Walter J. Freeman's Neurodynamics and Neurophilosophy of Meaning

I've been interested in Walter Freeman's work for a while now, and having just read his book 'How brains make up their minds' (HBMUTM; note the double entendre) on holiday, I thought I'd have a go at summarizing some of his ideas. This is a pretty tall order, for at least four reasons: there are a lot of them, they are sometimes quite complicated, they are sometimes quite unconventional, and they are sometimes a bit loose. Here goes...

The scope of material covered in HBMUTM is very impressive - from basic physiology and anatomy to a psychology (of sorts) of perception and action via an extremely well-developed mathematical theory of neural population dynamics, with regular commentaries and contributions from from philosophy of science and philosophy of mind. However by the final chapter on 'knowledge and meaning in societies', Freeman's unbridled and speculative elaboration of his ideas does become quite tiresome. For me, the majority of interesting content can be found in chapters 2 ("Meaning and representation"), 3 ("Dynamics of neurons and neuron populations"), 4 ("Sensation and perception") and 5 ("Emotion and intentional action"), although the discussion of causality in chapter 6 ("Awareness, consciousness, and causality") is also interesting. I'm going to pick out and base the following on what I see as the two main strands to the book:

1. Freeman's general theory of brain function ('nonlinear neurodynamics') and of how meaningful percepts are formed from sensory stimuli
2. The running commentary contrasting three 'modes of intepreting experimental data from the neural and cognitive sciences about the nature of the mind': materialism, cognitivism, and pragmatism. 

Nonlinear neurodynamics and the neural basis of meaning




Most of Freeman's experimental work comes from intracranial EEG (also called 'ECoG' - 'electrocorticogram') recordings from olfactory cortex of rabbits when they detect and respond to conditioned stimuli (i.e. stimuli, normally chemical odourants, that they have been trained to associate with a reward). He considers that this association of a reward to the stimulus makes an otherwise irrelevant sensation (e.g. the smell of burnt wood) 'meaningful' to the animal. Behavioural saliency of this kind appears to be quite an important component of his notion of meaning; in fact at one point he says that the amplitude modulation patterns (see below) that characterize the meaning of an odourant to the animal actually disappear when that odourant is 'unconditioned' through a new training regime, or when it is fed to satiety, which remove the behavioural salience of the stimuli.

Whether one would actually need to condition stimuli in this way to invoke a salience-based response in humans is probably an open question. Perhaps simply following instructions in a visual object processing task would be enough to establish the salience of the stimuli; whereas for rabbits it is necessary just to get them to do the task? Clearly for people working on constructs labelled 'meaning' in other areas such as language or vision, it's very important that this terminological/experimental difference be borne in mind when reading Freeman's less anthropocentric use of the term. Irrespective of whether one agrees with every aspect of his theory of meaning in all its neuroscientific and philosophical intricacies (and I will not go into all of these here), however, I think most neuroscientists interested in brain systems at the meso- or macroscopic scale will find something interesting in this body of work.

For Freeman, meanings 'arise as a brain creates intentional behaviours and then changes itself in accordance with the sensory consequences of those behaviours' (pg. 9). 'Intentional' here is in the sense of 'intentionality' - not in the Brentanoan sense of the 'aboutness' of a representation (as generally used by contemporary philosophers), but rather in the original sense of Thomas Aquinas (who actually coined the term), as the 'directing of an action towards some future goal'. After an introductory chapter and an outline of his philosophical position in chapter 2, the core neuroscientific content of HBMUTM is given in chapters 3-5, over which Freeman gradually sets out what he describes as the '10 building blocks that allow us to understand how neural populations sustain the chaotic dynamics of intentionality'. These are generously summarized first at the end of chapter 2 (pgs. 37-38):

10 building blocks in the dynamics of intentionality:

