White matter

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White matter
Grey matter and white matter - very high mag.jpg
Micrograph showing white matter with its characteristic fine meshwork-like appearance (left of image – lighter shade of pink) and grey matter, with the characteristic neuronal cell bodies (right of image – dark shade of pink). HPS stain.
Human brain right dissected lateral view description.JPG
Human brain right dissected lateral view, showing grey matter (the darker outer parts), and white matter (the inner and prominently whiter parts).
Details
Location Central nervous system
Identifiers
Latin substantia alba
MeSH D066127
TA98 A14.1.00.009
A14.1.02.024
A14.1.02.201
A14.1.04.101
A14.1.05.102
A14.1.05.302
A14.1.06.201
TA2 5366
FMA 83929
Anatomical terminology
White matter structure of human brain (taken by MRI). 3DSlicer-KubickiJPR2007-fig6.jpg
White matter structure of human brain (taken by MRI).

White matter refers to areas of the central nervous system (CNS) that are mainly made up of myelinated axons, also called tracts. [1] Long thought to be passive tissue, white matter affects learning and brain functions, modulating the distribution of action potentials, acting as a relay and coordinating communication between different brain regions. [2]

Contents

White matter is named for its relatively light appearance resulting from the lipid content of myelin. However, the tissue of the freshly cut brain appears pinkish-white to the naked eye because myelin is composed largely of lipid tissue veined with capillaries. Its white color in prepared specimens is due to its usual preservation in formaldehyde.

Structure

White matter

White matter is composed of bundles, which connect various grey matter areas (the locations of nerve cell bodies) of the brain to each other, and carry nerve impulses between neurons. Myelin acts as an insulator, which allows electrical signals to jump, rather than coursing through the axon, increasing the speed of transmission of all nerve signals. [3]

The total number of long range fibers within a cerebral hemisphere is 2% of the total number of cortico-cortical fibers (across cortical areas) and is roughly the same number as those that communicate between the two hemispheres in the brain's largest white tissue structure, the corpus callosum. [4] Schüz and Braitenberg note "As a rough rule, the number of fibres of a certain range of lengths is inversely proportional to their length." [4]

The proportion of blood vessels in the white matter in nonelderly adults is 1.7–3.6%. [5]

Grey matter

The other main component of the brain is grey matter (actually pinkish tan due to blood capillaries), which is composed of neurons. The substantia nigra is a third colored component found in the brain that appears darker due to higher levels of melanin in dopaminergic neurons than its nearby areas. Note that white matter can sometimes appear darker than grey matter on a microscope slide because of the type of stain used. Cerebral and spinal white matter do not contain dendrites, neural cell bodies, or shorter axons,[ citation needed ] which can only be found in grey matter.

Location

White matter forms the bulk of the deep parts of the brain and the superficial parts of the spinal cord. Aggregates of grey matter such as the basal ganglia (caudate nucleus, putamen, globus pallidus, substantia nigra, subthalamic nucleus, nucleus accumbens) and brainstem nuclei (red nucleus, cranial nerve nuclei) are spread within the cerebral white matter.

The cerebellum is structured in a similar manner as the cerebrum, with a superficial mantle of cerebellar cortex, deep cerebellar white matter (called the "arbor vitae") and aggregates of grey matter surrounded by deep cerebellar white matter (dentate nucleus, globose nucleus, emboliform nucleus, and fastigial nucleus). The fluid-filled cerebral ventricles (lateral ventricles, third ventricle, cerebral aqueduct, fourth ventricle) are also located deep within the cerebral white matter.

Myelinated axon length

Men have more white matter than women both in volume and in length of myelinated axons. At the age of 20, the total length of myelinated fibers in men is 176,000 km while that of a woman is 149,000 km. [6] There is a decline in total length with age of about 10% each decade such that a man at 80 years of age has 97,200 km and a woman 82,000 km. [6] Most of this reduction is due to the loss of thinner fibers. However, this study only included 36 participants. [6]

Function

White matter is the tissue through which messages pass between different areas of grey matter within the central nervous system. The white matter is white because of the fatty substance (myelin) that surrounds the nerve fibers (axons). This myelin is found in almost all long nerve fibers, and acts as an electrical insulation. This is important because it allows the messages to pass quickly from place to place.

