Neuroplasticity and Brachial Plexus Injury

Neuroplasticity and Brachial Plexus Injury

Accepted Manuscript Neuroplasticity and brachial plexus injury Kathleen Joy Khu, MD PII: S1878-8750(15)00813-X DOI: 10.1016/j.wneu.2015.06.065 Ref...

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Accepted Manuscript Neuroplasticity and brachial plexus injury Kathleen Joy Khu, MD PII:

S1878-8750(15)00813-X

DOI:

10.1016/j.wneu.2015.06.065

Reference:

WNEU 3017

To appear in:

World Neurosurgery

Received Date: 27 June 2015 Accepted Date: 27 June 2015

Please cite this article as: Khu KJ, Neuroplasticity and brachial plexus injury, World Neurosurgery (2015), doi: 10.1016/j.wneu.2015.06.065. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

Neuroplasticity and brachial plexus injury

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A commentary

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ACCEPTED MANUSCRIPT

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Kathleen Joy Khu, MD

Section of Neurosurgery, Department of Clinical Neurosciences University of the Philippines, Philippine General Hospital Manila, Philippines

Telephone: +6325242338 Email: [email protected]

ACCEPTED MANUSCRIPT NEUROPLASTICITY AND BRACHIAL PLEXUS INJURY

The human nervous system is a wonderful thing. Because of a phenomenon called plasticity, lost function could be regained after injury or illness. This is

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achieved not by direct repair of damaged neurons, but by reorganization and formation of new connections between intact neurons, resulting in compensation or functional substitution.

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Neuroplasticity is defined as the ability of the central nervous system to adapt and modify its structural organization and function as an adaptive response to

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functional demand (1). Because of this property, brain function is dynamic rather than static, allowing it to adapt and change in response to both physiologic and pathologic stimuli. The mechanisms involved include changes in cortical maps, as well as anatomic changes such as collateral sprouting, synaptic changes, and adaptations in

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neuronal properties (4). In terms of physiologic adaptation, it has been found that behaviorally relevant stimulation and motor learning could lead to expansion of the topographical representation of trained areas within the motor cortex (9), changes that

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result from altered anatomy and physiology at the cellular level (6). On the other hand, injury to the nervous system results in a greater extent and larger scale of

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cortical change, referred to as cortical remapping or cortical reorganization. This has been found to occur in stroke, amputation, spinal cord injury, and other pathologies of the nervous system.

Marked cortical rearrangement has been observed following limb amputation

or deafferentiation. After an amputation, the brain’s motor and somatosensory cortex do not receive input from the amputated limb; consequently, neighboring regions supplying intact structures expand, increasing their territory within the cortex (2). This results in a “remapped” cortex. A similar phenomenon is observed in recovery

ACCEPTED MANUSCRIPT after stroke. New structural and functional circuits are formed through cortical reorganization, enabling regions of the brain with partial function to recover in a matter of days to weeks through remapping (8). Injury to the nervous system temporarily enhances neuroplasticity. The

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mechanisms contributing to this have not been fully elucidated, but they are believed to include injury-induced transient upregulation of so-called immediate early genes, neurotropic factors, and the downregulation of growth-inhibitory components such as

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chondroitin sulfate proteoglycans (CSPG) found within the perineuronal net (4). In addition, sensory deprivation to the cortex plays an important role in cortical

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remapping (2). It has been theorized that the loss of sensory feedback from the periphery may lead to reduction of inhibitory potentials to surrounding cortex, eventually allowing cortical reorganization (5).

Recovery after brachial plexus injury is a function not only of nerve

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regeneration, but also cortical reorganization. The latter has been studied by several authors using functional MRI (fMRI) (2,7,10,11). Yoshikawa and colleagues (11) performed a series of functional MRI’s on a small group of patients with brachial

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plexus injury, the first one prior to brachial plexus repair and the subsequent ones

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approximately one, two, and three years post-injury. They found changes in sensorimotor cortex (SMC) activation during the motor task of elbow flexion over time, illustrating cortical reorganization. There was a decrease in SMC activation at three months and at one year post-injury, which the authors attributed to the lack of neural input/output signals from the periphery. However, there was a concomitant increase in SMC activation during the second and third year post-injury in patients who exhibited clinical improvement in motor strength (11). Mallesy and co-workers (7) also reported poor cortical activation on fMRI prior to brachial plexus repair, but

ACCEPTED MANUSCRIPT when they performed fMRI on recovering patients several months post-operatively, they found that activation in the primary motor cortex contralateral to the affected side did not differ significantly from the unaffected side during elbow flexion task. Cortical reorganization was also demonstrated after intercostal to musculocutaneous

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nerve transfer using fMRI and diffusion tensor imaging (DTI) performed pre- and post-operatively (10).

