Gyrification: Difference between revisions

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{{Image|ComparitiveBrainSize.jpg|right|350px|Comparative anatomy of brains from various vertebrate species, highlighting the gradual differences in gyrification.}}
<!--{{Image|ComparitiveBrainSize.jpg|right|350px|Comparative anatomy of adult brains from various vertebrate species, highlighting the differences in [[brain size|size]] and gyrification.}}-->
<imagemap>
Image:ComparitiveBrainSize.jpg|thumb|right|350px|Comparative anatomy of adult brains from various vertebrate species, highlighting the differences in brain size and gyrification. <small>Image credit: University of Wisconsin and Michigan State Comparative Mammalian Brain Collections and National Museum of Health and Medicine (see http://www.brainmuseum.org/). </small>
default [[Brain evolution]]


In the brain sciences, '''gyrification''' (or ''cortical folding'', ''cortical convolution'', ''fissuration'' or ''fissurization'') refers to both the process and the extent of folding of the [[cerebral cortex]] in [[mammal]]s as a consequence of brain growth during [[embryonic development|embryonic]] and early [[postnatal development]].
rect 16 230 205 480 [[Dolphin|Dolphin]]
poly 202 378 227 363 230 361 244 374 203 407 204 377 [[Dolphin|Dolphin]]
rect 288 408 381 478 [[Macaque|Macaque]]
rect 231 390 354 406 [[Macaque|Macaque]]
poly 215 227 330 229 404 296 404 393 356 392 346 385 268 380 221 291 [[Gorilla|Gorilla]]
rect 0 37 245 225 [[Human|Human]]
poly 205 4 208 29 255 37 255 222 341 227 402 260 431 237 537 175 535 44 348 2 [[Elephant|Elephant]]
rect 15 3 198 30 [[Human|Human]]
rect 205 432 282 484 [[Allometry|Allometry]]
rect 381 429 501 473 [[Mouse|Mouse]]
rect 405 344 531 429 [[Cat|Cat]]
poly 409 261 459 225 536 224 543 341 505 341 494 342 492 345 415 342 [[Dog|Dog]]


In the process, [[gyrus|gyri]] (ridges) and [[sulcus|sulci]] (fissures) form on the external surface of the brain (i.e. at the boundary between the [[cerebrospinal fluid]] and the [[gray matter]]). A low extent of gyrification in a given brain is commonly referred to as [[lissencephaly]] (which may range from [[agyria]], the total absence of folding, to [[pachygyria]]), while [[gyrencephaly]] describes a high degree of folding<ref name=Francis2006>{{citation
desc none
</imagemap>
{{TOC|right}}
 
 
In the brain sciences, '''gyrification''' refers to both the process and the extent of folding of the [[cerebral cortex]] in [[mammal]]s as a consequence of brain growth during [[embryonic development|embryonic]] and early [[postnatal development]]. Alternative terms for gyrification include ''gyration''/''sulcation'', ''cortical folding'', ''cortical convolution'', ''fissuration'' and ''fissurization''.
 
In the process (also known as ''gyrogenesis''), [[gyrus|gyri]] (ridges) and [[sulcus|sulci]] (grooves) form on the external surface of the brain (i.e. at the boundary between the [[cerebrospinal fluid]] and the [[grey matter]])<ref name=Armstrong1995>{{cite journal
| author = Armstrong, E.
| coauthors = Schleicher, A.; Omran, H.; Curtis, M.; Zilles, K.
| year = 1995
| title = The Ontogeny of Human Gyrification
| journal = Cerebral Cortex
| volume = 5
| issue = 1
| pages = 56-63
| url = http://cercor.oxfordjournals.org/cgi/content/abstract/5/1/56
}}</ref>. A low extent of gyrification in a given brain is commonly referred to as [[lissencephaly]] (which may range from [[agyria]], the total absence of folding, to [[pachygyria]]<ref name=Dhellemmes1988>{{citation
| last1 = Dhellemmes | first1 = C.
| last2 = Girard | first2 = S.
| last3 = Dulac | first3 = O.
| last4 = Robain | first4 = O.
| last5 = Choiset | first5 = A.
| last6 = Tapia | first6 = S.
| year = 1988
| title = Agyria—pachygyria and Miller-Dieker syndrome: clinical, genetic and chromosome studies
| journal = Human Genetics
| volume = 79
| issue = 2
| pages = 163–167
| doi = 10.1007/BF00280557
| url = http://www.springerlink.com/index/QQR0H684886267X9.pdf
}}</ref>), while [[gyrencephaly]] describes a high degree of folding<ref name=Francis2006>{{citation
  | last1 = Francis | first1 = F.
  | last1 = Francis | first1 = F.
  | last2 = Meyer | first2 = G.
  | last2 = Meyer | first2 = G.
Line 23: Line 69:
}}</ref>.
}}</ref>.


