The “reptilian” / triune brain: The origins of a misguided idea

The misguided idea of the “reptilian brain”. Figure from the excellent review by Ann Butler. Butler A B (2009). Triune Brain Concept: A Comparative Evolutionary Perspective. In: Squire LR (ed.) Encyclopedia of Neuroscience, volume 9, pp. 1185-1193. Oxford: Academic Press.

One of the presentations at the 1881 International Medical Congress in London was by Friedrich Goltz, a professor of physiology at the University of Strasburg. Like several of his contemporaries, Goltz was interested in the localization of function in the brain. He not only published several influential papers on the problem, but attracted widespread attention by exhibiting dogs with brain lesions at meetings throughout Europe. His presentations were quite a spectacle. He would take the lectern and bring a dog with him to demonstrate an impaired or spared behavior that he wanted to discuss. Or, he would open his suitcase and produce the skull of a dog with the remnants of its brain. In some cases, a separate panel of internationally acclaimed scientists would even evaluate the lesion and report their assessment to the scientific community.

In some of his studies, Goltz would remove the entire cortical surface of a dog’s brain, and let the animal recover. The now decorticated animal would survive, though it would generally not initiate action and remain still. Goltz showed that animals with an excised cortex still exhibited uncontrolled “rage” reactions, leading to the conclusion that the territory is not necessary for the production of emotional expressions. But if the cortex wasn’t needed, the implication was that subcortical areas were involved. That emotion was a subcortical affair was entirely consistent with nineteenth century thinking.

Victorian England and the beast within

In the conclusion of The Descent of Man, Charles Darwin wrote in 1871 that “the indelible stamp of his lowly origin” could still be discerned in the human mind, with the implied consequence that it was necessary to suppress the “beast within” – at least at times. This notion was hardly original, of course, and in the Western world can be traced back to at least ancient Greece. At Darwin’s time, with emotion being considered primitive and reason the more advanced faculty, “true intelligence” was viewed as residing in cortical areas, most notably in the frontal lobe, while emotion was viewed as residing in the basement, the lowly brainstem.

The decades following the publication of Darwin’s Origin of Species (in 1859) were a time of much theorizing not only in biology but in the social sciences, too. Herbert Spencer and others applied key concepts of biological evolutionary theory to social issues, including culture and ethics. Hierarchy was at the core of this way of thinking. For the survival of evolved societies, it was necessary to legitimize a hierarchical governing structure, as well as a sense of self-control at the level of the individual – it was argued[1]. These ideas, in turn, had a deep impact on neurology, the medical specialization characterizes the consequences of brain damage on survival and behavior. John Hughlings Jackson, to this day the most influential English neurologist, embraced a hierarchical view of brain organization rooted in a logic of evolution as a process of the gradual accrual of more complex structures atop more primitive ones. What’s more, “higher” centers in the cortex bear down on “lower” centers underneath, and any release from this control could make even the most civilized human act more like his primitive ancestors[2]. This stratified scheme was also enshrined in Sigmund Freud’s framework of the id (the lower level) and the super-ego (the higher level). (Freud also speculated that the ego played an in-between role between the other two.) Interestingly, Freud was initially trained as a clinical neurologist and was a great admirer of Jackson’s work.

Against this backdrop, it’s not surprising that brain scientists would search for the neural basis of emotion in subcortical territories, while viewing “rational thinking” as the province of the cerebral cortex, especially the frontal lobe.

The “reptilian” brain

In 1896 the German anatomist Ludwig Edinger published The Anatomy of the Central Nervous System of Man and other Vertebrates. The book, which established Edinger’s reputation as the founder of comparative neuroanatomy, described the evolution of the forebrain as a sequence of additions, each of which establishing new brain parts that introduced new functions.

Edinger viewed the forebrain as containing an “old encephalon” found in all vertebrates. On top of the old encephalon, there was the “new encephalon,” a sector only more prominent in mammals. In one of the most memorable passages of his treatise, Edinger illustrates his concept by asking the reader to imagine precisely inserting a reptilian brain into that of a marsupial (a “simple” mammal). When he superimposed them, the difference between the two was his new encephalon. He then ventures that, in the brain of the cat, the old encephalon “persists unchanged underneath the very important” new encephalon[3]. Put differently, the part that was present before is left unaltered. Based on his coarse analysis of morphological features, his suggestion was reasonable. But to a substantial degree, his ideas were very much in line with the notion of brain evolution as progress toward the human brain – à la old Aristotle and the scala naturae. Given the comprehensive scope of Endinger’s analysis across vertebrates, his views had a lasting impact and shaped the course of research for the subsequent decades.

More than a century later, knowledge about the brains of vertebrates has expanded by leaps and bounds. Yet, old thinking dies hard. Antiquated views of brain evolution continue to influence, if only implicitly, neuroscience. As an example, bear in mind that most frameworks of brain organization are heavily centered on the cortex. These descriptions view “newer” cortex as controlling subcortical regions, which are assumed to be (relatively) unchanged throughout eons of evolution. Modern research on brain anatomy from a comparative viewpoint indicates, in contrast, that brain evolution is better understood in terms of the reorganization of large-scale connectional systems (Figure 2). These ideas are developed extensively in [4].

Figure 2. The basic architecture of the brain is shared across all vertebrates. Extensive anatomical connectivity between sectors of the brain is observed in birds, reptiles, and mammals. The “pallium” corresponds to “cortex” in mammals. From: Pessoa, L., Medina, L., Hof, P. R., & Desfilis, E. (2019). Neural architecture of the vertebrate brain: Implications for the interaction between emotion and cognition. Neuroscience & Biobehavioral Reviews, 107, 296-312.

[1] Edinger (1910, p. 446).

[2] See Parvizi (2009) for an accessible discussion.

[3] For discussion, see Finger (1994, p. 271).

[4] Pessoa, L., Medina, L., Hof, P. R., & Desfilis, E. (2019). Neural architecture of the vertebrate brain: Implications for the interaction between emotion and cognition. Neuroscience & Biobehavioral Reviews, 107, 296-312.

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