On the evolutionary origin of the vertebrate cortex
Author: Suryanarayana, Shreyas M
Date: 2019-12-06
Location: Biomedicum 1, D0320, Karolinska institutet, Solna
Time: 13.15
Department: Inst för neurovetenskap / Dept of Neuroscience
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Thesis (5.173Mb)
Abstract
The aim of this thesis is to dissect out the minimalistic ancestral neural hardware, which has been conserved in homologue structures of the cerebral cortex and in particular the neocortex, across vertebrates. For this purpose, we utilise the lamprey - a cyclostome (jawless vertebrate), and we compare its anatomical homologue of cortex, the lateral pallium (LPal), in terms of its connectivity, cytoarchitecture and sensory organisation with that of the mammalian neocortex. The lamprey has an important phylogenetic position as a basal and most ancestral vertebrate group that diverged from the main vertebrate line of evolution around 560 million years ago. The dissection of the homologue cortical structures in lamprey will allow us to understand the ancestral design of cortex in the common vertebrate ancestor, consequently contributing to develop a potential pan-vertebrate schema for cortical evolution.
In Paper 1, the role of lateral pallium in generation of different types of movements, as well as its efferent projection pattern to downstream motor centres were investigated. The results showed that the lamprey LPal mirrors the efferent projection pattern seen in the neocortex in mammals, with projections to the basal ganglia nuclei, optic tectum, mesencephalic tegmentum and to the rostral spinal cord. Electrical stimulation of the LPal generated well-defined movements of the eyes, mouth, body as well as locomotion, demonstrating the presence of a motor area. Following this in Paper 2, the cytoarchitecture and the microcircuit was examined and the LPal was shown to be a three-layered cortex and consist of similar proportions of excitatory neurons and GABAergic neurons as the mammalian cortex. The LPal also had equivalent functional cell types - the efferent projection neurons similar to neocortical layer 5b cells (PT-type), the thalamo-recipient neurons as layer 4-like cells and the intratelencephalic (IT)-type neurons. The results indicated the presence of a basic input-output microcircuitry reminiscent of the mammalian neocortex. In Paper 3, the organisation of visual and somatosensory input was examined. The lamprey as other anamniotes, was thought to have largely olfactory processing in the “primitive” pallium. Our investigations showed that the lamprey LPal/cortex indeed had a visual area with a retinotopic organisation, as well as a somatosensory area with distinct representations of the head and body, all relayed via the thalamus. There is thus a motor area and separate visual and somatosensory areas in the lamprey cortex. In paper 4, we examined the afferent and efferent connectivity of the dopaminergic substancia nigra pars compacta (SNc) which was virtually identical to that seen in mammals, including a strong input from the LPal.
The overall results of the four studies demonstrated an unforeseen level of conservation of the basic microcircuitry, cytoarchitecture, cell-types, efferent connectivity and sensorimotor organisation of the lamprey LPal/cortex providing compelling evidence for common ancestry with the mammalian neocortex. This leads to the overarching conclusion that the basic features of the cortex, and when taken in tandem with previous extensive subcortical homologies demonstrated, the basic design of the forebrain, had already evolved at the dawn of vertebrate evolution.