The term ''gyrification'' is also sometimes used instead of the more common term ''[[foliation]]'' to describe the folding patterns of the [[cerebellum]], which is highly convoluted in other [[taxa]], too, e.g. in [[bird]]s<ref name=Iwaniuk2006>{{citation
The term ''gyrification'' is also sometimes used instead of the more common term ''[[foliation]]''<ref name=Demaerel2002>{{citation
| last = Demaerel | first =  P.
| year = 2002
| title = Abnormalities of cerebellar foliation and fissuration: classification, neurogenetics and clinicoradiological correlations
| journal = Neuroradiology
| volume = 44
| issue = 8
| pages = 639–646
| doi = 10.1007/s00234-002-0783-1
| url = http://www.springerlink.com/index/KBKU4WR1MXNU7CU9.pdf
}}</ref> to describe the folding patterns of the vertebrate [[cerebellum]]<ref name=Mares1970>{{citation
| last1 = Mares | first1 = V.
| last2 = Lodin | first2 = Z.
| year = 1970
| title = The cellular kinetics of the developing mouse cerebellum. II. The function of the external granular layer in the process of gyrification
| journal = Brain Res
| volume = 23
| issue = 3
| pages = 343–352
| doi = 10.1016/0006-8993(70)90061-2
| url = http://www.ncbi.nlm.nih.gov/pubmed/5478302
}}</ref> that is highly convoluted in other [[taxa]], e.g. in [[bird]]s<ref name=Iwaniuk2006>{{citation
  | author = Iwaniuk, A.N.; Hurd, P.L.; Wylie, D.R.
  | author = Iwaniuk, A.N.; Hurd, P.L.; Wylie, D.R.
  | year = 2006
  | year = 2006
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  | doi = 10.1159/000093530
  | doi = 10.1159/000093530
  | url = http://www.ncbi.nlm.nih.gov/pubmed/16717442
  | url = http://www.ncbi.nlm.nih.gov/pubmed/16717442
}}</ref>, and of [[mushroom body]] [[calyx|calyces]] in [[insect]] brains<ref name=Farris2005>{{citation
| last1 = Farris | first1 = S.M.
| last2 = Roberts | first2 = N.S.
| year = 2005
| title = Coevolution of generalist feeding ecologies and gyrencephalic mushroom bodies in insects
| journal = Proceedings of the National Academy of Sciences
| volume = 102
| issue = 48
| pages = 17394–17399
| doi = 10.1073/pnas.0508430102
| url = http://www.pnas.org/cgi/reprint/102/48/17394.pdf
}}</ref>.
}}</ref>.


==Phylogeny==
== Phylogeny ==
''See also [[brain evolution]]''.
''See also [[brain evolution]]''.


Line 50: Line 128:
  | coauthors = Mwamengele, G.L.; Dantzer, V.; Williams, S.
  | coauthors = Mwamengele, G.L.; Dantzer, V.; Williams, S.
  | year = 1996
  | year = 1996
  | title = The gyrification of mammalian cerebral cortex: quantitative evidence of anisomorphic surface expansion during phylogenetic and ontogenetic development.
  | title = The gyrification of mammalian cerebral cortex: quantitative evidence of anisomorphic surface expansion during phylogenetic and ontogenetic development
  | journal = Journal of Anatomy
  | journal = Journal of Anatomy
  | volume = 188
  | volume = 188
  | issue = Pt 1
  | issue = Pt 1
  | pages = 53
  | pages = 53-58
  | url = http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1167632  
  | url = http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1167632  
}}</ref> in a gradually different manner: It increases slowly with overall brain size, following a [[power law]]
}}</ref>, with [[cetacean]]s dominating the upper end of the spectrum<ref name=Marino2007>{{citation
| last1 = Marino | first1 = L.
| last2 = Connor | first2 = R.C.
| last3 = Ewan Fordyce | first3 = R.
| last4 = Herman | first4 = L.M.
| last5 = Hof | first5 = P.R.
| last6 = Lefebvre | first6 = L.
| last7 = Lusseau | first7 = D.
| last8 = McCowan | first8 = B.
| last9 = Nimchinsky | first9 = E.A.
| last10 = Pack | first10 = A.A.
| last11 = Others
| year = 2007
| title = Cetaceans Have Complex Brains for Complex Cognition
| journal = PLoS Biology
| volume = 5
| issue = 5
| pages = e139
| doi = 10.1371/journal.pbio.0050139
| url = http://biology.plosjournals.org/perlserv/?request=get-document
}}</ref>. It generally increases slowly with overall [[brain size]], following a [[power law]]
<ref name=Hofman1989>{{cite journal
<ref name=Hofman1989>{{cite journal
  | author = Hofman, M.A.
  | author = Hofman, M.A.
Line 67: Line 165:
  | url = http://www.ncbi.nlm.nih.gov/pubmed/2645619  
  | url = http://www.ncbi.nlm.nih.gov/pubmed/2645619  
  | doi = 10.1016/0301-0082(89)90013-0   
  | doi = 10.1016/0301-0082(89)90013-0   
}}</ref>, and a range of theoretical models exist as to the degree to which it hints at the evolution of cognitive abilities in a given range of species<ref name=Stangier1937>{{citation
}}</ref>: Small-brained placental species are indeed lissencephalic<ref name=Ferrer1986gss_i>{{:CZ:Ref:PMC1166506}}</ref><ref name=Pillay2007>{{citation
| last1 = Pillay | first1 = P.
| last2 = Manger | first2 = P.R.
| year = 2007
| title = Order-specific quantitative patterns of cortical gyrification
| journal = European Journal of Neuroscience
| volume = 25
| issue = 9
| pages = 2705–2712
| doi = 10.1111/j.1460-9568.2007.05524.x
| url = http://dx.doi.org/10.1111/j.1460-9568.2007.05524.x
}}</ref>, and amongst the two living species of [[monotreme]]s, the small-brained [[platypus]] is lissencephalic, while the larger brains of [[echidna]] are gyrencephalic<ref name=Hassiotis2003>{{citation
| last1 = Hassiotis | first1 = M.
| last2 = Paxinos | first2 = G.
| last3 = Ashwell | first3 = K.W.S.
| year = 2003
| title = The anatomy of the cerebral cortex of the echidna (Tachyglossus aculeatus)
| journal = Comparative Biochemistry and Physiology, Part A
| volume = 136
| issue = 4
| pages = 827–850
| doi = 10.1016/S1095-6433(03)00166-1
| url = http://linkinghub.elsevier.com/retrieve/pii/S1095643303001661
}}</ref>. Conversely, large-brained mammals are usually highly gyrencephalic<ref name=Ferrer1986gss_ii>{{citation
| last1 = Ferrer | first1 = I.
| last2 = Fabregues | first2 = I.
| last3 = Condom | first3 = E.
| year = 1986
| title = A Golgi study of the sixth layer of the cerebral cortex. II. The gyrencephalic brain of Carnivora, Artiodactyla and Primates
| journal = J Anat
| volume = 146
| pages = 87–104
| url = http://www.ncbi.nlm.nih.gov/pubmed/3693064
}}</ref><ref name=Hof2005>{{citation
| last1 = Hof | first1 = P.R.
| last2 = Chanis | first2 = R.
| last3 = Marino | first3 = L.
| year = 2005
| title = Cortical Complexity in Cetacean Brains
| journal = Anatomical Record Part a Discoveries in Molecular Cellular and Evolutionary Biology
| volume = 287
| issue = 1
| pages = 1142
| doi = 10.1002/ar.a.20258
| url = http://dx.doi.org/10.1002/ar.a.20258
}}</ref><ref name=Hakeem2005>{{citation
| last1 = Hakeem | first1 = A.Y.
| last2 = Hof | first2 = P.R.
| last3 = Sherwood | first3 = C.C.
| last4 = Switzer | first4 = R.C. 3rd
| last5 = Rasmussen | first5 = L.E.
| last6 = Allman | first6 = J.M.
| year = 2005
| title = Brain of the African elephant (Loxodonta africana): neuroanatomy from magnetic resonance images
| journal = Anat Rec A: Discov Mol Cell Evol Biol
| volume = 287
| issue = 1
| pages = 1117–1127
| url = http://doi.wiley.com/10.1002/ar.a.20255
}}</ref>, with [[sirenian]]s being a notable exception<ref name=Reep1990>{{citation
| last1 = Reep | first1 = R.L.
| last2 = O'Shea | first2 = T.J.
| year = 1990
| title = Regional brain morphometry and lissencephaly in the Sirenia
| journal = Brain Behav Evol
| volume = 35
| issue = 4
| pages = 185–194
| doi = 10.1159/000115866
| url = http://content.karger.com/ProdukteDB/produkte.asp?Aktion=ShowPDF&ArtikelNr=115866&Ausgabe=233939&ProduktNr=223831&filename=115866.pdf
}}</ref>. A range of theoretical models exist as to the degree to which gyrification hints at the evolution of cognitive abilities in a given range of species<ref name=Stangier1937>{{citation
  | last = Stangier | first =  H.
  | last = Stangier | first =  H.
  | year = 1937
  | year = 1937
Line 100: Line 268:
}}</ref>.
}}</ref>.