Unlike grey matter, which peaks in development in a person's twenties, the white matter continues to develop, and peaks in middle age. [7]

Research

Multiple sclerosis (MS) is the most common of the inflammatory demyelinating diseases of the central nervous system which affect white matter. In MS lesions, the myelin sheath around the axons is deteriorated by inflammation. [8] Alcohol use disorders are associated with a decrease in white matter volume. [9]

Amyloid plaques in white matter may be associated with Alzheimer's disease and other neurodegenerative diseases. [10] Other changes that commonly occur with age include the development of leukoaraiosis, which is a rarefaction of the white matter that can be correlated with a variety of conditions, including loss of myelin pallor, axonal loss, and diminished restrictive function of the blood–brain barrier. [11]

There is also evidence that substance abuse may damage white matter microstructure, though prolonged abstinence may in certain cases reverse such white matter changes. [12]

White matter lesions on magnetic resonance imaging are linked to several adverse outcomes, such as cognitive impairment and depression. [13] White matter hyperintensity are more than often present with vascular dementia, particularly among small vessel/subcortical subtypes of vascular dementia. [14]

Volume

Smaller volumes (in terms of group averages) of white matter might be associated with larger deficits in attention, declarative memory, executive functions, intelligence, and academic achievement. [15] [16] However, volume change is continuous throughout one's lifetime due to neuroplasticity, and is a contributing factor rather than determinant factor of certain functional deficits due to compensating effects in other brain regions. [16] The integrity of white matter declines due to aging. [17] Nonetheless, regular aerobic exercise appears to either postpone the aging effect or in turn enhance the white matter integrity in the long run. [17] Changes in white matter volume due to inflammation or injury may be a factor in the severity of obstructive sleep apnea. [18] [19]

Imaging

The study of white matter has been advanced with the neuroimaging technique called diffusion tensor imaging where magnetic resonance imaging (MRI) brain scanners are used. As of 2007, more than 700 publications have been published on the subject. [20]

A 2009 paper by Jan Scholz and colleagues [21] used diffusion tensor imaging (DTI) to demonstrate changes in white matter volume as a result of learning a new motor task (e.g. juggling). The study is important as the first paper to correlate motor learning with white matter changes. Previously, many researchers had considered this type of learning to be exclusively mediated by dendrites, which are not present in white matter. The authors suggest that electrical activity in axons may regulate myelination in axons. Or, gross changes in the diameter or packing density of the axon might cause the change. [22] [ self-published source? ] A more recent DTI study by Sampaio-Baptista and colleagues reported changes in white matter with motor learning along with increases in myelination. [23]

See also

Related Research Articles

<span class="mw-page-title-main">Axon</span> Long projection on a neuron that conducts signals to other neurons

An axon, or nerve fiber, is a long, slender projection of a nerve cell, or neuron, in vertebrates, that typically conducts electrical impulses known as action potentials away from the nerve cell body. The function of the axon is to transmit information to different neurons, muscles, and glands. In certain sensory neurons, such as those for touch and warmth, the axons are called afferent nerve fibers and the electrical impulse travels along these from the periphery to the cell body and from the cell body to the spinal cord along another branch of the same axon. Axon dysfunction can be the cause of many inherited and acquired neurological disorders that affect both the peripheral and central neurons. Nerve fibers are classed into three types – group A nerve fibers, group B nerve fibers, and group C nerve fibers. Groups A and B are myelinated, and group C are unmyelinated. These groups include both sensory fibers and motor fibers. Another classification groups only the sensory fibers as Type I, Type II, Type III, and Type IV.

<span class="mw-page-title-main">Central nervous system</span> Brain and spinal cord

The central nervous system (CNS) is the part of the nervous system consisting primarily of the brain and spinal cord. The CNS is so named because the brain integrates the received information and coordinates and influences the activity of all parts of the bodies of bilaterally symmetric and triploblastic animals—that is, all multicellular animals except sponges and diploblasts. It is a structure composed of nervous tissue positioned along the rostral to caudal axis of the body and may have an enlarged section at the rostral end which is a brain. Only arthropods, cephalopods and vertebrates have a true brain, though precursor structures exist in onychophorans, gastropods and lancelets.

<span class="mw-page-title-main">Myelin</span> Fatty substance that surrounds nerve cell axons to insulate them and increase transmission speed

Myelin is a lipid-rich material that surrounds nerve cell axons to insulate them and increase the rate at which electrical impulses pass along the axon. The myelinated axon can be likened to an electrical wire with insulating material (myelin) around it. However, unlike the plastic covering on an electrical wire, myelin does not form a single long sheath over the entire length of the axon. Rather, myelin ensheaths the axon segmentally: in general, each axon is encased in multiple long sheaths with short gaps between, called nodes of Ranvier. At the nodes of Ranvier, which are approximately one thousandth of a mm in length, the axon's membrane is bare of myelin.

