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Structural and functional changes in the brain after surgically repaired median nerve injury
Umeå University, Faculty of Medicine, Department of Integrative Medical Biology (IMB), Physiology. Umeå University, Faculty of Medicine, Department of Surgical and Perioperative Sciences, Hand Surgery.
2019 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Despite the best available surgical repair, traumatic median nerve injury within the forearm typically causes lifelong impairment in hand function. This stems from an inadequate reinnervation of the nerves supporting sensory functions of the thumb, index and long finger, and of nerves supplying intrinsic hand muscles. This thesis examines whether median nerve injuries can cause structural and functional changes in the brain. Understanding such changes can help the development of new treatments for improved recovery of hand function.

The first study introduces a novel apparatus and paradigm for examining tactile neural processing with fMRI under well-controlled behavioral conditions. The scientific issue challenged was whether, in healthy adults, different cortical areas could be involved in processing tactile stimuli depending on their temporal frequency content. In a threshold-tracking paradigm, the participants’ task was to detect oscillatory mechanical stimulations of various frequencies delivered to the tip of either left or right middle finger. Regardless of stimulated hand, tactile detection of audible frequencies (20 and 100 Hz) engaged the left auditory cortex while detection of slow object displacements (3 Hz) engaged visual cortex. These results corroborate and advance the metamodal theory of brain function, which posits that brain areas can contribute to sensory processing by performing specific computations – those for which they are specialized – regardless of input modality.

The second and third studies concern structural and functional changes in the brain of adults with one reinnervated hand after an injury transecting the median nerve in the forearm. Healthy individuals matched for sex, handedness and age served as controls. Irrespective of side of injury (left or right), voxel-based morphometry applied on T1 MR-images revealed reductions of gray matter in the left ventral and right dorsal premotor cortex, and reductions of white matter in related commissural pathways. We interpreted these as activity-dependent structural adaptations to reduced neural processing linked to restrictions in the diversity of the natural manual dexterity repertoire caused by a disturbed innervation of the hand. Conversely, increases in gray matter were observed bilaterally in a motion-processing visual cortical area. We interpreted this as a structural manifestation of increased neural processing linked to greater dependence on vision for controlling manual dexterity due to impaired tactile innervation of the affected hand.

To reveal functional changes in tactile cortical processing after median nerve reinnervation, we recorded brain activity using fMRI when study participants performed perceptually demanding tactile threshold-tracking and oddball detection tasks with our novel apparatus. The hand representation of the contralesional primary somatosensory cortex (S1) showed greater activity compared to the controls when the reinnervated index finger was engaged in the tasks, but strikingly also when fingers of both hands innervated by uninjured nerves were engaged, i.e., little finger of the reinnervated hand and index and little finger of the other hand. The generally increased activity indicates a general disinhibition of contralateral S1, suggesting that increased functional reorganization is an ongoing process of chronic nerve injury. In addition, prefrontal areas implicated in processes that support decision-making and response selection showed increased activity, suggesting that such processes were more computationally demanding after nerve injury.

Together, these results indicate that brain areas can undergo significant changes after peripheral nerve injury, even when followed by best available surgical repair and reinnervation conditions. These changes can include activity-dependent structural adaptations consisting of either regional decreases or increases in gray matter concentration, which likely depend on an area's functional specialization and on changes in its processing load due to behavioral constraints imposed by the injury. Moreover, the results also suggest that the affected hand's primary cortical projection area is still in a state of ongoing functional reorganization despite the fact that peripheral reinnervation of the hand should have been completed long ago, which should inspire the development of new therapeutic regimens for what today is considered a chronic impairment.

Place, publisher, year, edition, pages
Umeå: Umeå universitet , 2019. , p. 98
Series
Umeå University medical dissertations, ISSN 0346-6612 ; 2035
Keywords [en]
Humans, Hand, Touch, Peripheral nerve injury, Magnetic resonance imaging, Somatosensory Cortex, Cortical plasticity
National Category
Physiology
Research subject
Physiology; hand surgery 
Identifiers
URN: urn:nbn:se:umu:diva-159149ISBN: 978-91-7855-072-2 (print)OAI: oai:DiVA.org:umu-159149DiVA, id: diva2:1316650
Public defence
2019-06-13, Aula Anatomica (Hörsal BIO.A.206), Biologihuset, Umeå, 13:00 (English)
Opponent
Supervisors
Available from: 2019-05-23 Created: 2019-05-20 Last updated: 2019-05-22Bibliographically approved
List of papers
1. BOLD Responses to Tactile Stimuli in Visual and Auditory Cortex Depend on the Frequency Content of Stimulation
Open this publication in new window or tab >>BOLD Responses to Tactile Stimuli in Visual and Auditory Cortex Depend on the Frequency Content of Stimulation
2012 (English)In: Journal of cognitive neuroscience, ISSN 0898-929X, E-ISSN 1530-8898, Vol. 24, no 10, p. 2120-2134Article in journal (Refereed) Published
Abstract [en]