==Ontogeny==
== Ontogeny ==
''See also [[brain development]]''.
''See also [[brain development]]''.
{{Image|Baboon fetus MRI sagittal Kochunov et al. 2010.png|left|250px|[[Sagittal]] slice from an [[MRI]] scan of a [[baboon]] [[fetus]] at week 24 of [[uterus|in utero]] [[ontogenesis|development]], clearly showing the folded cortical surface.}}


The folding process usually starts during fetal development -- in [[human]]s around mid-gestation<ref name=Chi1977>{{citation
The folding process usually starts during fetal development—in [[human]]s around mid-gestation<ref name=Chi1977>{{citation
  | last1 = Chi | first1 = J.G.
  | last1 = Chi | first1 = J.G.
  | last2 = Dooling | first2 = E.C.
  | last2 = Dooling | first2 = E.C.
Line 115: Line 284:
  | doi = 10.1002/ana.410010109
  | doi = 10.1002/ana.410010109
  | url = http://doi.wiley.com/10.1002/ana.410010109
  | url = http://doi.wiley.com/10.1002/ana.410010109
}}</ref><ref name=Armstrong1995>{{cite journal
}}</ref><ref name=Armstrong1995/><ref name=Garel2003>{{citation
  | author = Armstrong, E.
| last1 = Garel | first1 = C.
  | coauthors = Schleicher, A.; Omran, H.; Curtis, M.; Zilles, K.
  | last2 = Chantrel | first2 = E.
  | year = 1995
  | last3 = Elmaleh | first3 = M.
  | title = The Ontogeny of Human Gyrification
| last4 = Brisse | first4 = H.
  | journal = Cerebral Cortex
| last5 = Sebag | first5 = G.
  | volume = 5
| year = 2003
  | issue = 1
| title = Fetal MRI: normal gestational landmarks for cerebral biometry, gyration and myelination
  | pages = 56-63
| journal = Child's Nervous System
  | url = http://cercor.oxfordjournals.org/cgi/content/abstract/5/1/56
| volume = 19
| issue = 7
| pages = 422–425
| doi = 10.1007/s00381-003-0767-4
| url = http://www.springerlink.com/index/U6Q23BDX1B67X21T.pdf
}}</ref><ref name=Toi2004>{{citation
| last1 = Toi | first1 = A.
| last2 = Lister | first2 = W.S.
| last3 = Fong | first3 = K.W.
  | year = 2004
  | title = How early are fetal cerebral sulci visible at prenatal ultrasound and what is the normal pattern of early fetal sulcal development?
  | journal = Ultrasound in Obstetrics and Gynecology
  | volume = 24
  | issue = 7
  | pages = 706–715
| doi = 10.1002/uog.1802
  | url = http://www3.interscience.wiley.com/journal/109841057/abstract
}}</ref><ref name=Regis2005>{{citation
}}</ref><ref name=Regis2005>{{citation
  | last1 = Regis | first1 = J.
  | last1 = Regis | first1 = J.
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  | last8 = Samson | first8 = Y.
  | last8 = Samson | first8 = Y.
  | year = 2005
  | year = 2005
  | title = " Sulcal root" generic model: a hypothesis to overcome the variability of the human cortex folding …
  | title = "Sulcal root" generic model: a hypothesis to overcome the variability of the human cortex folding patterns
  | journal = Neurol Med Chir (Tokyo)
  | journal = Neurol Med Chir (Tokyo)
  | volume = 45
  | volume = 45
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  | doi = 10.2176/nmc.45.1
  | doi = 10.2176/nmc.45.1
  | url = http://www.jstage.jst.go.jp/article/nmc/45/1/45_1/_article
  | url = http://www.jstage.jst.go.jp/article/nmc/45/1/45_1/_article
}}</ref> -- or shortly after birth, as in [[ferret]]s<ref name=Smart1986>{{citation
}}</ref><ref name=Ghai2006>{{citation
| last1 = Ghai | first1 = Sandeep
| last2 = Fong | first2 = Katherine W.
| last3 = Toi | first3 = Ants
| last4 = Chitayat | first4 = David
| last5 = Pantazi | first5 = Sophia
| last6 = Blaser | first6 = Susan
| year = 2006
| title = Prenatal US and MR Imaging Findings of Lissencephaly: Review of Fetal Cerebral Sulcal Development
| journal = RadioGraphics
| volume = 26
| issue = 2
| pages = 389–405
| doi = 10.1148/rg.262055059
| url = http://radiographics.rsnajnls.org/cgi/reprint/26/2/389.pdf
| pmid = 16549605
}}</ref> —or shortly after birth, as in [[ferret]]s<ref name=Smart1986>{{citation
  | last1 = Smart | first1 = I.H.
  | last1 = Smart | first1 = I.H.
  | last2 = McSherry | first2 = G.M.
  | last2 = McSherry | first2 = G.M.
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  | doi = 10.1111/j.1469-7580.2006.00674.x
  | doi = 10.1111/j.1469-7580.2006.00674.x
  | url = http://www.ncbi.nlm.nih.gov/pubmed/17229284
  | url = http://www.ncbi.nlm.nih.gov/pubmed/17229284
}}</ref> and proceeds synchronously in both hemispheres.
}}</ref>. It proceeds synchronously in both hemispheres by an expansion of gyral tissue, while the [[sulcal root]]s remain in a relatively stable position throughout gyrogenesis<ref name=Smart1986/><ref name=Armstrong1995/><ref name=Regis2005/>. In the adult human brain, variations due to [[gender]]<ref name=Robin2003>{{citation
 