<span class="mw-page-title-main">Grey matter</span> Areas of neuronal cell bodies in the brain

Grey matter, or gray matter in American English, is a major component of the central nervous system, consisting of neuronal cell bodies, neuropil, glial cells, synapses, and capillaries. Grey matter is distinguished from white matter in that it contains numerous cell bodies and relatively few myelinated axons, while white matter contains relatively few cell bodies and is composed chiefly of long-range myelinated axons. The colour difference arises mainly from the whiteness of myelin. In living tissue, grey matter actually has a very light grey colour with yellowish or pinkish hues, which come from capillary blood vessels and neuronal cell bodies.

<span class="mw-page-title-main">Cerebellum</span> Structure at the rear of the vertebrate brain, beneath the cerebrum

The cerebellum is a major feature of the hindbrain of all vertebrates. Although usually smaller than the cerebrum, in some animals such as the mormyrid fishes it may be as large as it or even larger. In humans, the cerebellum plays an important role in motor control. It may also be involved in some cognitive functions such as attention and language as well as emotional control such as regulating fear and pleasure responses, but its movement-related functions are the most solidly established. The human cerebellum does not initiate movement, but contributes to coordination, precision, and accurate timing: it receives input from sensory systems of the spinal cord and from other parts of the brain, and integrates these inputs to fine-tune motor activity. Cerebellar damage produces disorders in fine movement, equilibrium, posture, and motor learning in humans.

<span class="mw-page-title-main">Cerebral cortex</span> Outer layer of the cerebrum of the mammalian brain

The cerebral cortex, also known as the cerebral mantle, is the outer layer of neural tissue of the cerebrum of the brain in humans and other mammals. The cerebral cortex mostly consists of the six-layered neocortex, with just 10% consisting of the allocortex. It is separated into two cortices, by the longitudinal fissure that divides the cerebrum into the left and right cerebral hemispheres. The two hemispheres are joined beneath the cortex by the corpus callosum. The cerebral cortex is the largest site of neural integration in the central nervous system. It plays a key role in attention, perception, awareness, thought, memory, language, and consciousness. The cerebral cortex is part of the brain responsible for cognition.

<span class="mw-page-title-main">Schwann cell</span> Glial cell type

Schwann cells or neurolemmocytes are the principal glia of the peripheral nervous system (PNS). Glial cells function to support neurons and in the PNS, also include satellite cells, olfactory ensheathing cells, enteric glia and glia that reside at sensory nerve endings, such as the Pacinian corpuscle. The two types of Schwann cells are myelinating and nonmyelinating. Myelinating Schwann cells wrap around axons of motor and sensory neurons to form the myelin sheath. The Schwann cell promoter is present in the downstream region of the human dystrophin gene that gives shortened transcript that are again synthesized in a tissue-specific manner.

The development of the nervous system, or neural development (neurodevelopment), refers to the processes that generate, shape, and reshape the nervous system of animals, from the earliest stages of embryonic development to adulthood. The field of neural development draws on both neuroscience and developmental biology to describe and provide insight into the cellular and molecular mechanisms by which complex nervous systems develop, from nematodes and fruit flies to mammals.

<span class="mw-page-title-main">Saltatory conduction</span> Propagation of action potentials along the myelinated axons of neurons

In neuroscience, saltatory conduction is the propagation of action potentials along myelinated axons from one node of Ranvier to the next node, increasing the conduction velocity of action potentials. The uninsulated nodes of Ranvier are the only places along the axon where ions are exchanged across the axon membrane, regenerating the action potential between regions of the axon that are insulated by myelin, unlike electrical conduction in a simple circuit.

<span class="mw-page-title-main">Nervous tissue</span> Main component of the nervous system

Nervous tissue, also called neural tissue, is the main tissue component of the nervous system. The nervous system regulates and controls body functions and activity. It consists of two parts: the central nervous system (CNS) comprising the brain and spinal cord, and the peripheral nervous system (PNS) comprising the branching peripheral nerves. It is composed of neurons, also known as nerve cells, which receive and transmit impulses, and neuroglia, also known as glial cells or glia, which assist the propagation of the nerve impulse as well as provide nutrients to the neurons.

