TL;DR – Evolution of Human Emotion

Reading through references and reference lists for a previous post, I came across a short (open access) review article from Professor Joseph LeDoux entitled Evolution of Human Emotion: A view through fear. LeDoux deconstructs the notion of a ‘limbic system’ as the emotional centre of the brain, and even as a discrete ‘system’ at all. Here are the salient points:

The history of the limbic system 

Neuroscientist Paul MacLean (1913 – 2007) coined the phrase limbic system in 1952; part of his evolutionary theory of brain development (the Triune Brain) suggesting a three layer human brain consisting of three, evolutionary conserved, ‘layers’:

– the ‘reptilian brain’ – the basal ganglia and brainstem, responsible for instinctive behaviours

– the ‘paleomammalian brain’ – the limbic system, the emotional centre of the brain

– the ‘neomammalian brain’ – the neocortex, the source of high level cognition

The limbic system was said to include the amygdala, hippocampus, hypothalamus, septum and other subcortical nuclei.

MacLean suggested that in humans, the limbic system had decreased in size to make way for a larger cortex, giving humans greater control over ‘base’ emotions.

Four reasons the limbic system is not a thing

According to LeDoux, the concept of a limbic system persists in some scientific circles*, as well as many lay accounts of the brain but is an unacceptable notion (as an aside, I’ve heard patients and therapists talk about “the reptilian brain or the critter brain” being responsible for various distinct functions, often with a distinct sense of it being ‘other’, rather than ‘self’).

LeDoux outlines four key points:

1. The neocortex and limbic structures are not unique mammalian brain specialisations. The separation of human brains into paleomammalian and neomammalian systems is not justifiable:

“The classic notion that the evolution of mammals led to radical changes such that new forebrain structures (limbic system and neocortex) were added has not held up”

2. MacLean suggested that the neuronal architecture of the limbic system was ill-suited to cognitive processes,  but the hippocampus – MacLeans “centrepiece” of the limbic system and key structure for emotional functions, is now considered to be essential for a range of higher cognitive functions.

3. Efforts to define ‘the limbic system’ have failed – modern anatomical techniques have demonstrated that structures in the limbic system have widespread connections to the neocortex and the spinal cord. The limbic system is rather a diverse set of structures with diverse connections throughout the brain.

“Connectivity with old cortex is a flawed criterion if old cortex is itself an unjustified notion.”

4. There is just no evidence that the limbic system, however defined, is the key, integrated system that mediates emotion:

“Indeed, relatively few limbic areas have been shown to contribute to emotional functions.”

The amygdala

LeDoux has a theory on why the idea of the limbic system as the brain’s emotional system has persisted for so long – the amygdala. Classically subsumed into the limbic system, the amygdala has been consistently implicated in emotional behaviour, leading to a ‘guilt by association’ for the (idea of the) limbic system as a whole.

LeDoux reviews the history of research concerning the amygdala, noting that it has mainly been focussed on fear and avoidance conditioning.

Importantly, LeDoux also highlights the fact that the amygdala has also been associated with a range of other emotional states, the processing of rewards, motivation and reinforcement of behaviour, learning, drug addiction, and aggressive, maternal, sexual, eating and drinking behaviour.

In conclusion

In a nutshell:

“The idea that mammalian evolution is characterized by the addition [to a ‘reptilian brain’] of a limbic system (devoted to emotion) and a neocortex (devoted to cognition) is flawed”

“Modern efforts to understand the brain mechanisms of emotion have made more progress by focusing on specific emotion systems, like the fear or defense system, rather than on efforts to find a single brain system devoted to emotion”

“Efforts to use scientific methods identify [sic] circuits in animals that might correspond to circuits in the human brain that are responsible for conscious feelings are not likely to succeed since we have no way of scientifically measuring feelings in animals.”

“Conscious feelings are an important topic, but one that is best pursued through studies of humans.”

It might be time to get out the old neuroanatomy textbooks and rip out the chapter on the ‘limbic system’. While we’re at it we could also replace simplistic, erroneous concepts like ‘reptilian brains’ or ‘critter brains’ with an updated recognition of the magnificent, dynamic complexity of our human brains. Who knows, this might even lead further to an appreciation of embodied brains, embedded in an enacted world with ‘mind’ extended and distributed outside the magical membrane of the skull!

-Tim Cocks

* As an interesting example, this paper on ‘innate limbic system circuitry’ cites LeDoux’s limbic system deconstruction paper perhaps either in defiance or ignorance of his position.

NOIgroup is teaching around Australia in 2016 – supercharged 3 day combined EP and GMI courses in Townsville and Noosa, PPR in Adelaide, and details to come on our teaching visits to The Australian Institute of Sport in the Australian Capital Territory, and Perth