| last1 = Robin Highley | first1 = J.
| last2 = Delisi | first2 = L.E.
| last3 = Roberts | first3 = N.
| last4 = Webb | first4 = J.A.
| last5 = Relja | first5 = M.
| last6 = Razi | first6 = K.
| last7 = Crow | first7 = T.J.
| year = 2003
| title = Sex-dependent effects of schizophrenia: an MRI study of gyral folding, and cortical and white matter
| journal = Psychiatry Research: Neuroimaging
| volume = 124
| issue = 1
| pages = 11–23
| doi = 10.1016/S0925-4927(03)00076-3
| url = http://linkinghub.elsevier.com/retrieve/pii/S0925492703000763
}}</ref>, [[ethnicity]]<ref name=Zilles2001>{{citation
| last1 = Zilles | first1 = K.
| last2 = Kawashima | first2 = R.
| last3 = Dabringhaus | first3 = A.
| last4 = Fukuda | first4 = H.
| last5 = Schormann | first5 = T.
| year = 2001
| title = Hemispheric Shape of European and Japanese Brains: 3-D MRI Analysis of Intersubject Variability, Ethnical, and Gender Differences
| journal = Neuroimage
| volume = 13
| issue = 2
| pages = 262–271
| doi = 10.1006/nimg.2000.0688
| url = http://linkinghub.elsevier.com/retrieve/pii/S1053811900906888
}}</ref> and [[age]]<ref name=Magnotta1999>{{CZ:Ref:Magnotta 1999 Quantitative in Vivo Measurement of Gyrification in the Human Brain: Changes Associated with Aging}}</ref> have been demonstrated, and such interindividual differences appear to be highest in regions with strong gyrification<ref name=Zilles2001>{{citation
| last1 = Zilles | first1 = K.
| last2 = Kawashima | first2 = R.
| last3 = Dabringhaus | first3 = A.
| last4 = Fukuda | first4 = H.
| last5 = Schormann | first5 = T.
| year = 2001
| title = Hemispheric Shape of European and Japanese Brains: 3-D MRI Analysis of Intersubject Variability, Ethnical, and Gender Differences
| journal = Neuroimage
| volume = 13
| issue = 2
| pages = 262–271
| doi = 10.1006/nimg.2000.0688
| url = http://linkinghub.elsevier.com/retrieve/pii/S1053811900906888
}}</ref>.


