MYELINATION - keywords
myelination sequence: historical data
Flechsig 1921: fetus 7 months old; postcentral gyrus
myelinates first at cortical level, limited myelination in PLIC
Altman and Bayer: 6 weeks after term birth
Yakovlev and Lecours 1967
Buyanova and Arsalidou 2021
myeloarchitectonic cycles
spinal cord myelination starts at 12-14 weeks PMA; last areas to myelinate are intracortical fibers in adults; cycles of
myelination are long for supralimbic white matter
corpus callosum myelinates from front to back; genu myelinated by 6 months after term; myelination of corpus callosum and
fornix complete by age 20 years
cerebral white matter: posterior to anterior gradient
- first: median zone: median thalamus, hypothalamus, hippocampus, septal area
- second: paramedian zone: paramedian thalamus, subthalamus, internal capsule, pallidum, striatum, amygdala, claustrum
- third: supralimbic zone: bulk of white matter and opercula
myelination sequence: Flechsig 1920
dark before gray before white
-
central sites (around central sulcus) before poles of brain lobes
fronto-parieto-occipital areas before temporal and frontal sites
central sensory before motor systems
Flechsig P (1920) Anatomie des menschlichen Gehirns und R ckenmarks auf myelogenetischer
Grundlage. Thieme, Leipzig
Flechsig distinguished 45 myelogenetic areas, numbered according as a sequence of
myelination during fetal and early postnatal life. Classified in three categories, primordial
areas (1–16), which show signs of myelination before birth, intermediate areas (17–36),
which become myelinated between birth and the second postnatal month and terminal areas
(37–45), which myelinate after the second postnatal month.
ü
Prenatally myelinating fibres belong to the large sensory and motor projections. Postnatally
maturing fibres between associative cortex areas; hence the intermediate and terminal areas
were designated as association areas. Clusters of late-maturing areas form three association
centres: a large posterior association centre (occupying much of the parietal, occipital and
temporal lobes); an anterior association centre in front of the motor projection areas; a
small insular association centre.
term, one month old
myelination sequence: review 2021
Buyanova and Arsalidou 2021. Review of myelination
based on several MRI techniques and the histological
postmortem findings.
In the brainstem medial longitudinal fascicle and lateral
lemniscus myelinate early and rapidly before birth; the
fibers for general proprioceptive (muscle sense) and
exteroceptive (tactile and pain) somatic experience (e.g.
medial lemniscus, outer division of the inferior
cerebellar peduncle and bracchium conjunctivum)
myelinate later and at a slower rate. The middle
cerebellar peduncles myelinate only after birth in a
protracted cycle. The fibers in the reticular formation
(and basal forebrain) continue to gain in density and
tinctorial intensity of staining to at least the third
decade.
The geniculocalcarine (optic), postcentral (somesthetic)
and precentral (propriokinesthetic) projections from the
nuclei of the thalamus to their respective cortices
myelinate rapidly during the first year after birth and
precede myelination of the corticofugal systems. The
specific thalamocortico-pyramidal arcs have a relatively
short cycle of myelination completed during the first
postnatal year. The non-specific thalamocorticopontine
arcs, from the dorsolateral and posterior thalamus to the
areas surrounding the primary cortical sensory-motor
analysers and from there to the pons and cerebellum,
exhibits a long cycle protracted into early childhood.
In contrast the fibers in the paramedian zone of the
forebrain (e.g. cingulum, striatum, pallidum,
subthalamus and paramedian thalamus), exhibit a short
cycle of myelination which appears to be completed at
about the age of puberty. The short cycle of myelination
of this zone appears to correlate with the rapid
maturation of the reflex and behavioural patterns in the
sphere of 'innate' or 'instinctive' movements
conventionally assigned to basal ganglia and the
'extrapyramidal' system.
The commissural and association systems of the
outermost or supralimbic zones of the hemispheres
exhibit the longest cycles of myelination.
The intracortical neuropil of the frontal, parietal and
temporal association areas continue to show increase of
the reticulum of fine myelinated fibres through years of
maturity to senium.