<span class="mw-page-title-main">Oligodendrocyte</span> Neural cell type

Oligodendrocytes, also known as oligodendroglia, are a type of neuroglia whose main functions are to provide support and insulation to axons within the central nervous system (CNS) of jawed vertebrates. Their function is similar to that of Schwann cells, which perform the same task in the peripheral nervous system (PNS). Oligodendrocytes accomplish this by forming the myelin sheath around axons. Unlike Schwann cells, a single oligodendrocyte can extend its processes to cover around 50 axons, with each axon being wrapped in approximately 1 μm of myelin sheath. Furthermore, an oligodendrocyte can provide myelin segments for multiple adjacent axons.

<span class="mw-page-title-main">Cerebral hemisphere</span> Left and right cerebral hemispheres of the brain

The vertebrate cerebrum (brain) is formed by two cerebral hemispheres that are separated by a groove, the longitudinal fissure. The brain can thus be described as being divided into left and right cerebral hemispheres. Each of these hemispheres has an outer layer of grey matter, the cerebral cortex, that is supported by an inner layer of white matter. In eutherian (placental) mammals, the hemispheres are linked by the corpus callosum, a very large bundle of nerve fibers. Smaller commissures, including the anterior commissure, the posterior commissure and the fornix, also join the hemispheres and these are also present in other vertebrates. These commissures transfer information between the two hemispheres to coordinate localized functions.

<span class="mw-page-title-main">Human brain</span> Central organ of the human nervous system

The human brain is the central organ of the human nervous system, and with the spinal cord makes up the central nervous system. The brain consists of the cerebrum, the brainstem and the cerebellum. It controls most of the activities of the body, processing, integrating, and coordinating the information it receives from the sense organs, and making decisions as to the instructions sent to the rest of the body. The brain is contained in, and protected by, the skull bones of the head.

<span class="mw-page-title-main">Neural pathway</span> Connection formed between neurons that allows neurotransmission

In neuroanatomy, a neural pathway is the connection formed by axons that project from neurons to make synapses onto neurons in another location, to enable neurotransmission. Neurons are connected by a single axon, or by a bundle of axons known as a nerve tract, or fasciculus. Shorter neural pathways are found within grey matter in the brain, whereas longer projections, made up of myelinated axons, constitute white matter.

<span class="mw-page-title-main">Pyramidal tracts</span> Include both the corticobulbar tract and the corticospinal tract

The pyramidal tracts include both the corticobulbar tract and the corticospinal tract. These are aggregations of efferent nerve fibers from the upper motor neurons that travel from the cerebral cortex and terminate either in the brainstem (corticobulbar) or spinal cord (corticospinal) and are involved in the control of motor functions of the body.

<span class="mw-page-title-main">Node of Ranvier</span> Gaps between myelin sheaths on the axon of a neuron

In neuroscience and anatomy, nodes of Ranvier, also known as myelin-sheath gaps, occur along a myelinated axon where the axolemma is exposed to the extracellular space. Nodes of Ranvier are uninsulated and highly enriched in ion channels, allowing them to participate in the exchange of ions required to regenerate the action potential. Nerve conduction in myelinated axons is referred to as saltatory conduction due to the manner in which the action potential seems to "jump" from one node to the next along the axon. This results in faster conduction of the action potential.

Oligodendrocyte progenitor cells (OPCs), also known as oligodendrocyte precursor cells, NG2-glia, O2A cells, or polydendrocytes, are a subtype of glia in the central nervous system named for their essential role as precursors to oligodendrocytes. They are typically identified in the human by co-expression of PDGFRA and CSPG4.

Myelinogenesis is the formation and development of myelin sheaths in the nervous system, typically initiated in late prenatal neurodevelopment and continuing throughout postnatal development. Myelinogenesis continues throughout the lifespan to support learning and memory via neural circuit plasticity as well as remyelination following injury. Successful myelination of axons increases action potential speed by enabling saltatory conduction, which is essential for timely signal conduction between spatially separate brain regions, as well as provides metabolic support to neurons.

<span class="mw-page-title-main">Anatomy of the cerebellum</span> Structures in the cerebellum, a part of the brain

The anatomy of the cerebellum can be viewed at three levels. At the level of gross anatomy, the cerebellum consists of a tightly folded and crumpled layer of cortex, with white matter underneath, several deep nuclei embedded in the white matter, and a fluid-filled ventricle in the middle. At the intermediate level, the cerebellum and its auxiliary structures can be broken down into several hundred or thousand independently functioning modules or compartments known as microzones. At the microscopic level, each module consists of the same small set of neuronal elements, laid out with a highly stereotyped geometry.

