Triune brain

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The triune brain is a model of the evolution of the vertebrate forebrain and behavior were proposed by the American physician and neuroscientist Paul D. MacLean. MacLean originally formulated his model in the 1960s and propounded it at length in his 1990 book The Triune Brain in Evolution.[1] The triune brain consists of the reptilian complex, the paleomammalian complex (limbic system), and the neomammalian complex (neocortex), viewed as structures sequentially added to the forebrain in the course of evolution. However, this hypothesis is no longer espoused by the majority of comparative neuroscientists in the post-2000 era.

The triune brain hypothesis became familiar to a broad popular audience through Carl Sagan's Pulitzer prize winning 1977 book The Dragons of Eden. The theory has been embraced by some psychiatrists and at least one leading affective neuroscience researcher.[2]

Reptilian complex[edit]

The reptilian complex, also known as the R-complex or "reptilian brain" was the name MacLean gave to the basal ganglia, structures derived from the floor of the forebrain during development. The term derives from the fact that comparative neuroanatomists once believed that the forebrains of reptiles and birds were dominated by these structures. MacLean proposed that the reptilian complex was responsible for species-typical instinctual behaviors involved in aggression, dominance, territoriality, and ritual displays.

Paleomammalian complex[edit]

The paleomammalian brain consists of the septum, amygdalae, hypothalamus, hippocampal complex, and cingulate cortex. MacLean first introduced the term "limbic system" to refer to this set of interconnected brain structures in a paper in 1952. MacLean's recognition of the limbic system as a major functional system in the brain was not widely accepted among neuroscientists, and is generally regarded as his most important contribution to the field. MacLean maintained that the structures of the limbic system arose early in mammalian evolution (hence "paleomammalian") and were responsible for the motivation and emotion involved in feeding, reproductive behavior, and parental behavior.

Neomammalian complex[edit]

The neomammalian complex consists of the cerebral neocortex, a structure found uniquely in higher mammals, specifically humans. MacLean regarded its addition as the most recent step in the evolution of the mammalian brain, conferring the ability for language, abstraction, planning, and perception.

Status of the model[edit]

MacLean originally formulated the triune brain hypothesis in the 1960s, drawing on comparative neuroanatomical work done by Ludwig Edinger, Elizabeth C. Crosby and C. J. Herrick early in the twentieth century.[3][4] The 1980s saw a rebirth of interest in comparative neuroanatomy, motivated in part by the availability of a variety of new neuroanatomical techniques for charting the circuitry of animal brains. Subsequent findings have refined the traditional neuroanatomical ideas upon which MacLean based his hypothesis.

For example, the basal ganglia (structures derived from the floor of the forebrain and making up MacLean's reptilian complex) were shown to take up a much smaller portion of the forebrains of reptiles and birds (together called sauropsids) than previously supposed, and to exist in amphibians and fish as well as mammals and sauropsids. Because the basal ganglia are found in the forebrains of all modern vertebrates, they most likely date to the common evolutionary ancestor of the vertebrates, more than 500 million years ago, rather than to the origin of reptiles.

Some recent behavioral studies do not support the traditional view of sauropsid behavior as stereotyped and ritualistic (as in MacLean's reptilian complex). Birds have been shown to possess highly sophisticated cognitive abilities, such as the toolmaking of the New Caledonian crow and the language-like categorization abilities of the African grey parrot.[5] Structures of the limbic system, which MacLean proposed arose in early mammals, have now been shown to exist across a range of modern vertebrates. The "paleomammalian" trait of parental care of offspring is widespread in birds and occurs in some fishes as well. Thus, like the basal ganglia, the evolution of these systems presumably date to a common vertebrate ancestor.[4][6]

Finally, recent studies based on paleontological data or comparative anatomical evidence strongly suggest that the neocortex was already present in the earliest emerging mammals.[4] In addition, although non-mammals do not have a neocortex in the true sense (that is, a structure comprising part of the forebrain roof, or pallium, consisting of six characteristic layers of neurons), they possess pallial regions, and some parts of the pallium are considered homologous to the mammalian neocortex. While these areas lack the characteristic six neocortical layers, birds and reptiles generally possess three layers in the dorsal pallium (the homolog of the mammalian neocortex).[4][6] The telencephalon of birds and mammals makes neuroanatomical connections with other telecencephalic structures[4] like those made by neocortex. It mediates similar functions such as perception, learning and memory, decision making, motor control, conceptual thinking, and tool use.