Myelination of the cortical end of the acoustic radiation
in the temporal lobe is protracted beyond the first
postnatal year, in sharp contrast to the optic radiation
which myelinates rapidly soon after birth in one short
spurt from retina to its end about the calcarine fissure.
myelination sequence: histological data
- first MBP in human thalamus ~18w PMA
- no mature myelin in CNS before ~ 22w PMA
- no myelin in forebrain before ~ 25w PMA (habenulo-
- non-specific thalamic radiations myelinate entirely after
- myelin in reticular formation starts after term and is
- peridentate myelin from around 37w PMA
interpeduncular tract first)
very protracted
term
- internal capsule at mesencephalon: central before
medial and lateral sides
Pathway
begin*
completed*
Spinal motor roots
16 weeks
42 weeks
Spinal sensory roots
20 weeks
5 months
Cranial motor nerves III,IV,V,VI
20 weeks
28 weeks
Ventral commissure, spinal cord
24 weeks
4 months
Dorsal columns, spinal cord
28 weeks
36 weeks
Medial longitudinal fasciculus
24 weeks
28 weeks
Habenulopeduncular tract
28 weeks
34 weeks
Acoustic nerve
24 weeks
36 weeks
Trapezoid body & lateral lemniscus (octavus system)
24 weeks
36 weeks
Acoustic radiations (thalamocortical)
40 weeks
3 years
Inferior cerebellar peduncle (inner part)(outer: later, protracted)
26 weeks
36 weeks
Subthalamus (biphasic course, starts early, potracted after term)
26 weeks
> 1 year
Middle cerebellar peduncle
42 weeks
4 years
Superior cerebellar peduncle
arriving at VL thalamus ~36w PMA
28 weeks
8 months
Medial lemniscus
arriving at VL thalamus ~32w PMA
24 weeks
12 months
36 weeks
6 months
37 weeks
6 months
Ansa lenticularis
28 weeks
8 months
Pallidum (internum myelinates earlier than externum)
25 weeks
1-2 years
Fornix (limbic system myelinates after term)(cingulum before fornix)
2 months
2 years
Caudate and putamen
35 weeks
4 years
Mammillothalamic tract
38 weeks
6 years
Thalamocortical specific radiations (acoustic:somesthetic before visual)
38 weeks
7 years
Corticospinal tract, rolandic cortex (pyramidal tract extends up from pons)
35 weeks
2 years
Corpus callosum (from splenium to genu)
2 months
14 years
Internal capsule (PLIC before ALIC)
25 weeks
first year
Cortico-pontine tracts
after 40w
> 1 year
Subcortical fibers (first pericentral, calcarine and Heschl gyri)
35 weeks
years
Intracortical association fibers (frontotemporal & frontoparietal))
3 months
32 years
Optic nerve and tract, superior colliculi
Optic radiations
late onset of optic myelination, but
short postnatal cycle
* myelination as observed with LM methods (e.g. luxol fast blue or Loyez); adding MBP (myelin basic protein) for
staining advances detection of myelin by a few weeks (correction of Yakovlev and Lecours data)
Hasegawa et al. 1992, Yakovlev and Lecours 1967
myelination sequence: MRI data
radial diffusivity and fractional anisotropy correlate with amount and quality of myelin
myelin: high lipid content, only 70 % H2O, tight multi-lamellar structure
T1 relaxation (increased signal, more white) is more sensitive to myelin
T2 relaxation (decreased signal, more dark) correlates best with compact myelin quantity
GA w
myelinating structure
16
spinal motor roots
20
spinal sensory roots
multimodal MRI necessary
McArdle MR
motor nerves for eye muscles (III, IV, VI)
22
medial longitudinal fascicle (pons before medulla)
lateral lemniscus
stato-acoustic tectum and tegmentum (trapezoid body)
inferior collicle
cuneate fascicle
23
inferior cereballar peduncle (restiform body) inner part
24
medial lemniscus
26
spinocerebellar and spinothalamic tracts
subthalamus
nerves VII and VIII
28
ventrolateral thalamus (related to lateral lemniscus)
M2
pallidum (efferent fibers)
gracile fascicle
nerves V, IX, X, XII
superior cerebellar peduncle (fibers to thalamus at 36 w)
30
optic chiasm and tract
32
rubrospinal and tectospinal tract
34
posterior commissure
M1
M3 pt
posterior limb internal capsule
M4 comp
36
optic nerve and radiation
M5
38
pre- and postcentral gyri (post slightly earlier)
acoustic radiation
40
middle cerebellar peduncle
> 44
corona radiata
M6
anterior limb internal capsule
M7
myelin at PMA, LFB
onset
mature myelin
comment
PLIC
38 w
44 w
optic radiation
43
52
optic radiation proximal before distal before calcarine cortex
acoustic radiation
41
67
proximal auditory radiation before Heschl gyri
corpus callosum
44
60-65