Despite the number of previous fMRI studies investigating cortical

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reorganization after brachial plexus injury, Feng et al (3) are the first to compare the functional reorganization of the brain in dominant versus non-dominant brachial

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plexus injuries. The authors found that injury to the dominant upper limb induced a greater degree of cortical reorganization, presumably because there is a need for the non-dominant limb to learn to perform activities that were previously done by the dominant limb. In contrast, injury to the non-dominant limb also resulted in some

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degree of cortical reorganization, but not to the same extent as the dominant limb. This may be due to the fact that the non-dominant limb performed fewer independent actions and acted more as a “helping hand” to the dominant limb. It was also

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interesting to note that reorganization was not limited to areas subserving motor

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function, but also involved higher order recognition-related cortical regions. This implies that cognition and learning are important components of the adaptive changes in the brain after injury. This is an interesting paper describing the patterns of cortical reorganization

after dominant versus non-dominant brachial plexus injuries in right-handed individuals. However, it would also be helpful to know if the patients underwent brachial plexus repair surgery, if they exhibited clinical improvement over time, if serial fMRI showed further changes in cortical reorganization, and if the fMRI

ACCEPTED MANUSCRIPT findings could be correlated to clinical improvement. In addition, would the patterns of cortical reorganization be similar in left-handed patients? Perhaps the authors’ protocol could be used to expand the study further in terms of sample size,

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longitudinal follow-up, and handedness.

REFERENCES

1. Bach-y-Rita P: Brain plasticity as a basis for recovery of function in humans.

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Neuropsychologia 28:547-554, 1990.

2. Dimou S, Biggs M, Tonkin M, Hickie IB, Lagopoulos J: Motor cortex

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neuroplasticity following brachial plexus transfer. Front Hum Neurosci 7:500, 2013. doi: 10.3389/fnhum.2013.00500. eCollection 2013. 3. Feng JT, Liu HQ, Xu JG, Gu YD, Shen YD: Differences in brain adaptive functional reorganization in right and left total brachial plexus injury patients.

ahead of print]

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World Neurosurg 2015 Apr 29. doi: 10.1016/j.wneu.2015.04.046. [Epub

4. Fouad K, Forero J, Hurd C: A simple analogy for nervous system plasticity

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after injury. Exerc Sport Sci Rev 43:100-106, 2015.

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5. Hallett M: Plasticity of the human motor cortex and recovery from stroke. Brain Res Rev 36:169-174, 2001.

6. Kleim JA, Lussnig E, Schwarz ER, Comery TA, Greenough WT: Synaptogenesis and FOS expression in the motor cortex of the adult rat after motor skill learning. J Neurosci 16:4529-4535, 1996. 7. Malessy MJ, Bakker D, Dekker AJ, Van Duk JG, Thomeer RT: Functional magnetic resonance imaging and control over the biceps muscle after intercostal-musculocutaneous nerve transfer. J Neurosurg 98:261-268, 2003.

ACCEPTED MANUSCRIPT 8. Murphy TH, Corbett D: Plasticity during stroke recovery: from synapse to behaviour. Nat Rev Neurosci 10:861-872, 2009. 9. Remple MS, Bruneau RM, Van den Berg PM, Goertzen C, Kleim JA: Sensitivity of cortical movement representations to motor experience:

reorganization. Behav Brain Res 123:133-141, 2001.

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evidence that skill learning but not strength training induces cortical

10. Sokki AM, Bhat DI, Devi BI: Cortical reorganization following neurotization:

Neurosurgery 70:1305-1311, 2012.

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a diffusion tensor imaging and functional magnetic resonance imaging study.

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11. Yoshikawa T, Hayashi N, Tajiri Y, Satake Y, Ohtomo K: Brain reorganization in patients with brachial plexus injury: a longitudinal functional MRI study. Scientific World Journal 2012:501751. doi: 10.1100/2012/501751. Epub 2012

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Neuroplasticity and brachial plexus injury

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A commentary

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ACCEPTED MANUSCRIPT

Kathleen Joy Khu, MD

Section of Neurosurgery, Department of Clinical Neurosciences University of the Philippines, Philippine General Hospital Manila, Philippines Telephone: +6325242338 Email: [email protected]

ACCEPTED MANUSCRIPT HIGHLIGHTS: Neuroplasticity contributes to return of function after injury to the nervous system



Neuroplasticity can range from cellular changes to changes in cortical maps



Injury to the nervous system results in cortical reorganization or cortical remapping



Cortical reorganization has been illustrated by several authors using functional MRI

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