Gyrification

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

In the brain sciences, gyrification (or cortical folding or fissuration) refers to the folding of the cerebral cortex as a consequence of brain growth during embryonic and early postnatal development. In this process, gyri (ridges) and sulci (fissures) form on the outermost surface of the brain. 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 birds[1].


Phylogeny

As illustrated in the figure, gyrification occurs across mammals[2] in gradually different manner: It increases slowly with overall brain size, following a power law [3], 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[4][5].

Ontogeny

The folding process usually starts during embryonic development[6], in humans around mid-gestation [7]. While the extent of cortical folding has been found to be partly determined by genetic factors[8][9][10][11], 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 forces[12][13][14][15]. Possible causes of the non-isotropy include thermal noise, variations in the number and timing of cell divisions, cell migration, cortical connectivity, synaptic pruning, brain size and metabolism (phospholipids in particular), all of which may interact[16][17][18][19].


Medical relevance

This multitude of underlying processes has rendered the concept of gyrification increasingly important for clinical diagnostics in recent years, since gyrification in some areas of the human brain appears to reflect functional development[20] and thus to correlate with measures of intelligence[21], and disturbances in the folding pattern — as determined by non-invasive neuroimaging — can be taken as indicators of neuropsychiatric diseases if differences due to gender and age are accounted for [22]. Apart from being a marker of disorders like schizophrenia or Williams syndrome[23][24], a number of disorders exist of which abnormal gyrification is a dominant feature, e.g. agyria, pachygyria, polymicrogyria or lissencephaly[17].


Quantification

Over the last decades, several measures of gyrification have been proposed[25]. Following the developments in imaging techniques, they were initially focused on quantification in two-dimensional spaces, later in three-dimensional ones:

  1. Folding index
  2. Gyrification index
  3. Cortical complexity
  4. Fractal dimension
  5. Global gyrification index
  6. Local gyrification index
  7. Curvature measures

References

  1. ↑ 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
  2. ↑ 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.
  3. ↑ 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]
  4. ↑ 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
  5. ↑ 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
  6. ↑ Neal, J.; M. Takahashi & M. Silva et al. (2007), "Insights into the gyrification of developing ferret brain by magnetic resonance imaging", Journal of Anatomy 210 (1): 66–77, DOI:10.1111/j.1469-7580.2006.00674.x
  7. ↑ Armstrong, E.; Schleicher, A.; Omran, H.; Curtis, M.; Zilles, K. (1995). "The Ontogeny of Human Gyrification". Cerebral Cortex 5 (1): 56-63.
  8. ↑ Bartley, A.J.; Jones, D.W.; Weinberger, D.R.. "Genetic variability of human brain size and cortical gyral patterns". Brain 120 (2): 257-269.
  9. ↑ Chenn, Anjen; Walsh, Christopher A. (2002), "Regulation of Cerebral Cortical Size by Control of Cell Cycle Exit in Neural Precursors", Science 297 (5580): 365–9, DOI:10.1126/science.1074192 [e]
  10. ↑ Kippenhan, J. Shane; Rosanna K. Olsen & Carolyn B. Mervis et al. (2005), "Genetic Contributions to Human Gyrification: Sulcal Morphometry in Williams Syndrome", Journal of Neuroscience 25 (34): 7840, DOI:10.1523/JNEUROSCI.1722-05.2005
  11. ↑ Kerjan, G. & J.G. Gleeson (2007), "Genetic mechanisms underlying abnormal neuronal migration in classical lissencephaly", Trends in Genetics 23 (12): 623–630, DOI:10.1016/j.tig.2007.09.003 [e]
  12. ↑ Van Essen, D.C. (1997). "A tension-based theory of morphogenesis and compact wiring in the central nervous system". Nature 385 (6614): 313-8.
  13. ↑ Hilgetag, C.C. & H. Barbas (2005), "Developmental mechanics of the primate cerebral cortex", Anat Embryol (Berl) 210 (5-6): 411–7, DOI:10.1007/s00429-005-0041-5
  14. ↑ Mora, T.; Boudaoud, A. (2006). "Buckling of swelling gels". The European Physical Journal E - Soft Matter 20 (2): 119-124.
  15. ↑ Hilgetag, C.C. & H. Barbas (2006), "Role of Mechanical Factors in the Morphology of the Primate Cerebral Cortex", PLoS Comput Biol 2 (3): e22, DOI:10.1371/journal.pcbi.0020022
  16. ↑ Price, D.J. (2004). "Lipids make smooth brains gyrate". Trends in Neurosciences 27 (7): 362-364.
  17. ↑ 17.0 17.1 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
  18. ↑ Xu, G.; P.V. Bayly & L.A. Taber (2008), "Residual stress in the adult mouse brain", Biomech Model Mechanobiol, DOI:10.1007/s10237-008-0131-4
  19. ↑ Toro, R.; Perron, M.; Pike, B.; Richer, L.; Veillette, S.; Pausova, Z.; Paus, T. (2008). "Brain Size and Folding of the Human Cerebral Cortex". Cerebral Cortex.
  20. ↑ Dubois, J.; M. Benders & C. Borradori-tolsa et al. (2008), "Primary cortical folding in the human newborn: an early marker of later functional development", Brain 131 (8): 2028, DOI:10.1093/brain/awn137 [e]
  21. ↑ Lüders, Eileen; Narr, Katherine L.; Bilder, Robert M.; Szeszko, Philip R.; Gurbani, Mala N.; Hamilton, Liberty; Toga, Arthur W.; Gaser, Christian (2007), "Mapping the Relationship between Cortical Convolution and Intelligence: Effects of Gender", Cerebral Cortex 18 (9): 2019, DOI:10.1093/cercor/bhm227
  22. ↑ Lüders, E.; K.L. Narr & P.M. Thompson et al. (2004), "Gender differences in cortical complexity", Nat Neurosci 7 (8): 799–800, DOI:10.1038/nn1277
  23. ↑ White, T.; Andreasen, N.C.; Nopoulos, P.; Magnotta, V. (2003), "Gyrification abnormalities in childhood- and adolescent-onset schizophrenia", Biological Psychiatry 54 (4): 418–426, DOI:10.1016/S0006-3223(03)00065-9
  24. ↑ Schmitt, J.E.; Watts, K.; Eliez, S.; Bellugi, U.; Galaburda, A.M.; Reiss, A.L. (2002). "Increased gyrification in Williams syndrome: evidence using 3D MRI methods". Developmental Medicine & Child Neurology 44 (5): 292-295. DOI:10.1111/j.1469-8749.2002.tb00813.x. Research Blogging.
  25. ↑ Rodriguez-Carranza, C.E.; P. Mukherjee & D. Vigneron et al. (2008), "A framework for in vivo quantification of regional brain folding in premature neonates", Neuroimage 41: 462, DOI:10.1016/j.neuroimage.2008.01.008
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