splenium weeks before genu, posterior to anterior gradient
precentral gyrus subcortical white matter
41
70
posterior frontal subcortical white matter
47
80
occipital pole
47
87
posterior parietal subcortical white matter
53
99
Brody et al. 1987, Kinney et al. 1988
the oligodendrocyte lineage
block by ischaemia,
inflammation,
excitotoxic cascade ——>
mature OL, O1 + and MBP +
immature OL, O1 + and MBP +
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I weeks before mature
I stage
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I predominate 20-30wI PMA
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18w PMA
30w PMA
40w PMA
——>
premyelinating late OPC (pre-OL), PDGFR-, O4 + and O1 -
near term and after
PDGFR@ +
early OPC
Olig 1 +
I
I
I
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9w PMA
OL precursors derive from neural stem cells in the SVZ that become
oligodendrocyte progenitors (influenced by Olig 1, Olig 2, Nkx2.2, Sox 10)
MYELINATION
mainly after term
PREMYELINATION
human 20-30+w PMA
between late
oligodendrocyte
precursor and OL stages
-
premyelination starts
with O1 positivity in
subplate
-
-
slow myelin turn-over in
humans
activity dependent
(re)myelination
homeostatic balance by
stable pool of mature OL
(O1+ and MBP+)
stimulation (PDGF@ from astrocytes)
disinhibtion
OL precursors migrate
along vessels
OL precursors promote angiogenesis because they need vessels
for migration and for myelin deposition
CNP, MAG, GALC,
sulfatide O4+, O1
and MBP-
mature myelin
contains MAG, MOG,
MBP, PLP
sources of oligodendrocyte precursors (OPC)
MAG, MOG,
MBP, PLP
OL precursors (OPC) secrete semaphorin 6a/6b that binds to plexin receptors on interneurons,
which drives these interneurons into a migration path away from blood vessels
OL-vascular interaction: migration
along vessels and jumping from one
vessel to another
-
-
neural stem cells (NSCs) differentiate into (OPCs) under
the influence of OL-specific transcription factors Olig1/2,
Nkx2.2, and Sox10
OPCs migrate toward an appropriate site via blood vessels,
at the same time promoting angiogenesis in a HIF1adependent manner, in areas requiring more oxygen
slow turn-over in humans
activity dependent
-
-
at their final destination, OPCs proliferate to expand the
pool of OPCs, under the regulation of transcription factors
such as Id2, Id4, Tcf4, and Hes5
when proliferation is inhibited, OLs differentiate into
premyelinating OLs (pre-OLs), and finally into mature OLs
that enwrap neuronal axons with myelin sheaths, under the
influence of, for example, Myrf
ventral wave
MGE and anterior entopeduncular area (SHH dep.)
—-> OL for hypothalamus, optic nerve …
mouse E12.5
medial wave
LGE and CGE
——> OL for entire forebrain
dorsal wave
cortical SVZ (SHH indep.)
OL for cortex
throughout preterm period
human OPC cells in dorsal areas from 19w PMA
human 10w PMA PDGFR@+ cells present in forebrain
this OL population disappears after birth
mouse P0
human liflelong
Jakovcevski et al. 2009
Lepiemme et al. 2002
van Tilborg et al. 2018
mouse E15.5
OPC come from the subventricular zone (Ortega et al. 2018)
- subpallial germinal matrix GM is considered the ‘factory’
- the subplate has spontaneous electrical activity, the SVZ
-
- RGCells transform into astrocytes (GFAP and vimentin
for production of most brain cells
neurons and most macroglia originate in the ventricular
zone (VZ) but later on also in a secondary germinal area,
the subventricular zone (SVZ)
- SVZ appears at 8 weeks of gestation and persists until
does not
positive cells) from early fetal life on until term
- neuroblasts derived from the subpallial eminences
migrate to reach the cortex along a scaffold of radial glial
fibers; precursor cells first migrate laterally (radially) and
then change direction in the subventricular zone,
engaging in tangential migration
birth and in a rudimentary form later (the subependymal
zone), in subpallium but also in cortical areas
- pyramidal (projection) neurons for the deep cortical
plate are generated in the VZ but glutamatergic neurons
for the upper cortical plate, some interneurons, some
oligodendrocytes (mainly after birth) and astrocytes are
generated in the SVZ
- as GM is a major source for oligodendrocytes, their
number can be reduced and differentiation can be
impaired due to GMH; this may therefore contribute to
white matter injury (Ulfig 2002).
