Escaping the nocturnal bottleneck, and the evolution of the dorsal and ventral streams of visual processing in primates

Abstract

Early mammals were small and nocturnal. Their visual systems had regressed and they had poor vision. After the extinction of the dinosaurs 66 mya, some but not all escaped the ‘nocturnal bottleneck’ by recovering high-acuity vision. By contrast, early primates escaped the bottleneck within the age of dinosaurs by having large forward-facing eyes and acute vision while remaining nocturnal. We propose that these primates differed from other mammals by changing the balance between two sources of visual information to cortex. Thus, cortical processing became less dependent on a relay of information from the superior colliculus (SC) to temporal cortex and more dependent on information distributed from primary visual cortex (V1). In addition, the two major classes of visual information from the retina became highly segregated into magnocellular (M cell) projections from V1 to the primate-specific temporal visual area (MT), and parvocellular-dominated projections to the dorsolateral visual area (DL or V4). The greatly expanded P cell inputs from V1 informed the ventral stream of cortical processing involving temporal and frontal cortex. The M cell pathways from V1 and the SC informed the dorsal stream of cortical processing involving MT, surrounding temporal cortex, and parietal–frontal sensorimotor domains. This article is part of the theme issue ‘Systems neuroscience through the lens of evolutionary theory’.

Frontoparietal connectivity as a product of convergent evolution in rodents and primates: functional connectivity topologies in grey squirrels, rats, and marmosets

“…At present, it cannot be ruled out that a frontoparietal network organization is typical in many rodent species and that the subfamily Muridae, which includes Old World rats and mice, lost this organization due to their adaptation to a terrestrial and mainly nocturnal lifestyle. It has been recently posited that evolution of the dorsal and ventral visual processing streams in both primates and squirrels was the result of occupying new, diurnal environments after the extinction of dinosaurs 14 .…”

“…Like most primates, grey squirrels are diurnal. They have a much better developed visual system than nocturnal rats 15 , including two-cone color vision 16 , 17 , larger visual cortical areas 17 and 18 18 , a 5-layered geniculate nucleus 19 , and a superior colliculus that is about ten times bigger than would be expected for a rat of similar size 14 , 15 . Studies using histochemical tracing and electrical microstimulation in squirrels suggest that connectivity of somatosensory and motor cortex have an organization that may be more similar to primates than that of rats or mice 20 .…”

“…The North American grey squirrel ( Sciurus carolinensis ) resembles the small New World marmoset monkey ( Callithrix jacchus ) in several major ways: they have a similar arboreal lifestyle, they both have long tails that help them keep their balance, their digits have sharp claws, and they have similar body sizes 14 . Like most primates, grey squirrels are diurnal.…”

Lessons from comparative primatology for understanding trait covariation and diversity in evolutionary ecology

“…Research on visual input also provided an integrated perspective (van Essen et al 1992). This research has entailed a focus on the integration of, for example, the brain–vision system (Kirk 2006a) and also on external drivers, such as period of activity (Kirk 2006b, Ross & Kirk 2007, Kaas et al 2022) and diet (Kirk 2006b). In addition to intersecting with disciplines such as anthropology, psychology, comparative anatomy, and behavioural ecology, our bibliometric analyses evidence that comparative studies of primates intersect with more recent fields, such as conservation biology (e.g.…”

Neuroscience needs evolution

“…Another dramatic transition started with the mammalian retreat into nocturnal life and then, about 200 million years later, a return to diurnal life in some primate species. This is described in a paper by Jon Kaas, Hui-Xin Qi and Iwona Stepniewska, which focuses on the corresponding changes to the visual system [ 48 ]. In particular, unlike other mammals, primates evolved good vision even when still nocturnal.…”