Lay interest[edit]

The triune model of the mammalian brain is seen as an oversimplified organizing theme by some in the field of comparative neuroscience[7] It continues to hold public interest because of its simplicity. While technically inaccurate as an explanation for brain activity, it remains one of very few approximations of the truth we have to work with: the "neocortex" represents that cluster of brain structures involved in advanced cognition, including planning, modeling and simulation; the "limbic brain" refers to those brain structures, wherever located, associated with social and nurturing behaviors, mutual reciprocity, and other behaviors and affects that arose during the age of the mammals; and the "reptilian brain" refers to those brain structures related to territoriality, ritual behavior and other "reptile" behaviors. The broad explanatory value makes this approximation very engaging and is a useful level of complexity for high school students to begin engaging with brain research.

Howard Bloom, in his book The Lucifer Principle, references the concept of the triune brain in his explanations of certain aspects of human behavior. Arthur Koestler made MacLean's concept of the triune brain the centerpiece of much of his later work, notably The Ghost in the Machine. English novelist Julian Barnes quotes MacLean on the triune brain in the foreword to his 1982 novel Before She Met Me.

References[edit]

  1. ^ Kazlev, et al., M. Alan (2003-10-19). "The Triune Brain.". KHEPER. Retrieved 2007-05-25. 
  2. ^ Panksepp, J. (2003). Foreword to Cory, G. and Gardner, R. (2002) The Evolutionary Neuroethology of Paul MacLean: Convergences and Frontiers. ISBN 978-0275972196
  3. ^ Reiner, A. (1990). "An Explanation of Behavior". Science 250 (4978): 303–305. doi:10.1126/science.250.4978.303-a. PMID 17797318. 
  4. ^ a b c d e Striedter, G. F. (2005) Principles of Brain Evolution. Sinauer Associates.
  5. ^ Patton, Paul (December 2008). "One World, Many Minds: Intelligence in the Animal Kingdom". Scientific American. Retrieved 29 December 2008. 
  6. ^ a b Butler, A. B. and Hodos, W. Comparative Vertebrate Neuroanatomy: Evolution and Adaptation, Wiley
  7. ^ Smith CU., 2010, The triune brain in antiquity: Plato, Aristotle, Erasistratus. Journal of the History of the Neurosciences, 19:1-14. doi:10.1080/09647040802601605

Further reading[edit]

  • Nomura, Tadashi; Kawaguchi, Masahumi; Ono, Katsuhiko; Murakami, Yasunori (2013). "Reptiles: A New Model for Brain Evo-Devo Research". Journal of Experimental Zoology Part B: Molecular and Developmental Evolution 320 (2): 57–73. doi:10.1002/jez.b.22484. PMID 23319423. 
  • The Avian Brain Nomenclature Consortium; Güntürkün, Onur; Bruce, Laura; Csillag, András; Karten, Harvey; Kuenzel, Wayne; Medina, Loreta; Paxinos, George; Perkel, David J.; Shimizu, Toru; Striedter; Wild, J. Martin; Ball, Gregory F.; Dugas-Ford, Jennifer; Durand, Sarah E.; Hough, Gerald E.; Husband, Scott; Kubikova, Lubica; Lee, Diane W.; Mello, Claudio V.; Powers; Siang, Connie; Smulders, Tom V.; Wada, Kazuhiro; White, Stephanie A.; Yamamoto, Keiko; Yu, Jing; Reiner, Anton; Butler, Ann B.; Avian Brain Nomenclature Consortium (2005). "Avian brains and a new understanding of vertebrate brain evolution". Nature reviews. Neuroscience 6 (2): 151–159. doi:10.1038/nrn1606. PMC 2507884. PMID 15685220. 
  • Gardner, Russell; Cory, Gerald A. (2002). The evolutionary neuroethology of Paul MacLean: convergences and frontiers. New York: Praeger. ISBN 0-275-97219-4. OCLC 49649452. 
  • Heimer, Lennart; Van Hoesen, Gary W.; Trimble, Michael; Zahm, Daniel S. (2008). "The Triune Brain Concept and the Controversy Surrounding It". Anatomy of neuropsychology: The new anatomy of the basal forebrain and its implications for neuropsychiatric illness. Amsterdam; Boston: Academic Press-Elsevier. pp. 15–16, 19. ISBN 978-0-12-374239-1. OCLC 427506175. 
  • Kral, V. A.; MacLean, Paul D. (1973). A Triune concept of the brain and behaviour, by Paul D. MacLean. Including Psychology of memory, and Sleep and dreaming; papers presented at Queen's University, Kingston, Ontario, February 1969, by V. A. Kral [et al. Toronto]: Published for the Ontario Mental Health Foundation by Univ. of Toronto Press. ISBN 0-8020-3299-0. OCLC 704665. 
  • MacLean, PD (1985). "Brain evolution relating to family, play, and the separation call". Archives of general psychiatry 42 (4): 405–17. doi:10.1001/archpsyc.1985.01790270095011. PMID 3977559. 
  • MacLean, Paul D. (1990). The triune brain in evolution: role in paleocerebral functions. New York: Plenum Press. ISBN 0-306-43168-8. OCLC 20295730.