In Paper 1, the role of lateral pallium in generation of different types of movements, as well as its efferent projection pattern to downstream motor centres were investigated. The results showed that the lamprey LPal mirrors the efferent projection pattern seen in the neocortex in mammals, with projections to the basal ganglia nuclei, optic tectum, mesencephalic tegmentum and to the rostral spinal cord. Electrical stimulation of the LPal generated well-defined movements of the eyes, mouth, body as well as locomotion, demonstrating the presence of a motor area. Following this in Paper 2, the cytoarchitecture and the microcircuit was examined and the LPal was shown to be a three-layered cortex and consist of similar proportions of excitatory neurons and GABAergic neurons as the mammalian cortex. The LPal also had equivalent functional cell types - the efferent projection neurons similar to neocortical layer 5b cells (PT-type), the thalamo-recipient neurons as layer 4-like cells and the intratelencephalic (IT)-type neurons. The results indicated the presence of a basic input-output microcircuitry reminiscent of the mammalian neocortex. In Paper 3, the organisation of visual and somatosensory input was examined. The lamprey as other anamniotes, was thought to have largely olfactory processing in the “primitive” pallium. Our investigations showed that the lamprey LPal/cortex indeed had a visual area with a retinotopic organisation, as well as a somatosensory area with distinct representations of the head and body, all relayed via the thalamus. There is thus a motor area and separate visual and somatosensory areas in the lamprey cortex. In paper 4, we examined the afferent and efferent connectivity of the dopaminergic substancia nigra pars compacta (SNc) which was virtually identical to that seen in mammals, including a strong input from the LPal.
The overall results of the four studies demonstrated an unforeseen level of conservation of the basic microcircuitry, cytoarchitecture, cell-types, efferent connectivity and sensorimotor organisation of the lamprey LPal/cortex providing compelling evidence for common ancestry with the mammalian neocortex. This leads to the overarching conclusion that the basic features of the cortex, and when taken in tandem with previous extensive subcortical homologies demonstrated, the basic design of the forebrain, had already evolved at the dawn of vertebrate evolution.
List of papers:
I. Ocana, F.M*., Suryanarayana, S.M*., Saitoh, K., Kardamakis, A.A., Capantini, L., Robertson, B., Grillner, S. (2015). The lamprey pallium provides a blueprint of the mammalian motor projections from cortex. Curr Biol. 25:413–423. *Co-first authors.
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II. Suryanarayana, S.M., Robertson, B., Wallén.P., Grillner, S. (2017). The lamprey pallium provides a blueprint of the mammalian layered cortex. Curr Biol. 27: 3264-3277.
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III. Suryanarayana, S.M., Pérez-Fernández, J., Robertson, B., Grillner, S. The evolutionary origin of visual and somatosensory representation in the cortici of vertebrates. [Manuscript]
IV. Pérez-Fernández, J., Stephenson-Jones, M., Suryanarayana, S.M., Robertson, B., Grillner, S. (2014). Evolutionarily conserved organization of the dopaminergic system in lamprey: SNc/VTA afferent and efferent connectivity and D2 receptor expression. J Comp Neurol. 522:3775–3794.
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I. Ocana, F.M*., Suryanarayana, S.M*., Saitoh, K., Kardamakis, A.A., Capantini, L., Robertson, B., Grillner, S. (2015). The lamprey pallium provides a blueprint of the mammalian motor projections from cortex. Curr Biol. 25:413–423. *Co-first authors.
Fulltext (DOI)
Pubmed
View record in Web of Science®
II. Suryanarayana, S.M., Robertson, B., Wallén.P., Grillner, S. (2017). The lamprey pallium provides a blueprint of the mammalian layered cortex. Curr Biol. 27: 3264-3277.
Fulltext (DOI)
Pubmed
View record in Web of Science®
III. Suryanarayana, S.M., Pérez-Fernández, J., Robertson, B., Grillner, S. The evolutionary origin of visual and somatosensory representation in the cortici of vertebrates. [Manuscript]
IV. Pérez-Fernández, J., Stephenson-Jones, M., Suryanarayana, S.M., Robertson, B., Grillner, S. (2014). Evolutionarily conserved organization of the dopaminergic system in lamprey: SNc/VTA afferent and efferent connectivity and D2 receptor expression. J Comp Neurol. 522:3775–3794.
Fulltext (DOI)
Pubmed
View record in Web of Science®
Institution: Karolinska Institutet
Supervisor: Grillner, Sten
Co-supervisor: Robertson, Brita; Wallén, Peter; Hellgren Kotaleski, Jeanette
Issue date: 2019-11-07
Rights:
Publication year: 2019
ISBN: 978-91-7831-632-8
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