History Module: The Triune Brain/Limbic System Model—What To Keep, What To Discard

The triune-brain model was introduced in the 1960s by American physician and neuroscientist Paul D. MacLean. This model, including the idea of the limbic system as one of the brain’s three main components, has gained such wide acceptance that both “triune brain” and “limbic system” have become common parlance in pop psychology. But over the years since MacLean introduced these concepts, a number of studies have been published that cast doubt on certain aspects of them. The time has come to revisit these concepts and dust them off a bit.

Why has this model been so successful?

One reason that the triune-brain model has so captured people’s imaginations is that it is so simple and meshes so perfectly with a very old conception of the three basic elements of human nature: will, emotion, and rationality (or, more colorfully, “gut, heart, and head”). This model thus posits three brains that emerged in succession in the course of evolution and are now nested one inside the other in the modern human brain: a “reptilian brain” in charge of survival functions, a “limbic brain” in charge of emotions, and the neocortex, in charge of abstract, rational thinking.

Another reason for this model’s success, some think, is that it seems to provide anatomical foundations for the psychoanalytic concepts of Freud. According to MacLean, the three parts of the brain communicate poorly with one another; the neocortex dominates (or, as Freud would put it, “represses”) the two others. Moreover, this idea of the brain as being organized into three hierarchical layers, from the oldest to the most recent, also fits neatly into Darwinian theory. Lastly, there have never really been any other models of the brain that were so simple to understand and so easy to teach.

Limbic system definition vague

The term “limbic” was introduced in the 19th century by Paul Broca, when he used the expression “great limbic lobe” to designate an arc-shaped region of the cortex, consisting of the inward-folding edges of the gyri (the Latin word limbus means border or edge) and other brain structures associated with them. Later, in 1937, James Papez described a circuit that he believed was involved in the forming of emotions. The Papez circuit, also called the hippocampal/mammillothalamic tract, connects several structures belonging to what has since come to be known as the limbic system.

But as neuroanatomist Helmut Wicht has said, if you put any group of serious neuroanatomists into a room and ask them to define precisely which brain structures make up the limbic system, the discussion rapidly degenerates into a brawl. So the first major problem with the triune-brain model is that there is no consensus on the definition of one of the three main layers that it posits: the limbic system. In fact, if there is one thing on which neuroanatomists agree, it is that the idea of the limbic system as an anatomical theory of the “emotional brain” must be abandoned.

Indeed, electrophysiological studies of the structures supposedly belonging to the limbic system have assigned them functions other than the processing of emotions. For one example, some cells in all of the relays of the Papez circuit (a sub-set of the limbic system) have been found to react not to emotional stimuli, but to the head’s physical orientation relative to the body’s axis. For another, in rats, lesions in the mammillary nuclei, or in their connections to the thalamus and the cortex, disrupt memorization of spatial information about the environment. True, the Papez circuit is absent in amphibians and fish, and rudimentary in reptiles. It really appeared only with the emergence of the first mammals, but it seems to be associated more with their motor adaptation to their environment than to their emotions.

In light of these more recent findings, the association of the limbic system with the emotional brain in MacLean’s model is problematic, to say the least.

Problems with the idea of the “reptilian brain”

MacLean’s concept of the “reptilian brain” also has its share of problems. First of all, we now know that the brains of current reptiles contain a cortex organized into layers, just like the brains of mammals. Reptiles were long thought to have a very small cortex and a large striatum (a structure more primitive than the cortex), but this idea was based on an erroneous anatomical interpretation that has since been corrected. The error was that the dorsal ventricular ridge in reptiles—a mass of neurons in their anterior brain—was thought to be analogous to the striatum in mammals, which lies in a similar position. And because the mammalian striatum is involved in executing movements in potential reward situations, a primitive, “reptilian” role was erroneously ascribed to this dorsal ventricular ridge. But subsequently, neurochemical data and the nature of this structure’s connections have shown that it is actually part of the reptile’s cortex.

Now that we know that the brains of current reptiles have such a well developed cortex, it is hard to speak in terms of a “reptilian brain” whose functions are purely visceral. And equally hard to sustain MacLean’s theory that the human brain has been built up in successive layers, the oldest of which resembles the brain of current reptiles.

Today’s mammals and reptiles do indeed have a common, “reptilian” ancestor, but we know almost nothing about the structure of its brain. It was probably simpler, somewhat like an amphibian brain today. From this common ancestor, the brains of reptiles and mammals took divergent paths of differentiation. This means that the cortex of current mammals is not “more recent” than that of current reptiles; the two evolved according to the differing constraints to which they were subjected, thus resulting in the two different forms of cortex that we see in mammals and reptiles today.

No strict hierarchy

One final problem with the triune-brain model is that it treats the brain as if it were organized along strict hierarchical lines. Just because the cerebral cortex is where conscious thought takes place does not mean that it sits at the top of a pyramid and controls all the lower levels of the brain. On the contrary, some deeper structures in the brain (the brainstem in particular) exercise significant, continuous control over activity in the cortex—for example, by modifying the synchronization of its neurons according to whether the individual is asleep or awake.

What we can keep from this model

If, as the statistician George E.P. Box wrote, “essentially, all models are wrong, but some are useful”, then is there anything useful that we can retain from MacLean’s triune-brain model?

First, we can accept a few general ideas—for example, that some structures in our brains are older than others, from an evolutionary standpoint, and that our emotions involve some relatively primitive brain circuits that have been preserved over the course of mammalian evolution. The fear circuit and the pleasure circuit, for instance, are specific neuronal circuits that form what might best be called not our “emotional brain” but rather our “emotional neural networks”.

In short, if we want to continue associating the term “limbic system” with the emotions, then we need to redefine this term so that it includes these circuits specific to each emotion. The switches in these circuits consist of structures such as the amygdala, the nucleus accumbens, the hippocampus, the hypothalamus, the thalamus, and certain areas of the prefrontal cortex and the temporal cortex. And no doubt other structures are involved that remain to be discovered.