==Mechanism==
== Mechanism ==
While the extent of cortical folding has been found to be partly determined by genetic factors<ref name=Bartley1997>{{cite journal
While the extent of cortical folding has been found to be partly determined by genetic factors<ref name=Bartley1997>{{cite journal
  | author = Bartley, A.J.
  | author = Bartley, A.J.
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  | pages = 257-269
  | pages = 257-269
  | url = http://brain.oxfordjournals.org/cgi/content/abstract/120/2/257  
  | url = http://brain.oxfordjournals.org/cgi/content/abstract/120/2/257  
}}</ref><ref name=Rubenstein1999>{{citation
}}</ref><ref name=Rubenstein1999gccr>{{citation
  | last1 = Rubenstein | first1 = John L.R.
  | last1 = Rubenstein | first1 = John L.R.
  | last2 = Anderson | first2 = Stewart
  | last2 = Anderson | first2 = Stewart
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  | url = http://cercor.oxfordjournals.org/cgi/content/full/9/6/524
  | url = http://cercor.oxfordjournals.org/cgi/content/full/9/6/524
  | pmid = 10498270
  | pmid = 10498270
}}</ref><ref name=Rubenstein1999>{{citation
}}</ref><ref name=Rubenstein1999gccd>{{citation
  | last1 = Rubenstein | first1 = John L.R.
  | last1 = Rubenstein | first1 = John L.R.
  | last2 = Rakic | first2 = Pasko
  | last2 = Rakic | first2 = Pasko
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  | url = http://www.neuroscience.org/cgi/reprint/25/34/7840
  | url = http://www.neuroscience.org/cgi/reprint/25/34/7840
  | pmid = 16120786
  | pmid = 16120786
}}</ref><ref name=Kerjan2007>{{citation
}}</ref><ref name=Kerjan2007>{{CZ:Ref:Kerjan 2007 Genetic mechanisms underlying abnormal neuronal migration in classical lissencephaly}}</ref>, the underlying [[biomechanical]] mechanisms are not yet well understood. The overall folding pattern, however, can be mechanistically explained in terms of the cerebral cortex buckling under the influence of non-[[isotropic]] [[force]]s<ref name=Van1997>{{cite journal
| last1 = Kerjan | first1 = G.
| last2 = Gleeson | first2 = J.G.
| year = 2007
| title = Genetic mechanisms underlying abnormal neuronal migration in classical lissencephaly
| journal = Trends in Genetics
| volume = 23
| issue = 12
| pages = 623–630
| doi = 10.1016/j.tig.2007.09.003
| url = http://linkinghub.elsevier.com/retrieve/pii/S0168952507003289
}}</ref>, the underlying [[biomechanical]] mechanisms are not yet well understood. The overall folding pattern, however, can be mechanistically explained in terms of the cerebral cortex behaving as a gel that buckles under the influence of non-[[isotropic]] [[force]]s<ref name=Van1997>{{cite journal
  | author = Van Essen, D.C.
  | author = Van Essen, D.C.
  | year = 1997
  | year = 1997
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  | pages = 313-8
  | pages = 313-8
  | url = http://www.nature.com/nature/journal/v385/n6614/abs/385313a0.html  
  | url = http://www.nature.com/nature/journal/v385/n6614/abs/385313a0.html  
}}</ref><ref name=Mangin2004>{{citation
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| last2 = Rivière | first2 = D.
| last3 = Cachia | first3 = A.
| last4 = Duchesnay | first4 = E.
| last5 = Cointepas | first5 = Y.
| last6 = Papadopoulos-orfanos | first6 = D.
| last7 = Scifo | first7 = P.
| last8 = Ochiai | first8 = T.
| last9 = Brunelle | first9 = F.
| last10 = Régis | first10 = J.
| year = 2004
| title = A framework to study the cortical folding patterns
| journal = Neuroimage
| volume = 23
| pages = 129–138
| doi = 10.1016/j.neuroimage.2004.07.019
| url = http://dx.doi.org/10.1016/j.neuroimage.2004.07.019
}}</ref><ref name=Hilgetag2005>{{citation
}}</ref><ref name=Hilgetag2005>{{citation
  | last1 = Hilgetag | first1 = C.C.
  | last1 = Hilgetag | first1 = C.C.
Line 288: Line 539:
  | doi = 10.1371/journal.pcbi.0020022
  | doi = 10.1371/journal.pcbi.0020022
}}</ref>.  
}}</ref>.  
Possible causes of the non-isotropy include [[thermal]] [[noise]], variations in the number and timing of [[cell division]]s<ref name=Kornack1998>{{:CZ:Ref:DOI:10.1073/pnas.95.3.1242}}</ref>, [[cell migration]], [[cortical connectivity]], [[synaptic pruning]], [[brain size]] and [[metabolism]] ([[phospholipid]]s in particular), all of which may interact<ref name=Price2004>{{cite journal
Possible causes of the non-isotropy include differential growth of the cortical layers due to variations in the number and timing of [[cell division]]s<ref name=Kornack1998>{{:CZ:Ref:DOI:10.1073/pnas.95.3.1242}}</ref>, [[cell migration]], [[myelination]], [[cortical connectivity]] and [[thalamus|thalamic]] input<ref name=Dehay1996>{{citation
| last1 = Dehay | first1 = C.
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}}</ref><ref name=Francis2006/><ref name=Xu2008>{{citation
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}}</ref>. The folding, in turn, imposes constraints on the shape of cells, particulary in the outer cortical layers (V and VI)<ref name=Ferrer1987>{{citation
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}}</ref>.


==Function==
== Function ==
The primary effect of a folding process is always an increase of [[surface area]] relative to [[volume]]. Due to the laminar arrangement of the cerebral cortex, an increased cerebral surface area correlates with an increased number of neurons, which is presumed to enhance the computational capacities of the cortex within some metabolic and connectivity limits<ref name=Wen2005>{{citation
The primary effect of a folding process is always an increase of [[surface area]] relative to [[volume]]. Due to the laminar arrangement of the cerebral cortex, an increased cerebral surface area correlates with an increased number of neurons, which is presumed to enhance the computational capacities of the cortex within some metabolic and connectivity limits<ref name=Wen2005>{{citation
  | last1 = Wen | first1 = Q.
  | last1 = Wen | first1 = Q.
Line 392: Line 693:
}}</ref>.
}}</ref>.


