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On the appropriateness of Paul MacLean's “triune brain” theory

Since we are knees-deep in affective neuroscience, my first post here will be on the appropriateness of a major theory in the field – Paul MacLean's “triune brain” theory – that addresses brain evolution. I have delayed other, more pressing matters, in order to discuss this. The second post  on the evolutionary neuroscience of emotion will probably be on the influence of Darwin's The Expression of Emotions in Man and Animals on emotional research in general. I hope you few scattered readers will not give up on me at this point =)

MacLean's theory is rather simple. The observations of Papez (1937) on the brain circuits involved on emotional behaviour, which sprout from a rather heated history of debates on the brain structures involved on this, were what ignited MacLean's model. According to the “triune brain” theory (MacLean, 1970), structures found in the Papez Circuit (septo-hippocampal system, mammilary bodies of the hypothalamus, and cingulate gyrus and cortex), together with other regions of the hypothalamus, nucleus accumbens, amygdala, subiculum and orbitofrontal cortex, are responsible for emotional processing of stimuli. The two other divisions of the triune brain comprised functions of controlling stereotypical behaviors and cognitive processing. According to his model, thus, there are three main divisions of the brain:

  1. Protoreptilian brain: the fundamental axis of the nervous system, composed of spinal cord, brainstem, diencephalon and basal ganglia. Responsible for genetically-determined stereotypical behaviors.

  2. Paleomammalian brain: the limbic system, composed of hippocampus, amygdala, hypothalamus and periventricular structures. Responsible for mechanisms associated with self-awareness and awareness of internal bodily conditions.

  3. Neomammalian brain: the cerebral cortex – with special attention to the frontal cortex. Responsible for cognitive functions and the analysis of the external environment.

MacLean's theory is not only a neuroanatomical one, but also a comparative neuroanatomy theory. The title of his book, The Triune Brain in Evolution, is witness to this. His theory, though, is an early theory of brain evolution, and is based on earlier theories by Herrick (1948) and von Baer (1828). It is interesting to note that both theories that influenced MacLean are pre-synthesis theories, and, as such, rely on scala naturae-like concepts. According to MacLean, the history of brain evolution is the history of addition of structures or areas to pre-existing ones, resulting in the three divisions he proposed. However, as modern theories state, modification of existing structures, as opposed to addition of new ones, is probably a more common process in brain evolution than addition (Striedter, 2005; Butler and Hodos, 2005). True novelty in the brain is rarer in more proximate taxa, and more common in distant clades. However, the addition of structures is only one of many processes involved in novelty. Let us follow Striedter (2005) in his proposed thought experiment.

Imagine that you are comparing two sister species, A and B, and that any similarities shared between them also are found in the next more closely related species C. In that case, any character shared by species A and B would, according to cladistic methodology, be homologous between them (Striedter, 2005, p. 182).

Figure 1 presents three hypothetical species, and three traits; one of them is a novel trait. The question here is: how do you determine what was the mechanism that produced novelty in the three taxa? There are several possibilities here. The first one is called “novelty by phylogenetic conversion”, and occurs when clear one-to-one homologies can be found in species A, B and C, but one of the traits analysed (red square in figure 1A) presents so many differences from its homologues (red circles) that it should be called “new”. The second alternative is called “novelty by phylogenetic proliferation”, and occurs when species A, for example, presents more traits than species B and C (figure 1B), and that condition is derived (ie, not primitive). Proliferation can happen in two ways: phylogenetic addition (figure 1C) and phylogenetic segregation (figure 1D). Phylogenetic addition occurs when one of the extra characters cannot be homologized across species A, B, and C, but the other characters can; phylogenetic segregation occurs when two or more characters of the derived condition (taxon A) exhibit all or most of the characteristics of a single character in the primitive condition (taxa B and C). Decision between which process of proliferation occurred is done using the following rule of thumb:

If, of the two remaining characters in species A, one is far more similar than the other to the remaining characters in species B and C, then the other, nonmatching character was probably added in species A. On the other hand, if both of the remaining characters in species A are equally similar to the remaining characters in B and C, then segregation most likely occurred (Striedter, 2005, p. 185).

This last case is what Butler and Hodos (2005) call “field homology” – ie, the derivation of structures from a common morphogenetic field. If we consider field homology, however, there is a second process of addition – that of addition of a completely new morphogenetic field, probably due to duplication of genes.

How can we determine whether proliferation occurred in any of the structures of MacLean's triune brain? Let's take, for example, the septo-hippocampal system. MacLean's model predicts that this structure will be absent in sauropsidia (birds and reptiles), amphibia and fishes, and present in early mammals (or proxies for those, such as insectivores) and extant mammalian species. However, it can be demonstrated that the lateral pallium of anamniotes present field homology with the hippocampus of amniotes. This observation, alone, is not enough to repel the possibility of proliferation of hippocampal structures in the phylogenetic series; however, the fact that a clear one-to-one homologue of hippocampus exists in birds is enough to dismiss MacLean's model, at least for this character. The medial pallium of teleosts and the DVR of sauropsids was proposed as homologous to the tetrapod amygdala (Braford, 1995; Striedter, 1997; Butler, 2000); if this hypothesis is true, we have yet another structure whose evolution does not fit MacLean's model. Thus, the limbic structures that the triune brain theory predicts to be first present only in early mammals were found in nonmammalian vertebrates, dismissing in toto the model. As a side note, homologues of neocortical and dorsal thalamic nuclei were also found in nonmammals, which testifies against the hypothesis that they should be first present only in extant mammals. It should also be noted, as Butler and Hodos (2005) put it, that

MacLean's observations on the behavioral differences between mammals and nonmammals are oversimplified and ignore the elaborate social and parental behaviors of some nonmammalian vertebrates, including birds and a variety of ray-finned fishes (p. 114).