- the SVZ is subdivided into the smaller inner (iSVZ) and
expanded outer SVZ (oSVZ)
lateral section
medial section
cortical
matrix
ganglionic
eminence
matrix
migratory pathways of oligodendrocyte progenitors (OPCs) in the
human forebrain at mid-gestation
- Vimentin+ radial glial cells co-label with the oligodendrocyte
marker OLIG2, suggesting oligodendroglia is gnerated in the
cortical VZ at mid-gestation
- from the cortical proliferative zone multipotent cells migrate
toward white matter (IZ) or first to the SVZ and then to the IZ
-
late, non-migratory O4+ OPCs are dispersed throughout the
VZ/SVZ and accumulate in the subplate
PDGFRα+ cells migrate in the fetal human cortex and are also
observed in the amygdala
A, amygdala; BG, basal ganglia; CC, corpus callosum; Cx,
cortex; CP, cortical plate
NG2 glia as progenitors for oligodendrocytes
Progeny of NG2-glia at different
developmental stages and in disease while
during development NG2-glia generate more
NG2-glia, oligodendrocytes and astrocytes, in
the adult CNS their progeny remains purely
oligodendrogenic. However, under some
pathological conditions of the adult brain,
NG2-glia can also generate astrocytes and
myelinating Schwann cells. Evidence in favor
of generation of neurons from NG2-glia
still remains highly contentious. (Dimou and
Gallo 2015)
oligodendrocyte precursors for life
in adults precursors for OL mainly come from dorsoventral SVZ
VZ
SVZ
pre neuroblast C
ependyma
A
B
B
vessel
apical cilium
pre OPC C
C
matrix fractones
- cells with astroglial properties (type B cells) function as stem cells
- type B cells slowly divide and give rise to rapidly dividing intermediate progenitor cells (IPCs) or
transient amplifying progenitors (type C cells)
- type C divide further to generate neuroblasts (type A cells) or OPC
Maki et al. 2013
migration and differentiation of oligodendrocytes
adaptive myelination throughout life
-
some OLs are specific for
glutamatergic neurons, others for
GABAergic or mixed neurons
sensory experience: auditory, visual, sensory
social experience in critical periods (deprivation)(neuregulin, endothelin)
motor learning
memory and cognition (BDNF on TrkB receptors on OL)
at least 7 OL phenotypes
trophic factors
—————————
BDNF
neurotrophin 3
PDGF
CNTF
activity regulated
myelination
final postioning and differentiation
CXCL1
tenascin-C
neurotransmitters and channels
regulation of intracellular Ca++ via
glutamate on AMPA/integrin receptors
and via voltage gated channels
astrocytes produce semaphorins that repel
OL from vessels and place astrocyte endfeet
at the space free of OL; IL6 from astrocytes
induces CXCL1 expression in OL
neuromodulation via adenosine
growth factors
PDGF (ubiquitous
stimulus of motility)
HGF, FGF8
OL motility
extracellular matrix
components
laminin
fibronection
vitronectin
molecular cues
netrin-1 chemorepellent
TGFß repellent
different functions for different
semaphorins (on neuropilins and
plexins as receptors)
inhibition by tenascin
and collagen
reelin repellent
CNTF attractant
cell polarity
proteoglycan NG2
engagement to vessel scaffold
angiopoietin-1 expressed by progenitor cell and TGFß from endothelium in
return to commit OL precursor (coupling by HIF 1/2a from OL precursors)
crucial Wnt signalling to maintain migration
VEGF-A
Xia and Fancy 2021, Wolf et al. 2021, Su et al. 2022
cellular interaction for myelination
microglia
neuron
astrocyte
iron
folate
vitamin B112
phagocytosis of
excess myelin
fatty acids
<—
IGF1 leads developmental
myelination
connexins
thyroxine (MCT8 transporter)