Review
Neurotransmitter organization and connections of turtle cortex: implications for the evolution of mammalian isocortex

https://doi.org/10.1016/0300-9629(93)90149-XGet rights and content

Abstract

Telencephalic cortex in turtles is a simple three layered-structure. The dorsal most part of this structure is thought to resemble the reptilian forerunner of at least parts of mammalian isocortex. This dorsal part of turtle cortex contains several functionally distinct regions that show similarity in their connections and function to specific areas in mammalian isocortex. The types of neurons found in turtle dorsal cortex (as defined by their morphology and neurotransmitter content) also show great similarity to those observed in mammals, with the major exception that turtle cortex appears to lack the types of neurons found in granular and supragranular layers of mammalian isocortex. Similar results have also been observed in other living reptiles. Thus, one major step in the evolution of reptilian cortex into mammalian cortex must have been the addition of the types of neurons found in the granular and supragranular layers of mammalian isocortex. These observations for turtles also suggest that turtle cortex in particular and reptilian telencephalic cortex in general must differ functionally from mammalian isocortex with respect to those features associated with the laminar and columnar organization of isocortex. These issues are discussed in more detail below and in Reiner (1991).

References (99)

  • A Reiner et al.

    Somatostatin and neuropeptide Y are almost exclusively found in the same neurons in the telencephalon of turtles

    Brain Res.

    (1987)
  • A Reiner et al.

    Evolution of the amniote basal ganglia

    Trends Neurosci.

    (1984)
  • S.R Vincent et al.

    Coexistence of somatostatin and avian pancreatic polypeptide (APP)-like immunoreactivity in some forebrain neurons

    Neuroscience

    (1982)
  • A Weindl et al.

    Somatostatin in the brain of the turtle Testudo hermami gmelin an immunohistochemical mapping study

    Peptides

    (1984)
  • J Allman

    Evolution of Neocortex

  • C.U Ariëns Kappers et al.

    The Comparative Anatomy of the Nervous System of Vertebrates, Including Man

    (1936)
  • C.D Balaban

    Organization of thalamic afferents to anterior dorsal ventricular ridge in turtles: I. Projection of thalamic nuclei

    J. comp. Neurol.

    (1981)
  • M.G Belekhova

    Neurophysiology of the forebrain

  • M.G Blanton et al.

    Actions of acetylcholine in turtle dorsal cortex

    Soc. Neurosci. Abs.

    (1986)
  • M.G Blanton et al.

    Evidence for the inhibitory neurotransmitter γ-aminobutyric acid in aspiny and sparsely spiny nonpyramidal neurons of the turtle dorsal cortex

    J. comp. Neurol.

    (1987)
  • R.C Bohringer et al.

    The organization of the sensory and motor areas of cerebral cortex in the platypus (Omithorhynchus anatinus)

    J. comp. Neurol.

    (1977)
  • L.L Bruce et al.

    Telencephalic connections in lizards. I. Projections to cortex

    J. comp. Neurol.

    (1984)
  • L.L Bruce et al.

    Telencephalic connections in lizards. II. Projections to anterior dorsal ventricular ridge

    J. comp. Neurol.

    (1984)
  • A.B Butler

    Telencephalon of the lizard Gekko gecko (Linnaeus): Some connections of the cortex and dorsal ventricular ridge

    Brain Behav. Evol.

    (1976)
  • B.W Connors et al.

    Cellular physiology of the turtle visual cortex: distinctive properties of pyramidal and stellate neurons

    J. Neurosci.

    (1986)
  • J Cranney et al.

    The effects of core nucleus and cortical lesions in turtles on reversal and dimensional shifting

    Physiol. Psych.

    (1983)
  • R.A Dart

    The dual structure of the neopallium: its history and significance

    J. Anal. (London)

    (1934)
  • J.C Davila et al.

    Ultrastructure of the dorsal cortex of the lizard Psammodromus algirus

    J. Himforsch

    (1986)
  • J.C Davila et al.

