Crick and Koch’s new “Framework for Consciousness”

It is not often that a top scientific journal features a lead article on consciousness, and we at SCR rejoice to see Francis Crick and Christof Koch’s commentary “A Framework for Consciousness,” featured in the February 2003 issue of Nature Neuroscience. In this article, Crick and Koch describe ten aspects of a framework that they believe offers a coherent scheme for explaining the neural correlates of consciousness (NCC) in terms of competing cellular assemblies in the brain.

Amid the welter of speculation and philosophizing about consciousness that has grown in the past 10 years, Crick and Koch have remained steadfast in their chosen experimental and theoretical approach to consciousness:

They specifically use visual consciousness in the primate.

• They acknowledge that the hardest problem of consciousness is to explain qualia, but think that it is fruitless to approach this head-on.
• They are not concerned about mechanisms that “turn on” consciousness, such as the lower brainstem (reticular activating system), but about cortical areas that underpin specific conscious experiences.
• They feel the answer lies in the detailed behavior of single neurons or small groups of neurons on very fast time scales in awake primates. In contrast, imaging methods such as fMRI are said to be too coarse in both space and time to be of much use for the problem of consciousness.

The current article presents the latest “snapshot” in the evolution of Crick and Koch’s thinking as they continue with this approach. By calling it a “framework,” Crick and Koch say they are only suggesting an approach to the problem of consciousness, one that may lead to testable hypotheses. A framework, to them is one that “sounds reasonably plausible relative to available scientific data and that turns out to be largely correct…but is unlikely to be correct in all the details.”

The key elements of the Crick and Koch framework are:

• The homunculus: By this they mean that it is useful to think of the “front” or higher/executive part of the cortex (anterior to the central sulcus) as looking at and interacting with the “back”, or sensory part.
• Zombie modes: These are response to sensory inputs that are rapid, transient, stereotyped and unconscious, and could be thought of as cortical reflexes (e.g. those associated with the dorsal or parietal visual stream), while conscious modes deal with broader, more elaborate and less stereotyped actions. Crick and Koch hypothesize that in a zombie mode, the main flow of information is feed-forward: a forward-traveling net-wave of neural activity. In the conscious mode, it seems likely that the flow is in both directions so that it resembles more of a standing net-wave.
• Coalitions of neurons: This is the key idea in the framework: that conscious experiences are sustained by shifting coalitions of neurons. The various neurons in a coalition in some sense support one another, either directly or indirectly, by increasing the activity of their fellow members. In general, at any moment, the winning coalition is somewhat sustained, and embodies what we are conscious of. Thus, a coalition could be produced by visual imagination (with one’s eyes closed), and this may be less widespread than a coalition produced by a vivid and sustained visual input from the environment. Unlike previously advanced ideas, Crick and Koch do not believe that neuronal synchrony (such as the 40 Hz hypothesis) is necessary to sustain a coalition.
• Explicit representations: Every explicit conscious representation of a particular visual scene has a group of neurons responsible for it. If they are all lost by brain damage, then the subject is unable to consciously perceive that aspect directly, as in achromatopsia (loss of color perception), prosopagnosia (loss of face recognition) or akinetopsia (loss of motion perception). Crick and Koch call such a group of neurons “a node,” that could be a part of a coalition, but cannot by itself produce consciousness. They hypothesize that the smallest useful node is a cortical column or a portion of it.
• The higher level first: Neural activity first travels rapidly and unconsciously up the sensory hierarchy to a high level, and then starts to move backward down the hierarchy so that the first stages to reach consciousness are at the higher levels (e.g. showing the gist of the scene). This activity then moves further backward to give the details of the scene.
• Driving and modulating inputs: Inputs to a cortical neuron fall roughly into two broad classes: driving and modulating inputs. Driving inputs largely contact the basal dendrites, the classical input branches of neurons, whereas modulatory inputs include back-projections and are largely to the apical dendrites. It is possible that the connections from the back of the brain to the front are largely driving, whereas the reverse pathways are largely modulatory.
• Snapshots: Crick and Koch propose that conscious awareness is a series of static snapshots of shifting neuronal coalitions. Dynamic aspects, such as motion, are represented as the firing rate of the neurons in the coalitions themselves, just as it is possible for a static image of say, a falling person, to suggest motion as shown in the picture. The coalitions need to be above a certain threshold to be conscious, but the nature of that threshold is completely unknown. We do not even know whether it is quantitative (firing rates, firing in bursts) or qualitative (pyramidal cells projecting to the front of the brain)..
• Attention and binding: Attention can be volitional and top-down (back-projections from the front of the brain, or from the intra-laminar nucleus of the thalamus) or saliency controlled and bottom-up (layer 5 neurons projecting to thalamus). In either case, attention can bias competition among developing coalitions. The idea of coalitions effectively finesses the “binding problem”—how different attributes of the same object are brought together—by stating that the ‘binding’ of the features of a single object/event is simply the co-membership in a particular coalition
• Styles of firing: Synchronized firing may help a nascent coalition in its competition with other (nascent) coalitions. Such firing may not be needed once a successful coalition has reached consciousness
• Penumbra and Meaning: The firing of NCC neurons will influence many neurons that are not part of the NCC. Crick and Koch call this sphere of influence the ‘penumbra’. This penumbra includes past associations, expected consequences, possible plans for movement associated with NCC neurons, and other aspects that serve to give meaning to the percept. For example, a hammer represented in the NCC is likely to influence plans for hammering. Crick and Koch speculate that the penumbra neurons may be the site of unconscious priming. Other authors have called this “fringe” consciousness, after William James.

