Lobular homology in cerebellar hemispheres of humans, non-human primates and rodents: a structural, axonal tracing and molecular expression analysis

Abstract

Comparative neuroanatomy provides insights into the evolutionary functional adaptation of specific mammalian cerebellar lobules, in which the lobulation pattern and functional localization are conserved. However, accurate identification of homologous lobules among mammalian species is challenging. In this review, we discuss the inter-species homology of crus I and II lobules which occupy a large volume in the posterior cerebellar hemisphere, particularly in humans. Both crus I/II in humans are homologous to crus I/II in non-human primates, according to Paxinos and colleagues; however, this area has been defined as crus I alone in non-human primates, according to Larsell and Brodal. Our neuroanatomical analyses in humans, macaques, marmosets, rats, and mice demonstrate that both crus I/II in humans are homologous to crus I/II or crus I alone in non-human primates, depending on previous definitions, and to crus I alone in rodents. Here, we refer to the region homologous to human crus I/II lobules as "ansiform area (AA)" across animals. Our results show that the AA's olivocerebellar climbing fiber and Purkinje cell projections as well as aldolase C gene expression patterns are both distinct and conserved in marmosets and rodents. The relative size of the AA, as represented by the AA volume fraction in the whole cerebellum was 0.34 in human, 0.19 in macaque, and approximately 0.1 in marmoset and rodents. These results indicate that the AA reflects an evolutionarily conserved structure in the mammalian cerebellum, which is characterized by distinct connectivity from neighboring lobules and a massive expansion in skillful primates.

Cerebellar Lobulus Simplex and Crus I Differentially Represent Phase and Phase Difference of Prefrontal Cortical and Hippocampal Oscillations

“…Although primates and rodents share evolutionarily conserved features in protein expression, neural circuit projection patterns, and gross anatomy, specific adaptations exist, such as expansion of lobules and the functional maps therein. Therefore, although a direct extrapolation of our data into other higher-order species may be challenging, the fundamental basis of how the cerebellum is organized and how it interacts with other brain regions is predicted to share significant homology across mammals ( Luo et al, 2017 ; Sugihara, 2018 ).…”

Primate homologs of mouse cortico-striatal circuits

“…Tracer studies in rodents and non-human primates have shown that prefrontal projections to the cerebellar cortex are conserved across species (Kelly and Strick, 2003; Schmahmann and Pandya, 1997; Wiesendanger and Wiesendanger, 1982), however research also suggests that prefrontal-cerebellar circuits have selectively expanded in humans compared to other species. Specifically, prefrontal projections to the pontine nucleus (Ramnani et al, 2006), volume of prefrontal-projecting cerebellar lobules Crus I and Crus II (Balsters et al, 2010; Luo et al, 2017), and the volume and connections of the dorsal dentate nucleus (Baizer, 2014; Matano, 2001; Steele et al, 2016) have all expanded in humans relative to motor cerebellar circuitry across species. Studies of cerebellar evolution have generally suggested that Crus I and Crus II are homologous across species (Larsell, 1952) even though they have expanded in humans.…”

A cerebellar role in evidence-guided decision-making

“…We focused our study on the ansiform area (crus I) (Luo et al, 2017) of the posterior hemispheric cerebellum (Figure 1F), a region that evolutionarily expanded with prefrontal cortex (Balsters et al, 2010) and communicates bidirectionally with forebrain regions including prefrontal, parietal, and somatosensory cortex (Kelly & Strick, 2003; Prevosto et al, 2010; Proville et al, 2014). This cerebellar region represents orofacial features under anesthesia (Manni & Petrosini, 2004; Shambes, Beermann, & Welker, 1978), suggesting that it might aid in processing complex task-related information.…”