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Cited by 196Neurogenesis and neuroplasticity mechanismsDevelopmental Biology and Gene RegulationMemory and Neural Mechanisms

Thoughts on the development, structure and evolution of the mammalian and avian telencephalic pallium

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Puelles, Luis·2001·Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences
DOI 10.1098/rstb.2001.0973
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Abstract

Various lines of evidence suggest that the development and evolution of the mammalian isocortex cannot be easily explained without an understanding of correlative changes in surrounding areas of the telencephalic pallium and subpallium. These are close neighbours in a common morphogenetic field and are postulated as sources of some cortical neuron types (and even of whole cortical areas). There is equal need to explain relevant developmental evolutionary changes in the dorsal thalamus, the major source of afferent inputs to the telencephalon (to both the pallium and subpallium). The mammalian isocortex evolved within an initially small dorsal part of the pallium of vertebrates, surrounded by other pallial parts, including some with a non–cortical, nuclear structure. Nuclear pallial elements are markedly voluminous in reptiles and birds, where they build the dorsal ventricular ridge, or hypopallium, which has been recently divided molecularly and structurally into a lateral pallium and a ventral pallium. Afferent pallial connections are often simplified as consisting of thalamic fibres that project either to focal cell aggregates in the ventral pallium (predominant in reptiles and birds) or to corticoid areas in the dorsal pallium (predominant in mammals). Karten's hypothesis, put forward in 1969, on the formation of some isocortical areas postulates an embryonic translocation into the nascent isocortex of the ventropallial thalamorecipient foci and respective downstream ventropallial target populations, as specific layer IV, layers II– III, or layers V–VI neuron populations. This view is considered critically in the light of various recent data, contrasting with the alternative possibility of a parallel, separate evolution of the different pallial parts. The new scenario reveals as well a separately evolving tiered structure of the dorsal thalamus, some of whose parts receive input from midbrain sensory centres (collothalamic nuclei), whereas other parts receive oligosynaptic ‘lemniscal’ connections bypassing the midbrain (lemnothalamic nuclei). An ampler look into known hodological patterns from this viewpoint suggests that ancient collothalamic pathways, which target ventropallial foci, are largely conserved in mammals, while some emergent cortical connections can be established by means of new collaterals in some of these pathways. The lemnothalamic pathways, which typically target ancestrally the dorsopallial isocortex, show parallel increments of relative size and structural diversification of both the thalamic cell populations and the cortical recipient areas. The evolving lemnothalamic pathways may interact developmentally with collothalamic corticopetal collaterals in the modality–specific invasion of the emergent new areas of isocortex.

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  • Phylogenetically, some of the oldest cortical regions lie on the inferior brain surface in the medial aspect of the temporal lobe (posterior piriform cortex and entorhinal cortex) or on the inferior and medial aspect of the frontal lobe near the caudal end of the olfactory sulcus (anterior piriform cortex and orbital periallocortex).

    “Phylogenetically, some of the oldest cortical regions lie on the inferior brain surface in the medial aspect of the temporal lobe (the posterior part of the piriform cortex and the entorhinal cortex, for example) or on the inferior and medial aspect of the frontal lobe near the caudal end of the olfactory sulcus (anterior piriform cortex and the orbital periallocortex) (35–37).”

    From Dynamic mapping of human cortical development during childhood through early adulthood (2004) · cites this paper as [35]

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Research works printed but not linked: 7

  1. Bayer, S. A. & Altman, J. 1991 Neocortical development . NewYork: Raven Press.
  2. Bayer, S. A. & Altman, J. 1995 Development: principles of neurogenesis, neuronal migration, and neuronal circuit formation. In The rat nervous system , 2nd edn, pp. 1079^1098. San Diego, CA: Academic Press.
  3. Guille ¨ n, M. 1991 Estructura del epita ¨ lamo y complejo superior del ta ¨ lamo dorsal en aves: estudio embriolo ¨ gico y posibles homologias con mam|¨feros. PhD thesis, University of Murcia, Spain.
  4. Mart|¨ nez-de-la-T orre, M. 1985 Estructura del mesence ¨ falo y dience ¨ falo en aves y reptiles: aportaciones a una s|¨ ntesis en la bu ¨ squeda de homologias. PhD thesis, University of Murcia, Spain.
  5. ten Donkelaar, H. J. 1998 Reptiles. In The central nervous system of vertebrates , vol. 2 (ed. R. Nieuwenhuys, H. J. ten Donkelaar & C. Nicholson), pp. 1315^1524. Berlin: Springer.
  6. Ulinsky, P. S. 1983 Dorsal ventricular ridge . New York: Wiley.
  7. Valverde, F. 1985 The organizing principles of the primary visual cortex of the monkey. In Cerebral cortex , Vol. 3. Visual cortex (ed. A. Peters & E. G. Jones), pp. 207^257. New Y ork: Plenum.

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Authors
Puelles, L.
Affiliations
Universidad de Murcia (ES)
Corresponding author
Puelles, Luis
ORCID
Puelles, Luis
Venue
Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences
Publisher
The Royal Society
Published
2001-10-29
Volume
356
Issue
1414
Pages
1583-1598
ISSN
  • 0962-8436 (ISSN-L)
  • 1471-2970
DOI
10.1098/rstb.2001.0973
OpenAlex
W2119464603
Cited by
196
References
98
Citations by year
2026: 8 · 2025: 6 · 2024: 5 · 2023: 9 · 2022: 7 · 2021: 8 · 2020: 10 · 2019: 9 · 2018: 4 · 2017: 10 · 2016: 6 · 2015: 9 · 2014: 7 · 2013: 7 · 2012: 5
FWCI
1.84
Type
journal article
Language
en
Open access
Licence
royalsociety.org/journals/ethics-policies/data-sharing-mining/ (tdm)
Locations
  • Philosophical Transactions of the Royal Society B Biological Sciences (publishedVersion)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (publishedVersion)
Topics
  • Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Keywords
avian pallium, subpallium, dorsal thalamus, dorsal pallium, lemniscal pathway
MeSH terms
Animals, Birds, Biological Evolution, Mammals, Telencephalon, Gene Expression Regulation, Developmental

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