The stepwise development of the lamprey visual system and its evolutionary implications

Abstract

Lampreys, which represent the oldest group of living vertebrates (cyclostomes), show unique eye development. The lamprey larva has only eyespot-like immature eyes beneath a non-transparent skin, whereas after metamorphosis, the adult has well-developed image-forming camera eyes. To establish a functional visual system, well-organised visual centres as well as motor components (e.g. trunk muscles for locomotion) and interactions between them are needed. Here we review the available knowledge concerning the structure, function and development of the different parts of the lamprey visual system. The lamprey exhibits stepwise development of the visual system during its life cycle. In prolarvae and early larvae, the 'primary' retina does not have horizontal and amacrine cells, but does have photoreceptors, bipolar cells and ganglion cells. At this stage, the optic nerve projects mostly to the pretectum, where the dendrites of neurons in the nucleus of the medial longitudinal fasciculus (nMLF) appear to receive direct visual information and send motor outputs to the neck and trunk muscles. This simple neural circuit may generate negative phototaxis. Through the larval period, the lateral region of the retina grows again to form the 'secondary' retina and the topographic retinotectal projection of the optic nerve is formed, and at the same time, the extra-ocular muscles progressively develop. During metamorphosis, horizontal and amacrine cells differentiate for the first time, and the optic tectum expands and becomes laminated. The adult lamprey then has a sophisticated visual system for image-forming and visual decision-making. In the adult lamprey, the thalamic pathway (retina-thalamus-cortex/pallium) also transmits visual stimuli. Because the primary, simple light-detecting circuit in larval lamprey shares functional and developmental similarities with that of protochordates (amphioxus and tunicates), the visual development of the lamprey provides information regarding the evolutionary transition of the vertebrate visual system from the protochordate-type to the vertebrate-type.

Visuo-vestibular gaze control – conserved subcortical processing

“…The clear interconnectivity between pretectal, vestibular, and oculomotor nuclei also supports the notion that both OKR and VOR are of subcortical origins, highlighting a principal role of subcortical mechanisms, which has likely been maintained in mammals due to the phylogenetic preservation of the visual system 13,18,20,21 . The absence of a functional cerebellum in lampreys shows that cerebellar pathways are not needed for the OKR.…”

“…We here analyze stabilizing eye movements in the lamprey, the oldest extant vertebrate, and the neuronal pathways responsible for multisensory integration. Lampreys have well developed imageforming camera eyes, and the organization of eye muscles and motor nuclei is remarkably similar to other vertebrates 1,[11][12][13] . They exhibit VOR 14 , and the underlying pathways are similar to those of other vertebrates 15 .…”

The role of the optic tectum for visually evoked orienting and evasive movements

“…Our results support the notion that preferential activation of coBP neurons elicits orienting movements, while iBP neurons trigger evasive movements, depending on the characteristics of the visual stimuli (type, position, etc.). Pretectal neurons can also excite reticulospinal neurons and are known to mediate the dorsal light response and negative phototaxis (11,(28)(29)(30)(31), but they will not contribute to the effect of looming stimuli.…”

“…The emergence of the optic tectum is linked to the evolution of image-forming vision, and contributed to the evolutionary success of vertebrates (7)(8)(9)(10). Establishment of the neural circuits responsible for visual decision making at the level of the optic tectum represents a behavioral innovation and an important evolutionary event (11).…”

Expression of Urocortin 3 mRNA in the Central Nervous System of the Sea Lamprey Petromyzon marinus

“…A comparison between adults and larvae revealed important developmental changes in Ucn3 expression, with new positive populations appearing in the striatum, torus semicircularis, isthmus and nucleus of the solitary tract after the metamorphosis. Transformation in the sea lamprey is complex, and in the nervous system, it largely affects the visual system including the eye and optic tectum [36][37][38][39][40][41], but also other neural systems such as the medial pallium, cutaneous sensory systems and the olfactory rosette [42][43][44]. Other body organs also suffer important anatomical and physiological changes during transformation to adapt adult lampreys to a new adult life-style (free and ectoparasitic life), which is very different from the blind, burrowing, water-filtering larvae [31].…”