The Cerebellum and Cerebellum-Like Structures of Cartilaginous Fishes

Abstract

The cerebellum is well developed in cartilaginous fishes, with the same cell types (barring basket cells) and organizational features found in other vertebrate groups, including mammals. In particular, the lattice-like organization of cerebellar cortex (with a molecular layer of parallel fibers, interneurons, spiny Purkinje cell dendrites, and climbing fibers) is a defining characteristic. In addition to the cerebellum, cartilaginous fishes have cerebellum-like structures in the dorsolateral wall of the hindbrain. These structures are adjacent to and, in part, contiguous with the cerebellum. They are cerebellum-like in that they have a molecular layer of parallel fibers and inhibitory interneurons that has striking organizational similarities to the molecular layer of the cerebellar cortex. However, these structures also have characteristics that differ from the cerebellum. For example, cerebellum-like structures do not have climbing fibers and are clearly sensory. They receive direct afferent input from peripheral sensory receptors and relay their outputs to midbrain sensory areas. As a consequence of this close sensory association and the ability of researchers to characterize signal processing in these structures in a behaviorally relevant context, good progress has been made in determining the fundamental processing algorithm of the cerebellum-like structures. This algorithm enables the molecular layer to act as an adaptive filter that cancels self-generated noise in electrosensory and lateral line systems. Given the fundamental similarities of the molecular layer across these structures and the phylogeny of these structures across basal vertebrates, it is clear that these structures share a common genetic-developmental program. Syngeny is a term that has been used to describe similarity of structure due to a shared genetic-developmental program, whether the structures are phylogenetically homologous or not. Given that the cerebellum and cerebellum-like structures are physically adjacent, we propose that cerebellum-like structures were the evolutionary antecedent of the cerebellum and that the cerebellum arose through a change in the genetic-developmental program, amounting to a duplication of existing structure. Such duplication to form adjacent structures can be considered a special case of syngeny. On this view, the cerebellum is an evolutionary innovation in gnathostomes that is literally superimposed on pre-existing underlying brain structures and pathways. From this perspective, the cerebellum can be considered an example of ‘subsumption architecture’, a term that describes the addition of modules that add computational power while maintaining existing fundamental functionality. This addition is reflected in the finding that in elasmobranchs with relatively large brains, the size of the telencephalon and cerebellum enlarge disproportionately, while those parts of the brain that contain more direct sensory and motor connections do not. Added ‘computational’ power in the chondrichthyan brain and the compa...

Variation in Brain Organization of Coral Reef Fish Larvae according to Life History Traits

“…Moreover, several studies have shown that the importance of cytoarchitecture and fiber connections in the functions of the different brain subdivisions in fish [e.g. cerebellum, Montgomery et al, 2012]. However, to date, no data exist on the variation in brain morphology (for both external form and internal structure) of larval-stage coral reef fish.…”

Ontogenetic Shifts in Brain Organization in the Bluespotted Stingray <b><i>Neotrygon kuhlii</i></b> (Chondrichthyes: Dasyatidae)

“…Olfaction is known to be important for navigation in cartilaginous fishes [Gardiner et al, 2015;Nosal et al, 2016] and it has been suggested that a primary function of olfaction is navigation, with variability in the size of the olfactory bulbs among species reflecting variation in navigational demand [Jacobs, 2012]. Moreover, cerebellar size and complexity are associated with enhanced sensorimotor integration and motor performance in fishes [Bauchot et al, 1977;Ridet and Bauchot, 1990;Kotrschal et al, 1998;New, 2001;Wagner, 2001;Yopak et al, 2007;Lisney et al, 2008;Montgomery et al, 2012]. Therefore, it is not unreasonable to suggest that these two brain areas could become enlarged and/or more structurally complex in animals that increase their activity space and occupy new habitats during ontogeny.…”

Brain Evolution and Comparative Neuroanatomy

“…Whether the cerebellum exists in hagfish is debated, and it is absent in lampreys (Montgomery et al, 2012), but appears as a well-developed structure in chondrichthyes, the cartilaginous fishes, and in all gnathostomes (jawed vertebrates). It has been proposed that the cerebellum evolved by duplication of cerebellum-like structures in the dorsolateral wall of the hindbrain in cartilaginous fishes, which receive input from the lateral line system and the electrosensory system (Montgomery et al, 2012).…”

“…It has been proposed that the cerebellum evolved by duplication of cerebellum-like structures in the dorsolateral wall of the hindbrain in cartilaginous fishes, which receive input from the lateral line system and the electrosensory system (Montgomery et al, 2012). Such cerebellum-like structures are present in lampreys, in the absence of a cerebellum, suggesting that they may be forerunners of the cerebellum itself.…”