The Anarchic Brain

One notion that persists in various accounts of mind and brain is the notion of an executive, a highest-level function that controls all the rest. That such a function seems necessary, that it is logical to interpret this or that brain system (e.g. the prefrontal cortex) as being the executive, this, I suggest, has more to do with a culturally driven bias toward hierarchy than with the requirements of behavioral organization, much less with the ‘natural’ and ‘obvious’ way of interpreting observations about this or that brain system.

It is just as ‘natural’ to conceive of behavioral control as anarchic and opportunistic. Moreover, the age-old struggle between passion and reason tells as that, if there IS an executive, it’s NOT reason, because reason gets constantly over-ridden by passion. No, the top-down brain is an ideological fantasy, not a behavioral necessity.

The purpose of this post is to outline a somewhat different view of these matters that David Hays and I cooked up some years ago.

Warren McCulloch’s Heterarchical Brain

But let me start with one of the grand old men of neuroscience, the late Warren McCulloch. Back in 1945 he published a paper, “A Heterarchy of Values Determined by the Topology of Nervous Nets” in which he argued for a structure in which one can have behavioral sequences and neural structures such as: A controls B, B controls C, and C controls A. If you will, rock breaks scissors, scissors cuts paper, and paper covers rock. Some years later he collaborated with W. L. Kilmer on a model of the reticular formation that embodied such a heterarchical system, “A Model of the Vertebrate Central Command System.” In this model there is no one behavioral mode that dominates all others and thus is in a position to be an executive planner. [1]

When Hays and I incorporated McCulloch’s model into our a scheme for neuro-behavioral organization (Principles and Development of Natural Intelligence), we called it the modal principle and explained it as follows:

Definition. Modal choice feeds the results of calculation back into the biological realm, activating brain regions and selecting programs of operation which commit the organism to an interpretation of its world.

The concept of modal control has been explicated by Kilmer, McCulloch & Blum (1969) in an account of the reticular formation. They argue that animals must always be in one of several mutually exclusive modes of behavior and that the reticular formation, with its extensive afferent and efferent connections to the rest of the nervous system, is the obvious structure for implementing that commitment. The reticular formation facilitates activity in those brain regions which are most important for the current mode (see Fig. 1), while the actual behaviour of the organism when it is in the mode will be regulated by other brain centres and systems.

Kilmer et al. list 15 different modes, including, for example, sleeping, eating, fighting, hunting and grooming (see also MacLean, 1978). We are not interested in attacking or defending this particular list; what is important is recognizing that there is some small finite list of behavioural modes.

The thing about the reticular formation is that it is all-but the most primitive structure in the brain. You may be familiar with Paul McLean’s metaphor in which a reptilian brain is overlain by an old mammalian brain which is in turn overlain by the new mammalian brain. Well the reticular formation is, in effect, the chordate (worm) core of the reptilian brain. It is the oldest of the old.

It the brain has a behavioral ‘top’, it’s not at the phylogenetic, physiological or anatomical top, it’s at the bottom. The neocortex IS NOT in control; the prefrontal cortex does not rule the roost. To the extent that it makes sense to say that the roost is ruled, it’s ruled from the bottom. Hence passion can trump reason in a heartbeat.

Cortical Quadrants: Truth, Love, Beauty, and Justice

McCulloch’s account of the reticular formation is enough to defeat any proposal of top-down control, but one can say more. Back in the 1960s some clever neurosurgeons separated the cerebral hemispheres of patients with debilitating and otherwise untreatable epileptic seizures. They discovered, much to their surprise, that the two hemispheres could operate independently of one another and without the other’s knowledge. It was almost as though two persons existed in one brain. Further, the two hemispheres seemed to have rather different behavioral capacities, the left being analytical and propositional while the right was more holistic and physiognomic.

Thus began a seemingly endless parade of books and articles on the split brain. A parade that glossed over the equally important distinction between front and back, where the front half of the brain is devoted to motor activity while the back half is devoted to sensory. Working with neuroscientists A. R. Luria and Karl Pribram, Roman Jakobson concluded that the front of the brain regulated combinatorial or syntagmatic processes while the real regulated selectional or paradigmatic processes.[2]

Thus we arrive at this crude picture of the four cortical quadrants:

Left Front: analytic and propositional, combinatorial and syntagmatic

Left Rear: analytic and propositional, selectional and paradigmatic

Right Front: holistic and physiognomic, combinatorial and syntagmatic

Right Front: holistic and physiognomic, selectional and paradigmatic

As a short-hand way of talking about the quadrants Hays and I decided that the left front quadrant regulated goals for Truth, the left rear governed Justice, the right front bestowed Love, while the right rear sought Beauty. We came to think of truth, love, beauty and justice as the highest goals built-in to the nervous system.[3]

The names aren’t so important, what’s important is that there are four cortical quadrants, they have different behavioral and conceptual properties, and no one of them ‘trumps’ the others. Nor is there some other yet higher structure controlling them. The brain has four tops.

And a bottom, the reticular activating system, that trumps them all.

Who Rules the Roost?

The answer, it would seem, is nobody. The brain is run by committee. That makes sense, given that it is a network consisting of thousands upon millions of neurons ultimately connected to two worlds, the external world and the body’s interior milieu. And that its structures and processes have evolved over hundreds of millions of years. It’s a grab-bag of circuits and components.

Beyond this, I remind you that humans have very rich cultures. I suggest that this open-ended Heterarchical structure is radically open to cultural ‘shaping’. Different cultures assign different priorities to truth, love, beauty, and justice and deal with the pesky squirmy inner worm in different ways.

The mystery, of course, is that culture doesn’t do this from ‘above’ or ‘outside.’ Culture does this within, for there’s nowhere else it could be. And it does is collectively.

Spooky.

* * * * *

[1] Warren S. McCulloch, “A Heterarchy of Values Determined by the Topology of Nervous Nets”. Reprinted in McCulloch, Embodiments of Mind. MIT Press, 1965, pp. 40-45.

W. L. Kilmer, W. S. McCulloch, and J. Blum, “A Model of the Vertebrate Central Command System”. International Journal of Man-Machine Studies, vol. 1, 1969, pp. 279-309.

I’ve done a number of blog posts on behavioral mode.

[2] Roman Jakobson, Studies on Child Language and Aphasia. Mouton, 1971.

Karl Pribram, Languages of the Brain. Prentice-Hall, 1971, pp. 357 ff.

[3] We never published a detailed account of this scheme. Hays published the barest sketch as endnote 14 to “The Evolution of Expressive Culture”, Journal of Social and Evolutionary Systems 15(2): 187-215, 1993. I elaborate on that scheme primarily in endnote 3, but also endnote 11 and section 6.3 of “Culture as an Evolutionary Arena”, Journal of Social and Evolutionary Systems 19(4): 321-362, 1996.