==Medical relevance==
== Medical relevance ==
A number of disorders exist of which abnormal gyrification is a dominant feature, e.g. [[polymicrogyria]] or [[lissencephaly|lissencephalic disorders]] like [[agyria]] to [[pachygyria]]. They usually occur bilaterally but cases of, e.g., unilateral lissencephaly, have been described<ref name=Hager1991>{{citation
{{Image|Brain-disease-gyrification.png|left|400px|Gyrification from a clinical perspective: Normal adult human  [[cerebral cortex|cortical surface]] (left), [[polymicrogyria]] (center) and [[lissencephaly]] (right).}}
A number of disorders exist of which abnormal gyrification is a dominant feature, e.g. [[polymicrogyria]] or [[lissencephaly|lissencephalic disorders]]<ref name=Barkovich1991>{{citation
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| last2 = Koch | first2 = T.K.
| last3 = Carrol | first3 = C.L.
| year = 1991
| title = The spectrum of lissencephaly: report of ten patients analyzed by magnetic resonance imaging
| journal = Ann Neurol
| volume = 30
| issue = 2
| pages = 139–46
| doi = 10.1002/ana.410300204
| url = http://www.ncbi.nlm.nih.gov/pubmed/1897907
}}</ref> like [[agyria]] and [[pachygyria]]<ref name=Liang2002>{{citation
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| last2 = Lee | first2 = W.T.
| last3 = Young | first3 = C.
| last4 = Shinnforng Peng | first4 = S.
| last5 = Shen | first5 = Y.Z.
| year = 2002
| title = Agyria-pachygyria: Clinical, neuroimaging, and neurophysiologic correlations
| journal = Pediatric neurology
| volume = 27
| issue = 3
| pages = 171–176
| doi = 10.1016/S0887-8994(02)00401-0
| url = http://dx.doi.org/10.1016/S0887-8994(02)00401-0
}}</ref><ref name=Ramirez2004>{{citation
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| last2 = Lammer | first2 = E.J.
| last3 = Johnson | first3 = C.B.
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| year = 2004
| title = Autosomal recessive frontotemporal pachygyria
| journal = American Journal of Medical Genetics
| volume = 124
| issue = 3
| pages = 231–238
| doi = 10.1002/ajmg.a.20388
}}</ref><ref name=Kurul2004>{{citation
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| title = Agyria-pachygyria complex: MR findings and correlation with clinical features
| journal = Pediatric Neurology
| volume = 30
| issue = 1
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| doi = 10.1016/S0887-8994(03)00312-6
| url = http://linkinghub.elsevier.com/retrieve/pii/S0887899403003126
}}</ref>. They usually occur bilaterally but cases of, e.g., unilateral lissencephaly, have been described<ref name=Hager1991>{{citation
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}}</ref>, [[dyslexia]]<ref name=Casanova2004>{{citation
}}</ref>, [[dyslexia]]<ref name=Casanova2004>{{CZ:Ref:Casanova 2004 Reduced Brain Size and Gyrification in the Brains of Dyslexic Patients}}</ref>, [[velocardiofacial syndrome]]<ref name=Bearden2009>{{citation
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| title = Reduced Brain Size and Gyrification in the Brains of Dyslexic Patients
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}}</ref><ref name=Schaer2009>{{CZ:Ref:Schaer 2009 Congenital heart disease affects local gyrification in 22q11.2 deletion syndrome}}</ref>, [[Attention deficit hyperactivity disorder|Attention deficit hyperactivity disorder (ADHD)]]<ref name=Wolosin2009>{{citation
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}}</ref> or [[Williams syndrome]]<ref name=Schmitt2002>{{cite journal
}}</ref> or [[Williams syndrome]]<ref name=Schmitt2002>{{cite journal
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Line 540: Line 887:
}}</ref>or even throughout both hemispheres<ref name=Sallet2003rcf>{{:CZ:Ref:DOI:10.1176/appi.ajp.160.9.1606}}</ref>.
}}</ref>or even throughout both hemispheres<ref name=Sallet2003rcf>{{:CZ:Ref:DOI:10.1176/appi.ajp.160.9.1606}}</ref>.


==Quantification==
== Quantification ==
Folding of a brain can be described in both local and global terms, once a suitable representation of a brain surface has been obtained from [[neuroimaging]] data by some [[surface extraction]] technique. The latter usually delivers a triangulated surface representing either the boundary between the cerebrospinal fluid and the gray matter or between the latter and the [[white matter]] but in principle, any surface in between would do as well (e.g. the [[central layer]] which is also sometimes used). Leaving the multiple issues of [[resolution (imaging)|resolution]] and [[artifacts]] in these surface representations aside, the brain surface mesh, like any mesh of a [[manifold (geometry)|closed three-dimensional manifold]], can then be analyzed in terms of local [[curvature]] measures, from which global measures can be derived. Over the last decades, several such measures have been proposed<ref name=Rodriguez-carranza2008>{{citation
''See also the [[Gyrification/Addendum|Addendum]].''
 
{{Image|2D and 3D measures of gyrification.png|right|350px|Two possible approaches to quantify gyrification.}}
 
From the perspective of [[brain morphometry]], folding of a brain can be described in both local and global terms, once a suitable representation of a cortical surface has been obtained from [[neuroimaging]] data by some [[surface extraction]] technique. The latter usually delivers a triangulated surface representing either the boundary between the cerebrospinal fluid and the grey matter or between the latter and the [[white matter]] but in principle, any surface in between would do as well (e.g. the [[central layer]] which is also sometimes used). Leaving the multiple issues of [[resolution (imaging)|resolution]] and [[artifacts]] in these surface representations aside, the cortical surface mesh, like any mesh of a [[manifold (geometry)|closed three-dimensional manifold]], can then be analyzed in terms of local [[curvature]] measures, from which global measures can be derived. Over the last decades, several such measures have been proposed<ref name=Rodriguez-carranza2008>{{citation
  | last1 = Rodriguez-Carranza | first1 = C.E.
  | last1 = Rodriguez-Carranza | first1 = C.E.
  | last2 = Mukherjee | first2 = P.
  | last2 = Mukherjee | first2 = P.
Line 568: Line 919:
  | doi = 10.1002/ima.20138
  | doi = 10.1002/ima.20138
  | url = http://www3.interscience.wiley.com/journal/119877321/abstract
  | url = http://www3.interscience.wiley.com/journal/119877321/abstract
}}</ref>. Following the developments in imaging techniques, they were initially focused on quantification in two-dimensional spaces, later in three-dimensional ones. Some examples that are commonly used include:
}}</ref>. Following the developments in imaging techniques, they were initially focused on quantification in two-dimensional spaces, later in three-dimensional ones.
*[[L2 norm|<math> L^2 norms</math>]]:
**<math>LN_G = \tfrac{1}{4\pi} \textstyle \sqrt{\sum_A K^2}</math>, with <math>K = k_1 k_2</math> being the [[Gaussian curvature]], computed from the two [[principal curvature]]s <math>k_1</math> and <math>k_2</math>
**<math>LN_M =\tfrac{1}{4\pi} \textstyle \sum_A H^2</math>, with <math>H=\tfrac{1}{2}(k_1 + k_2)</math> being the [[Mean curvature]]
*Folding index
**<math>FI =\tfrac{1}{4\pi} \textstyle \sum_A k^{\ddagger}</math>, with <math>k^{\ddagger}=|k_1|(|k_1|-|k_2|)</math>
*Intrinsic curvature index
**<math>ICI =\tfrac{1}{4\pi} \textstyle \sum_A K^+</math>, with <math>K^+</math> being the positive Gaussian curvature
 
*Gyrification index
*Cortical complexity
*Fractal dimension
*Global gyrification index
*Local gyrification index
*Shape index
*Curvedness
*Roundness


== References==
== References ==
{{reflist|2}}
{{reflist|2}}[[Category:Suggestion Bot Tag]]

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Comparative anatomy of adult brains from various vertebrate species, highlighting the differences in brain size and gyrification. Image credit: University of Wisconsin and Michigan State Comparative Mammalian Brain Collections and National Museum of Health and Medicine (see http://www.brainmuseum.org/).


