Gyrification

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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]
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  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]
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  66. ↑ Bearden, Carrie E.; Theo G.M. Van Erp & Rebecca A. Dutton et al. (2009), "Alterations in Midline Cortical Thickness and Gyrification Patterns Mapped in Children with 22q11.2 Deletions", Cerebral Cortex 19 (1): 115, DOI:10.1093/cercor/bhn064
  67. ↑ Schaer M, Glaser B, Cuadra MB, Debbane M, Thiran JP, Eliez S (2009). "Congenital heart disease affects local gyrification in 22q11.2 deletion syndrome". Dev Med Child Neurol 51 (9): 746-53. DOI:10.1111/j.1469-8749.2009.03281.x. PMID 19416334. Research Blogging. [e]
    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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