Evolutionary origin of alpha rhythms in vertebrates.

The purpose of this review extends beyond the traditional triune brain model, aiming to elucidate the evolutionary aspects of alpha rhythms in vertebrates. The forebrain, comprising the telencephalon (pallium) and diencephalon (thalamus, hypothalamus), is a common feature in the brains of all vertebrates. In mammals, evolution has prioritized the development of the forebrain, especially the neocortex, over the midbrain (mesencephalon) optic tectum, which serves as the prototype for the visual brain. This evolution enables mammals to process visual information in the retina-thalamus (lateral geniculate nucleus)-occipital cortex pathway. The origin of posterior-dominant alpha rhythms observed in mammals in quiet and dark environments is not solely attributed to cholinergic pontine nuclei cells functioning as a 10 Hz pacemaker in the brainstem. It also involves the ability of the neocortex's cortical layers to generate traveling waves of alpha rhythms with waxing and waning characteristics. The utilization of alpha rhythms might have facilitated the shift of attention from external visual inputs to internal cognitive processes as an adaptation to thrive in dark environments. The evolution of alpha rhythms might trace back to the dinosaur era, suggesting that enhanced cortical connectivity linked to alpha bands could have facilitated the development of nocturnal awakening in the ancestors of mammals. In fishes, reptiles, and birds, the pallium lacks a cortical layer. However, there is a lack of research clearly observing dominant alpha rhythms in the pallium or organized nuclear structures in fishes, reptiles, or birds. Through convergent evolution, the pallium of birds, which exhibits cortex-like fiber architecture, has not only acquired advanced cognitive and motor abilities but also the capability to generate low-frequency oscillations (4-25 Hz) resembling alpha rhythms. This suggests that the origins of alpha rhythms might lie in the pallium of a common ancestor of birds and mammals.
Competing Interests: The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. The author(s) declared that they were an editorial board member of Frontiers, at the time of submission. This had no impact on the peer review process and the final decision.
(Copyright © 2024 Shibata, Hattori, Nishijo, Kuroda and Takakusaki.)