Group A nerve fibers are one of the three classes of nerve fiber as generally classified by Erlanger and Gasser. The other two classes are the group B nerve fibers, and the group C nerve fibers. Group A are heavily myelinated, group B are moderately myelinated, and group C are unmyelinated.

References

  1. ↑ Blumenfeld, Hal (2010). Neuroanatomy through clinical cases (2nd ed.). Sunderland, Mass.: Sinauer Associates. p. 21. ISBN   978-0878936137. Areas of the CNS made up mainly of myelinated axons are called white matter.
  2. ↑ Douglas Fields, R. (2008). "White Matter Matters". Scientific American. 298 (3): 54–61. Bibcode:2008SciAm.298c..54D. doi:10.1038/scientificamerican0308-54.
  3. ↑ Klein, S.B., & Thorne, B.M. Biological Psychology. Worth Publishers: New York. 2007.[ ISBN missing ][ page needed ]
  4. 1 2 Schüz, Almut; Braitenberg, Valentino (2002). "The human cortical white matter: Quantitative aspects of cortico-cortical long-range connectivity". In Schüz, Almut; Braitenberg, Valentino (eds.). Cortical Areas: Unity and Diversity, Conceptual Advances in Brain Research. Taylor and Francis. pp. 377–386. ISBN   978-0-415-27723-5.
  5. ↑ Leenders, K. L.; Perani, D.; Lammertsma, A. A.; Heather, J. D.; Buckingham, P.; Jones, T.; Healy, M. J. R.; Gibbs, J. M.; Wise, R. J. S.; Hatazawa, J.; Herold, S.; Beaney, R. P.; Brooks, D. J.; Spinks, T.; Rhodes, C.; Frackowiak, R. S. J. (1990). "Cerebral Blood Flow, Blood Volume and Oxygen Utilization". Brain. 113: 27–47. doi:10.1093/brain/113.1.27. PMID   2302536.
  6. 1 2 3 Marner, Lisbeth; Nyengaard, Jens R.; Tang, Yong; Pakkenberg, Bente (2003). "Marked loss of myelinated nerve fibers in the human brain with age". The Journal of Comparative Neurology. 462 (2): 144–152. doi:10.1002/cne.10714. PMID   12794739. S2CID   35293796.
  7. ↑ Sowell, Elizabeth R.; Peterson, Bradley S.; Thompson, Paul M.; Welcome, Suzanne E.; Henkenius, Amy L.; Toga, Arthur W. (2003). "Mapping cortical change across the human life span". Nature Neuroscience. 6 (3): 309–315. doi:10.1038/nn1008. PMID   12548289. S2CID   23799692.
  8. ↑ Höftberger, Romana; Lassmann, Hans (2018). "Inflammatory demyelinating diseases of the central nervous system". Handbook of Clinical Neurology. Vol. 145. Elsevier. pp. 263–283. doi:10.1016/b978-0-12-802395-2.00019-5. ISBN   978-0-12-802395-2. ISSN   0072-9752. PMC   7149979 . PMID   28987175.
  9. ↑ Monnig, Mollie A.; Tonigan, J. Scott; Yeo, Ronald A.; Thoma, Robert J.; McCrady, Barbara S. (2013). "White matter volume in alcohol use disorders: A meta-analysis". Addiction Biology. 18 (3): 581–592. doi:10.1111/j.1369-1600.2012.00441.x. PMC   3390447 . PMID   22458455.
  10. ↑ Roseborough, Austyn; Ramirez, Joel; Black, Sandra E.; Edwards, Jodi D. (2017). "Associations between amyloid β and white matter hyperintensities: A systematic review". Alzheimer's & Dementia. 13 (10): 1154–1167. doi:10.1016/j.jalz.2017.01.026. ISSN   1552-5260. PMID   28322203. S2CID   35593591.
  11. ↑ O'Sullivan, M. (2008-01-01). "Leukoaraiosis". Practical Neurology. 8 (1): 26–38. doi:10.1136/jnnp.2007.139428. ISSN   1474-7758. PMID   18230707. S2CID   219190542.