In the brain sciences, gyrification refers to both the process and the extent of folding of the cerebral cortex in mammals as a consequence of brain growth during embryonic and early postnatal development. Alternative terms for gyrification include gyration/sulcation, cortical folding, cortical convolution, fissuration and fissurization.

In the process (also known as gyrogenesis), gyri (ridges) and sulci (grooves) form on the external surface of the brain (i.e. at the boundary between the cerebrospinal fluid and the grey matter)[1]. A low extent of gyrification in a given brain is commonly referred to as lissencephaly (which may range from agyria, the total absence of folding, to pachygyria[2]), while gyrencephaly describes a high degree of folding[3].

The term gyrification is also sometimes used instead of the more common term foliation[4] to describe the folding patterns of the vertebrate cerebellum[5] that is highly convoluted in other taxa, e.g. in birds[6], and of mushroom body calyces in insect brains[7].

Phylogeny

See also brain evolution.

As illustrated in the figure, gyrification occurs across mammals[8][9], with cetaceans dominating the upper end of the spectrum[10]. It generally increases slowly with overall brain size, following a power law [11]: Small-brained placental species are indeed lissencephalic[12][13], and amongst the two living species of monotremes, the small-brained platypus is lissencephalic, while the larger brains of echidna are gyrencephalic[14]. Conversely, large-brained mammals are usually highly gyrencephalic[15][16][17], with sirenians being a notable exception[18]. A range of theoretical models exist as to the degree to which gyrification hints at the evolution of cognitive abilities in a given range of species[19][20][21].

Ontogeny

See also brain development.

(CC) Image: Kochunov et al., 2010
Sagittal slice from an MRI scan of a baboon fetus at week 24 of in utero development, clearly showing the folded cortical surface.

The folding process usually starts during fetal development—in humans around mid-gestation[22][1][23][24][25][26] —or shortly after birth, as in ferrets[27][28]. It proceeds synchronously in both hemispheres by an expansion of gyral tissue, while the sulcal roots remain in a relatively stable position throughout gyrogenesis[27][1][25]. In the adult human brain, variations due to gender[29], ethnicity[30] and age[31] have been demonstrated, and such interindividual differences appear to be highest in regions with strong gyrification[30].

Mechanism

While the extent of cortical folding has been found to be partly determined by genetic factors[32][33][34][35][36][37], the underlying biomechanical mechanisms are not yet well understood. The overall folding pattern, however, can be mechanistically explained in terms of the cerebral cortex buckling under the influence of non-isotropic forces[38][39][40][41][42]. Possible causes of the non-isotropy include differential growth of the cortical layers due to variations in the number and timing of cell divisions[43], cell migration, myelination, cortical connectivity and thalamic input[44], synaptic pruning, brain size and metabolism (phospholipids in particular), all of which may interact[45][46][47][48][3][49][50]. The folding, in turn, imposes constraints on the shape of cells, particulary in the outer cortical layers (V and VI)[51].

Function

The primary effect of a folding process is always an increase of surface area relative to volume. Due to the laminar arrangement of the cerebral cortex, an increased cerebral surface area correlates with an increased number of neurons, which is presumed to enhance the computational capacities of the cortex within some metabolic and connectivity limits[52]. In some areas of the human brain, gyrification appears indeed to reflect functional development[53] and thus to correlate with measures of intelligence[54], even though variations of these effects due to gender and age have been described [55].

Medical relevance

(CC) Image: Lefèvre and Mangin, 2010
Gyrification from a clinical perspective: Normal adult human cortical surface (left), polymicrogyria (center) and lissencephaly (right).

A number of disorders exist of which abnormal gyrification is a dominant feature, e.g. polymicrogyria or lissencephalic disorders[56] like agyria and pachygyria[57][58][59]. They usually occur bilaterally but cases of, e.g., unilateral lissencephaly, have been described[60]. Beyond these gross modifications of gyrification, more subtle variations occur in a number of neuropsychiatric disorders whose variety reflects the multitude of processes underlying gyrification[3]. Due to methodological advances in neuroimaging and computational morphometry since the late 1990s, folding patterns and abnormalities thereof can now be determined non-invasively. This is becoming increasingly important for clinical diagnostics, particular in relation to neuropsychiatric diseases like schizophrenia[61][62], autism[63], epilepsy[64], dyslexia[65], velocardiofacial syndrome[66][67], Attention deficit hyperactivity disorder (ADHD)[68] or Williams syndrome[69]. The direction of disease-associated changes depends on the cortical region and the disease subtype. In schizophrenics, for instance, gyrification has been found to increase in the dorsolateral prefrontal cortex[70] and, in different populations, to decrease in frontal and parietal regions of the left hemisphere[71]or even throughout both hemispheres[72].

Quantification

See also the Addendum.

CC Image
Two possible approaches to quantify gyrification.

From the perspective of brain morphometry, folding of a brain can be described in both local and global terms, once a suitable representation of a cortical surface has been obtained from neuroimaging data by some surface extraction technique. The latter usually delivers a triangulated surface representing either the boundary between the cerebrospinal fluid and the grey matter or between the latter and the white matter but in principle, any surface in between would do as well (e.g. the central layer which is also sometimes used). Leaving the multiple issues of resolution and artifacts in these surface representations aside, the cortical surface mesh, like any mesh of a closed three-dimensional manifold, can then be analyzed in terms of local curvature measures, from which global measures can be derived. Over the last decades, several such measures have been proposed[73][74]. Following the developments in imaging techniques, they were initially focused on quantification in two-dimensional spaces, later in three-dimensional ones.