    Distribution of neuropeptide Y (NPY) in the cerebral cortex of the lizards Psammodromus algirus] and Podarcis hispanica: Co-localization of NPY, somatostatin and GABA

    J. comp. Neurol.

    (1991)
  • I.T Diamond

    Organization of the visual cortex: comparative anatomical and behavioral studies

  • I.T Diamond et al.

    Evolution of neocortex

    Science

    (1969)
  • A Durward

    The cell masses in the forebrain of Sphenodon punctatum

    J. Anat.

    (1930)
  • S.O.E Ebbesson et al.

    The cytoarchitecture of the pallium in the tegu lizard (Tupinambis nigropunctatus)

    Brain Behav. Evol.

    (1969)
  • F.F Ebner

    A comparison of primitive forebrain organization in metatherian and eutherian mammals

    Ann. N.Y. Acad. Sci.

    (1969)
  • F.F Ebner

    The forebrain of reptiles and mammals

  • J.C Eccles

    The cerebral cortex. A theory of its operation

  • G Elliot Smith

    A preliminary note on the morphology of the corpus striatum and the origin of the neopallium

    J. Anat.

    (1919)
  • I.I Glezer et al.

    Implications of the “initial brain” concept for brain evolution in Cetacea

    Behav. Brain Sci.

    (1988)
  • W Grisham et al.

    Differential effects of medial and dorsal cortex lesions on spatial reversals in turtles (Chrysemys picta)

    Soc. Neurosci. Abs.

    (1984)
  • W Grisham et al.

    Function of the dorsal and medial cortex in learning

    Behav. Neurosci.

    (1989)
  • S Guirado et al.

    A Golgi study of the dorsal cortex in the lizard Psammodromus algirus

    J. Morphol.

    (1987)
  • W Hodos

    Some perspectives on the evolution of intelligence and the brain

  • P.V Hoogland et al.

    Efferent connections of the dorsal cortex of the lizard Gekko gecko studied with Phaseolus vulgaris—Leucoagglutinin

    J. comp. Neurol.

    (1989)
  • P.V Hoogland et al.

    Distribution of choline acetyltransferase immunoreactivity in the telencephalon of the lizard Gekko gecko

    Brain Behav. Evol.

    (1990)
  • J.A Hopson

    Paleoneurology

  • H.J Jerison

    Animal intelligence as encephalization

    Phil. Trans. R. Soc. Lond.

    (1985)
  • J.I Johnson

    Central nervous system of marsupials

  • J.P Johnston

    The cell masses in the forebrain of the turtle, Cistudo Carolina

    J. comp. Neurol.

    (1915)
  • J.P Johnston

    Evidence of a motor pallium in the forebrain of reptiles

    J comp. Neurol.

    (1916)
  • Cited by (106)

    • Variations of telencephalic development that paved the way for neocortical evolution

      2020, Progress in Neurobiology
      Citation Excerpt :

      Similar equivalence of neuronal types has also been found among pallial interneurons. Three main subtypes are identified in the pallium of mammals, chick, lizard and turtle regarding their expression of calcium-binding proteins such as somatostatin, parvalbumin or the serotonin receptor 5-HT3R (Reiner, 1993; Tosches et al., 2018; Tremblay et al., 2016). Although turtle parvalbumin type of interneurons do not express parvalbumin, transcriptomics shows that these interneurons express the whole set of markers common to mammalian parvalbumin-expressing interneurons.

    • Update on forebrain evolution: From neurogenesis to thermogenesis

      2018, Seminars in Cell and Developmental Biology
      Citation Excerpt :

      Numerous studies have noted similarities in connectivity and gene expression between the layers of the mammalian isocortex and the avian and reptilian pallia. However, these studies were limited to the analysis of few markers, leaving space to several conflicting hypotheses on neocortex evolution [30–32]. For example, recent studies have suggested the homology of mammalian layer 2/3, layer 4 and layer 5 cell types to adjacent regions in the avian telencephalon [27,31,33].

    • Comparative Biology and Species Effects on Expression of Epilepsy

      2017, Models of Seizures and Epilepsy: Second Edition
    View all citing articles on Scopus
    View full text