Although some brain areas preferentially process information from a particular sensory modality, these areas can also respond to other modalities. Here we used fMRI to show that such responsiveness to tactile stimuli depends on the temporal frequency of stimulation. Participants performed a tactile threshold-tracking task where the tip of either their left or right middle finger was stimulated at 3, 20, or 100 Hz. Whole-brain analysis revealed an effect of stimulus frequency in two regions: the auditory cortex and the visual cortex. The BOLD response in the auditory cortex was stronger during stimulation at hearable frequencies (20 and 100 Hz) whereas the response in the visual cortex was suppressed at infrasonic frequencies (3 Hz). Regardless of which hand was stimulated, the frequency-dependent effects were lateralized to the left auditory cortex and the right visual cortex. Furthermore, the frequency-dependent effects in both areas were abolished when the participants performed a visual task while receiving identical tactile stimulation as in the tactile threshold-tracking task. We interpret these findings in the context of the metamodal theory of brain function, which posits that brain areas contribute to sensory processing by performing specific computations regardless of input modality.

Place, publisher, year, edition, pages
Cambridge: MIT Press, 2012
National Category
Neurosciences
Identifiers
urn:nbn:se:umu:diva-60309 (URN)10.1162/jocn_a_00261 (DOI)000308422200012 ()
Available from: 2012-11-09 Created: 2012-10-09 Last updated: 2019-05-20Bibliographically approved
2. Structural changes in hand related cortical areas after median nerve injury and repair
Open this publication in new window or tab >>Structural changes in hand related cortical areas after median nerve injury and repair
2018 (English)In: Scientific Reports, ISSN 2045-2322, E-ISSN 2045-2322, Vol. 8, article id 4485Article in journal (Refereed) Published
Abstract [en]

Transection of the median nerve typically causes lifelong restriction of fine sensory and motor skills of the affected hand despite the best available surgical treatment. Inspired by recent findings on activity-dependent structural plasticity of the adult brain, we used voxel-based morphometry to analyze the brains of 16 right-handed adults who more than two years earlier had suffered injury to the left or right median nerve followed by microsurgical repair. Healthy individuals served as matched controls. Irrespective of side of injury, we observed gray matter reductions in left ventral and right dorsal premotor cortex, and white matter reductions in commissural pathways interconnecting those motor areas. Only left-side injured participants showed gray matter reduction in the hand area of the contralesional primary motor cortex. We interpret these effects as structural manifestations of reduced neural processing linked to restrictions in the diversity of the natural manual dexterity repertoire. Furthermore, irrespective of side of injury, we observed gray matter increases bilaterally in a motion-processing visual area. We interpret this finding as a consequence of increased neural processing linked to greater dependence on vision for control of manual dexterity after median nerve injury because of a compromised somatosensory innervation of the affected hand.

Place, publisher, year, edition, pages
Nature Publishing Group, 2018
National Category
Neurosciences
Identifiers
urn:nbn:se:umu:diva-146441 (URN)10.1038/s41598-018-22792-x (DOI)000427366200015 ()29540748 (PubMedID)
Available from: 2018-05-04 Created: 2018-05-04 Last updated: 2019-05-20Bibliographically approved
3. Disinhibition of human primary somatosensory cortex after median nerve transection and reinnervation
Open this publication in new window or tab >>Disinhibition of human primary somatosensory cortex after median nerve transection and reinnervation
(English)Manuscript (preprint) (Other academic)
National Category
Physiology
Research subject
Physiology
Identifiers
urn:nbn:se:umu:diva-159147 (URN)
Available from: 2019-05-20 Created: 2019-05-20 Last updated: 2019-05-20

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