Evolution of the cerebellar cortex: the selective expansion of prefrontal-projecting cerebellar lobules

Abstract

It has been suggested that interconnected brain areas evolve in tandem because evolutionary pressures act on complete functional systems rather than on individual brain areas. The cerebellar cortex has reciprocal connections with both the prefrontal cortex and motor cortex, forming independent loops with each. Specifically, in capuchin monkeys cerebellar cortical lobules Crus I and Crus II connect with prefrontal cortex, whereas the primary motor cortex connects with cerebellar lobules V, VI, VIIb, and VIIIa. Comparisons of extant primate species suggest that the prefrontal cortex has expanded more than cortical motor areas in human evolution. Given the enlargement of the prefrontal cortex relative to motor cortex in humans, our hypothesis would predict corresponding volumetric increases in the parts of the cerebellum connected to the prefrontal cortex, relative to cerebellar lobules connected to the motor cortex. We tested the hypothesis by comparing the volumes of cerebellar lobules in structural MRI scans in capuchins, chimpanzees and humans. The fractions of cerebellar volume occupied by Crus I and Crus II were significantly larger in humans compared to chimpanzees and capuchins. Our results therefore support the hypothesis that in the cortico-cerebellar system, functionally related structures evolve in concert with each other. The evolutionary expansion of these prefrontal-projecting cerebellar territories might contribute to the evolution of the higher cognitive functions of humans.

Figure 1:

Midsaggital and intermediate hemisphere sections of the cerebellum in humans (a-b), chimpanszees (c-d), and capuchin monkeys (e-f). Sections a-b from Larsell (1972). Sections c-f from Larsell (1970). Abreviations: v.m.a. anterior medullary velum; dec.n.IV, decussation of the trochlear never; f.prc, precentral fissure; f.pc, preculminate fissure; f incul, intraculinate fissure; f.pr. fissure prima; f.p.s. posterior superior fissure; f.v. folium vermis; f.in,cr intercrural fissure (f.hor, horizontal fissure); s.int cr1,2 intracural sulcus 1,2; f.ppd, prepyramidial fissure; f.apm, ansoparamedian fissure; s.ip, intrapyramidal sulcus; f.sec, fissura secunda; pl.ch, choroid plexus; f.pl, posterolateral fissure; s.int HVI,HVIIIA, intralobular sulcus of HVI,HVIIIA; to, tonsilla.

Figure 2:

Anatomical location of lobular masks in representative cases. Masks (coloured: Lobule V – red; Lobule VI – blue; Crus I – green; Crus II - magenta; Lobule VIIb - yellow; Lobule VIIIa - cyan) are overlaid on T1 anatomical images (greyscale). Sagittal slices, lateral (left) to medial (right).

Figure 3:

a) Graph showing the proportion of whole cerebellum occupied by each lobule. b) Graph showing the proportion of the masked area (sum area of lobules V, VI, Crus I, Crus II, VIIb, VIIIa) occupied by each lobule.