References

  1. ↑ 1.0 1.1 1.2 Armstrong, E.; Schleicher, A.; Omran, H.; Curtis, M.; Zilles, K. (1995). "The Ontogeny of Human Gyrification". Cerebral Cortex 5 (1): 56-63.
  2. ↑ Dhellemmes, C.; S. Girard & O. Dulac et al. (1988), "Agyria—pachygyria and Miller-Dieker syndrome: clinical, genetic and chromosome studies", Human Genetics 79 (2): 163–167, DOI:10.1007/BF00280557
  3. ↑ 3.0 3.1 3.2 Francis, F.; G. Meyer & C. Fallet-Bianco et al. (2006), "Human disorders of cortical development: from past to present", European Journal of Neuroscience 23 (4): 877–893, DOI:10.1111/j.1460-9568.2006.04649.x
  4. ↑ Demaerel, P. (2002), "Abnormalities of cerebellar foliation and fissuration: classification, neurogenetics and clinicoradiological correlations", Neuroradiology 44 (8): 639–646, DOI:10.1007/s00234-002-0783-1
  5. ↑ Mares, V. & Z. Lodin (1970), "The cellular kinetics of the developing mouse cerebellum. II. The function of the external granular layer in the process of gyrification", Brain Res 23 (3): 343–352, DOI:10.1016/0006-8993(70)90061-2
  6. ↑ Iwaniuk, A.N.; Hurd, P.L.; Wylie, D.R. (2006), "Comparative Morphology of the Avian Cerebellum: I. Degree of Foliation", Brain Behav Evol 68 (1): 45–62, DOI:10.1159/000093530
  7. ↑ Farris, S.M. & N.S. Roberts (2005), "Coevolution of generalist feeding ecologies and gyrencephalic mushroom bodies in insects", Proceedings of the National Academy of Sciences 102 (48): 17394–17399, DOI:10.1073/pnas.0508430102 [e]
  8. ↑ Prothero, J.W. (1984), "Folding of the Cerebral Cortex in Mammals", Brain Behavior and Evolution 24: 152-167, DOI:10.1159/000121313
  9. ↑ Mayhew, T.M.; Mwamengele, G.L.; Dantzer, V.; Williams, S. (1996). "The gyrification of mammalian cerebral cortex: quantitative evidence of anisomorphic surface expansion during phylogenetic and ontogenetic development". Journal of Anatomy 188 (Pt 1): 53-58.
  10. ↑ Marino, L.; R.C. Connor & R. Ewan Fordyce et al. (2007), "Cetaceans Have Complex Brains for Complex Cognition", PLoS Biology 5 (5): e139, DOI:10.1371/journal.pbio.0050139 [e]
  11. ↑ Hofman, M.A. (1989). "On the evolution and geometry of the brain in mammals.". Prog Neurobiol 32 (2): 137-58. DOI:10.1016/0301-0082(89)90013-0. Research Blogging. [e]
  12. ↑ Ferrer, I.; I. Fabregues & E. Condom (1986), "A Golgi study of the sixth layer of the cerebral cortex. I. The lissencephalic brain of Rodentia, Lagomorpha, Insectivora and Chiroptera", J Anat 145: 217–234
  13. ↑ Pillay, P. & P.R. Manger (2007), "Order-specific quantitative patterns of cortical gyrification", European Journal of Neuroscience 25 (9): 2705–2712, DOI:10.1111/j.1460-9568.2007.05524.x
  14. ↑ Hassiotis, M.; G. Paxinos & K.W.S. Ashwell (2003), "The anatomy of the cerebral cortex of the echidna (Tachyglossus aculeatus)", Comparative Biochemistry and Physiology, Part A 136 (4): 827–850, DOI:10.1016/S1095-6433(03)00166-1 [e]
  15. ↑ Ferrer, I.; I. Fabregues & E. Condom (1986), "A Golgi study of the sixth layer of the cerebral cortex. II. The gyrencephalic brain of Carnivora, Artiodactyla and Primates", J Anat 146: 87–104
  16. ↑ Hof, P.R.; R. Chanis & L. Marino (2005), "Cortical Complexity in Cetacean Brains", Anatomical Record Part a Discoveries in Molecular Cellular and Evolutionary Biology 287 (1): 1142, DOI:10.1002/ar.a.20258
  17. ↑ Hakeem, A.Y.; P.R. Hof & C.C. Sherwood et al. (2005), "Brain of the African elephant (Loxodonta africana): neuroanatomy from magnetic resonance images", Anat Rec A: Discov Mol Cell Evol Biol 287 (1): 1117–1127
  18. ↑ Reep, R.L. & T.J. O'Shea (1990), "Regional brain morphometry and lissencephaly in the Sirenia", Brain Behav Evol 35 (4): 185–194, DOI:10.1159/000115866
  19. ↑ Stangier, H. (1937), "Die Furchen der Großhirnrinde beim Schimpanse", Zeitschrift für Anatomie und Entwicklungsgeschichte 107: 647, DOI:10.1007/BF02118571
  20. ↑ Supèr, H.; Uylings, H.B.M. (2001), "The Early Differentiation of the Neocortex: a Hypothesis on Neocortical Evolution", Cerebral Cortex 11 (12): 1101–1109, DOI:10.1093/cercor/11.12.1101
  21. ↑ Sereno, M.I. & R.B. Tootell (2005), "From monkeys to humans: what do we now know about brain homologies?", Curr Opin Neurobiol 15 (2): 135–44, DOI:10.1016/j.conb.2005.03.014
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    A study notable for the relatively large sample size (44 participants with 22q11.2 deletion syndrome, a condition that affects only 1 in about 5,000 newborns) that corroborates previous studies linking 22q11.2DS to congenital heart disease and decreased gyrification. It is also interesting because it did not find a correlation between gyrification and cortical thickness.
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