 +/- 0.01 within 15.6-30.1 min after FST and then gradually recovered. Both primary afferent depolarization and the intensity of antidromic discharges in primary afferents increased with the presynaptic inhibition intensity. These results demonstrate a fatigue-related suppression of Ia excitation of synergistic motoneurones, probably arising from the activation of group III and IV afferents. The effects could in part be due to increased presynaptic inhibition, while recurrent inhibition plays a minor role.

Place, publisher, year, edition, pages
London: Cambridge U. P., 2004
Keyword
Animals, Cats, Decerebrate State, Electric Stimulation, Female, Hindlimb, Male, Muscle Fatigue/*physiology, Muscle; Skeletal/innervation/*physiology, Nerve Fibers/physiology, Neural Inhibition, Presynaptic Terminals/physiology, Reflex; Monosynaptic/*physiology, Time Factors
National Category
Medical and Health Sciences
Identifiers
urn:nbn:se:umu:diva-4153 (URN)10.1113/jphysiol.2003.053249 (DOI)14645451 (PubMedID)
Available from: 2004-10-08 Created: 2004-10-08 Last updated: 2011-03-14Bibliographically approved
6. Distinctive pattern of c-fos expression in the feline cervico-lumbar spinal cord after stimulation of vanilloid receptors in dorsal neck muscles
Open this publication in new window or tab >>Distinctive pattern of c-fos expression in the feline cervico-lumbar spinal cord after stimulation of vanilloid receptors in dorsal neck muscles
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2004 (English)In: Neuroscience Letters, ISSN 0304-3940, E-ISSN 1872-7972, Vol. 364, no 2, 94-97 p.Article in journal (Refereed) Published
Abstract [en]

In the present study, c-fos expression in the spinal cord has been used as a marker of neuronal activation induced by capsaicin-sensitive sensory afferents from the dorsal neck muscles in cats (n = 6). The number of Fos-immunoreactive neurons, which were revealed using the avidin-biotin-peroxidase method, was significantly increased in the cervical and lumbar spinal cord. In contrast to the control group (n = 3), 2 h after intramuscular capsaicin injection, c-fos expression was more extensive ipsilaterally to the injected side in the C3-C6 segments, and bilaterally in the L4-L6 segments. Most labeled neurons in the cervical spinal cord were small and giant cells, predominantly located in the middle and lateral parts of lamina I and, additionally, at the neck of the dorsal horn (lamina V), i.e., within the zones of termination of high-threshold muscle afferents. The widespread distribution of labeled cells throughout the cervical cord within the intermediate zone (lamina VII) coincided with the sites of last-order premotor interneurons and cells of origin of long crossed and uncrossed descending propriospinal pathways to the lumbar spinal cord. These findings suggest possible mechanisms for spreading of nociceptive signals between cervical and lumbar regions.

Place, publisher, year, edition, pages
Amsterdam: Elsevier Science, 2004
Keyword
Animals, Capsaicin/administration & dosage/pharmacology, Cats, Cell Size, Cervical Vertebrae, Female, Genes; fos/*genetics, Histocytochemistry, Injections, Lumbar Vertebrae, Male, Neck Muscles/innervation/metabolism/*physiology, Neural Pathways/physiology, Pain/physiopathology, Receptors; Drug/*agonists, Spinal Cord/*metabolism, Stimulation; Chemical
National Category
Medical and Health Sciences
Identifiers
urn:nbn:se:umu:diva-4154 (URN)10.1016/j.neulet.2004.04.019 (DOI)15196685 (PubMedID)
Available from: 2004-10-08 Created: 2004-10-08 Last updated: 2011-04-04Bibliographically approved

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