Since, as noted above, MacLean's theory was highly influenced by earlier theories of brain evolution – such as Herrick's, von Baer's and Hughlings Jackson's (1932) –, this scala naturae-like simplification is not surprising. As most early theories of brain evolution, MacLean's triune brain views the course of evolution as a progression from a simple to a complex condition. As such, homoplasy (specially parallelism and convergence) cannot enter these models, as it is not considered an important factor in evolution. The fact that independent evolution is more common than previously thought is not accomodated by scala naturae theories. “This unidimensional progression, seemingly under the direction of some imperative, is reminiscent of the now discredited, 'predetermined path' theory of apparent steady lines of 'progressive' evolution or a trend in one definite direction, referred to as orthogenesis” (Butler and Hodos, 2005, p. 116).

The “triune brain” theory is most influential in the lay press and among clinical psychologists. It had little impact on neurobiology per se, but is still defended by some researchers in the area of emotional behavior. For example, Panksepp (1998) writes:

This three-layered conceptualization helps us grasp the overall function of higher brain areas better than any other scheme yet devised. Of course, exceptions can be found to all generalizations, and it must be kept in mind that the brain is a massively interconnected organ whose every part can find an access pathway to any other part. Even though many specialists have criticized the overall accuracy of the image of a “triune brain”, the conceptualization provides a useful overview of mammalian brain organization above the lower brain stem (p. 70).

In defense of Panksepp, it must be said that he argues that the “protoreptilian brain” elaborates basic emotional variables, such as “seeking, and some aspects of fear, aggression and sexuality” (p. 70). It is probable that the ascending aminergic pathways (the serotoninergic raphe nuclei, the noradrenergic locus coeruleus and the dopaminergic mesolimbic and mesocortical pathways), as well as neuropeptide pathways – which are homologous in all vertebrates –, have a very important role in mediating emotional behavior. However, Panksepp's book concerns mammalian emotional processes, and makes little mention to nonmammals. This “mammalocentrism” biased his reading of the triune brain model.

The conceptual gains mentioned by Panksepp are overcome by other, more pressing needs. We addressed, in this post, one of those needs – viz., the need to report to evolutionary findings. The simplistic analysis of MacLean's triune brain model is not justified; at best, theories of emotional behavior should address specific circuits, or, at the extreme, “conceptual nervous system” approaches when knowledge about those circuits is not available. Scala naturae concepts such as the triune brain have proven to have little value to the pursuit of neuroscientific knowledge.

I ran out of things to write. The possible presence of a few scattered readers is rending my capability of writing any longer useless, and the wine has gone to my head. Then, go away, silly persons! That is it for today, see you in another post.


References
Braford Jr MR (1995). Comparative aspects of forebrain organization in the ray-finned fishes: Touchstones or not? Brain, Behavior and Evolution 46: 259-274. http://www.ncbi.nlm.nih.gov/sites/entrez?cmd=Retrieve&db=PubMed&list_uids=8564467&dopt=Citation

 


Butler AB (2000). Topography and topology of the teleosts telencephalon: A paradox resolved. Neuroscience Letters 293: 95-98. http://www.sciencedirect.com/science?_ob=ArticleURL&_udi=B6T0G-41C2R1D-4&_user=10&_coverDate=10%2F27%2F2000&_rdoc=1&_fmt=&_orig=search&_sort=d&view=c&_acct=C000050221&_version=1&_urlVersion=0&_userid=10&md5=e62f0e84ff33d2138f370fe382caf518


Butler AB, Hodos W (2005). Comparative Vertebrate Neuroanatomy. Evolution and Adaptation. 2a. Edição. Hoboken: John Wiley & Sons.


Herrick CJ (1948). The Brain of the Tiger Salamander. Chicago: University of Chicago Press.


MacLean P (1990). The Triune Brain in Evolution. New York: Plenum Press.


Panksepp J (1998). Affective Neuroscience: The Foundations of Human and Animal Emotions. New York: Oxford University Press.


Papez J (1937). A proposed mechanism of emotion. Journal of Neuropsychiatry and Clinical Neuroscience 7: 103-112. http://www.neuro.psychiatryonline.org/cgi/reprint/7/1/103


Striedter GF (1997). The telencephalon of tetrapods in evolution. Brain, Behavior and Evolution 49: 179-213. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&list_uids=9096908&dopt=Citation


Striedter GF (2005). Principles of Brain Evolution. Sunderland: Sinauer Associates.


von Baer KE (1828). Entwicklungsgeschichte der Thiere: Beobachtung und Refexion. Könisgbergb: Bornträger.

Tags: maclean triune brain emotion scala natur
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