This, then, is Crick and Koch’s ten-point framework. Is it original? Not in its parts, as the authors freely acknowledge: they site similar ideas by Baars, Dennett, Grossberg, Edelman and Tononi and Bachmann among others, and refer to a similar framework put forward by Dehaene and Naccache. What Crick and Koch’s framework does is to put together some of the best ideas relating to consciousness and the brain that have been floating around, some for as long as fifty years.

Some editorial reflections

How secure and solid is this framework? Sadly, not very. The article is filled with speculations, uncertainties, tenuous analogies (the competition of coalitions is like a political primary, winning coalitions can “relax a little” because they have “tenure”), is replete with words like may, might, perhaps and probably. In this respect, Koch and Crick’s structure resembles, not a solid framework, but rather a woolly, shifting, transient coalition of the exact type that they describe. Even when Crick and Koch talk about hard neuroscience (cortical connections, neuronal synchrony, driving versus modulating inputs), their words are not confident and conclusive, but uncertain and tentative.

Of course, it is unfair to blame Crick and Koch for this. This is the nature of the beast that all of us have to deal with. Koch and Crick’s thoughts and caution, after a decade of hard work, show the immense gap that exists in our knowledge, not just about how the brain gives rise to consciousness, but about the structure and functional organization of the brain itself. In this regard, the forward looking portion of this article is quite interesting: the authors call for more comprehensive studies of cortical architecture, and for multi-electrode recordings from humans and from primates. A specific experiment suggested is to record from a thousand or more electrodes from the owl monkey, for reason of its smooth cortex.

The fact that Koch and Crick’s framework can be a leading article in a top journal devoted to hard neuroscience shows that a lot of progress has been made in focusing scientific effort on consciousness. This is indeed good news, and the uncertain, stumbling steps that are being taken by the nascent science of consciousness are precisely on schedule for this crawling baby. Like Koch and Crick’s picture, their static snapshot of the posture of this new science suggests forward motion. The next several frames in this movie, to be played out in the coming decade, will show how well it is learning to walk.

© 2003, P. Mutalik

Author Information

Pradeep Mutalik
Yale Medical Schol
New Haven, CT

References

1. A framework for consciousness, Francis Crick & Christof Koch,Nature Neuroscience, February 2003 Volume 6 Number 2 pp 119 – 126

Abstract

Here we summarize our present approach to the problem of consciousness. After an introduction outlining our general strategy, we describe what is meant by the term ‘framework’ and set it out under ten headings. This framework offers a coherent scheme for explaining the neural correlates of (visual) consciousness in terms of competing cellular assemblies. Most of the ideas we favor have been suggested before, but their combination is original. We also outline some general experimental approaches to the problem and, finally, acknowledge some relevant aspects of the brain that have been left out of the proposed framework.