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 verteb...

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Main Authors: Takashi Shibata, Noriaki Hattori, Hisao Nishijo, Satoshi Kuroda, Kaoru Takakusaki
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-04-01
Series:Frontiers in Behavioral Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fnbeh.2024.1384340/full
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author Takashi Shibata
Takashi Shibata
Noriaki Hattori
Hisao Nishijo
Satoshi Kuroda
Kaoru Takakusaki
author_facet Takashi Shibata
Takashi Shibata
Noriaki Hattori
Hisao Nishijo
Satoshi Kuroda
Kaoru Takakusaki
author_sort Takashi Shibata
collection DOAJ
description 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.
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spelling doaj.art-d33a12d8d8944ef692124ab8e7762ff12024-04-08T04:41:08ZengFrontiers Media S.A.Frontiers in Behavioral Neuroscience1662-51532024-04-011810.3389/fnbeh.2024.13843401384340Evolutionary origin of alpha rhythms in vertebratesTakashi Shibata0Takashi Shibata1Noriaki Hattori2Hisao Nishijo3Satoshi Kuroda4Kaoru Takakusaki5Department of Neurosurgery, Toyama University Hospital, Toyama, JapanDepartment of Neurosurgery, Toyama Nishi General Hospital, Toyama, JapanDepartment of Rehabilitation, Toyama University Hospital, Toyama, JapanFaculty of Human Sciences, University of East Asia, Yamaguchi, JapanDepartment of Neurosurgery, Toyama University Hospital, Toyama, JapanThe Research Center for Brain Function and Medical Engineering, Asahikawa Medical University, Asahikawa, JapanThe 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.https://www.frontiersin.org/articles/10.3389/fnbeh.2024.1384340/fullalpha rhythmspedunculopontine nucleusvertebratesnocturnal mammalspalliumneocortex
spellingShingle Takashi Shibata
Takashi Shibata
Noriaki Hattori
Hisao Nishijo
Satoshi Kuroda
Kaoru Takakusaki
Evolutionary origin of alpha rhythms in vertebrates
Frontiers in Behavioral Neuroscience
alpha rhythms
pedunculopontine nucleus
vertebrates
nocturnal mammals
pallium
neocortex
title Evolutionary origin of alpha rhythms in vertebrates
title_full Evolutionary origin of alpha rhythms in vertebrates
title_fullStr Evolutionary origin of alpha rhythms in vertebrates
title_full_unstemmed Evolutionary origin of alpha rhythms in vertebrates
title_short Evolutionary origin of alpha rhythms in vertebrates
title_sort evolutionary origin of alpha rhythms in vertebrates
topic alpha rhythms
pedunculopontine nucleus
vertebrates
nocturnal mammals
pallium
neocortex
url https://www.frontiersin.org/articles/10.3389/fnbeh.2024.1384340/full
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