  12. ↑ Hampton WH, Hanik I, Olson IR (2019). "[Substance Abuse and White Matter: Findings, Limitations, and Future of Diffusion Tensor Imaging Research]". Drug and Alcohol Dependence. 197 (4): 288–298. doi:10.1016/j.drugalcdep.2019.02.005. PMC   6440853 . PMID   30875650. Given that our the central nervous system is an intricately balanced, complex network of billions of neurons and supporting cells, some might imagine that extrinsic substances could cause irreversible brain damage. Our review paints a less gloomy picture of the substances reviewed, however. Following prolonged abstinence, abusers of alcohol (Pfefferbaum et al., 2014) or opiates (Wang et al., 2011) have white matter microstructure that is not significantly different from non-users. There was also no evidence that the white matter microstructural changes observed in longitudinal studies of cannabis, nicotine, or cocaine were completely irreparable. It is therefore possible that, at least to some degree, abstinence can reverse effects of substance abuse on white matter. The ability of white matter to "bounce back" very likely depends on the level and duration of abuse, as well as the substance being abused.
  13. ↑ O'Brien, John T. (2014). "Clinical Significance of White Matter Changes". The American Journal of Geriatric Psychiatry. Elsevier BV. 22 (2): 133–137. doi:10.1016/j.jagp.2013.07.006. ISSN   1064-7481. PMID   24041523.
  14. ↑ Hirono, Nobutsugu; Kitagaki, Hajime; Kazui, Hiroaki; Hashimoto, Mamoru; Mori, Etsuro (2000). "Impact of White Matter Changes on Clinical Manifestation of Alzheimer's Disease". Stroke. Ovid Technologies (Wolters Kluwer Health). 31 (9): 2182–2188. doi: 10.1161/01.str.31.9.2182 . ISSN   0039-2499. PMID   10978049.
  15. ↑ Tasman, Allan (2015). Psychiatry (in Welsh). West Sussex, England: Wiley Blackwell. ISBN   978-1-118-84549-3. OCLC   903956524.
  16. 1 2 Fields, R. Douglas (2008-06-05). "White matter in learning, cognition and psychiatric disorders". Trends in Neurosciences. Elsevier BV. 31 (7): 361–370. doi:10.1016/j.tins.2008.04.001. ISSN   0166-2236. PMC   2486416 . PMID   18538868.
  17. 1 2 Handbook of the Psychology of Aging. Elsevier. 2016. doi:10.1016/c2012-0-07221-3. ISBN   978-0-12-411469-2.
  18. ↑ Castronovo, Vincenza; Scifo, Paola; Castellano, Antonella; Aloia, Mark S.; Iadanza, Antonella; Marelli, Sara; Cappa, Stefano F.; Strambi, Luigi Ferini; Falini, Andrea (2014-09-01). "White Matter Integrity in Obstructive Sleep Apnea before and after Treatment". Sleep. 37 (9): 1465–1475. doi:10.5665/sleep.3994. ISSN   0161-8105. PMC   4153061 . PMID   25142557.
  19. ↑ Chen, Hsiu-Ling; Lu, Cheng-Hsien; Lin, Hsin-Ching; Chen, Pei-Chin; Chou, Kun-Hsien; Lin, Wei-Ming; Tsai, Nai-Wen; Su, Yu-Jih; Friedman, Michael; Lin, Ching-Po; Lin, Wei-Che (2015-03-01). "White Matter Damage and Systemic Inflammation in Obstructive Sleep Apnea". Sleep. 38 (3): 361–370. doi:10.5665/sleep.4490. ISSN   0161-8105. PMC   4335530 . PMID   25325459.
  20. ↑ Assaf, Yaniv; Pasternak, Ofer (2007). "Diffusion Tensor Imaging (DTI)-based White Matter Mapping in Brain Research: A Review". Journal of Molecular Neuroscience. 34 (1): 51–61. doi:10.1007/s12031-007-0029-0. PMID   18157658. S2CID   3354176.
  21. ↑ Scholz, Jan; Klein, Miriam C; Behrens, Timothy E J; Johansen-Berg, Heidi (2009). "Training induces changes in white-matter architecture". Nature Neuroscience. 12 (11): 1370–1371. doi:10.1038/nn.2412. PMC   2770457 . PMID   19820707.
  22. ↑ "White Matter Matters". Dolan DNA Learning Center. Archived from the original on 2009-11-12. Retrieved 2009-10-19.[ self-published source ]
  23. ↑ Sampaio-Baptista, C.; Khrapitchev, A. A.; Foxley, S.; Schlagheck, T.; Scholz, J.; Jbabdi, S.; Deluca, G. C.; Miller, K. L.; Taylor, A.; Thomas, N.; Kleim, J.; Sibson, N. R.; Bannerman, D.; Johansen-Berg, H. (2013). "Motor Skill Learning Induces Changes in White Matter Microstructure and Myelination". Journal of Neuroscience. 33 (50): 19499–19503. doi:10.1523/JNEUROSCI.3048-13.2013. PMC   3858622 . PMID   24336716.

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