1. The state transition of an excitatory population from a point attractor with zero activity to a non-zero point attractor with steady-state activity by positive feedback
2. The emergence of oscillation through negative feedbck between excitatory and inhibitory neural populations
3. The state transition from a point attractor to a limit cycle attractor that regulates steady-state oscillation of a mixed excitatory-inhibitory cortical population
4. The genesis of chaos as background activity by combined negative and positive feedback among three or more mixed excitatory-inhibitory populations
5. The distributed wave of chaotic dendritic activity that carries a spatial pattern of amplitude modulation made by the local heights of the wave
6. The increase in nonlinear feedback gain that is driven by input to a mixed population, which results in construction of an amplitude-modulation pattern as the first step in perception
7. The embodiment of meaning in amplitude modulation patterns of neural activity, which are shaped by synaptic interactions that have been modified through learning
8. Attenuation of microscopic sensory-driven activity and enhancement of macroscopic amplitude-modulation patterns by divergent-convergent cortical projections underlying solipsism
9. The divergence of corollary discharges in preafference followed by multisensory convergence into the entorhinal cortex as the basis for Gestalt formation
10. The formation of a sequence of global amplitude-modulation patterns of chaotic activity that integrates and directs the intentional state of an entire hemisphere

(bold in original text)

Those familiar with Freeman's other, more technically-oriented work, will notice that this summary contains some of the key components of his so-called 'K-sets' - a hierarchical framework for modelling the dynamics of mixed excitatory-inhibitory neural populations (see the scholarpedia article on K-sets for more on this). These provide the analytical basis for understanding the general phenomenological feature of the ECoG data that has really been the focus of Freeman's research career - what he calls (after Karl Lashley) mass action. This gave the title of his seminal 1975 book Mass Action in the Nervous System, but I recommend the scholarpedia article on mass action for a more up-to-date and concise summary. In short, 'mass action' refers to the observation  (originally in the olfactory cortex of rabbits, and now apparently in all sensory cortices) of the aperiodic emergence of global patterns covering large swathes of cortex. These global patterns are referred to as 'wave packets', where all points (ECoG sensors) show the same basic waveform (the 'carrier wave'), but with varying amplitudes (heights and troughs of the wave), resulting in so-called spatial 'amplitude modulation' (AM) patterns. It is these distributed spatial AM patterns that, for Freeman, constitute the 'meaning' of the stimulus to the animal;

"[Mass action] refers to the collective synaptic actions that neurons in the cortex exert on each other in vast numbers by synchronizing their firing of action potentials. In the aggregate, [mass action] is a powerful force that creates bursts of cortical neural activity that resemble the vortices of tornadoes and hurricanes. The bursts rapidly and repeatedly retrieve memories and bind them with sensory information into percepts. In this way, [mass action] expresses and transmits the meaning of sensory information in spatial patterns of cortical activity that resemble frames in a movie." (from the mass action scholarpedia article)

Above is an example of AM patterns from an 8x8 grid of electrodes spaced 0.5mm apart on the olfactory bulb. I got the figure from the scholarpedia article on mass action, but it is also in HBMUTM. On the left are example time series of the local field potentials, on the right are contour plots showing the mean spatial AM pattern across the grid. According to the figure legend,

'The pattern difference in Trial Set 1 (above to below) reflects the formation of a neural assembly during training. The pattern differences from Set 1 to Set 3 with the same control and CS [conditioned stimulus] inputs reflect permanent changes in memory with consolidation. The lack of AM pattern invariance with invariant stimuli shows that AM patterns are retrieved from memory and modified by input. They are not representations of sensory stimuli; they are memories that are created by the sensory cortex.' 

Thus, for Freeman, the spatial AM patterns are not to be understood as representations of the stimulus, since they are highly dependent on personal history and current goals, and are not invariant across trials. The fact that they appear to incorporate such a high degree of abstraction and contextual dependence is remarkable, given that (in olfactory cortex at least) they are only one synapse away from the sensory receptors.

I imagine a lot of people reading this will be asking themselves the same question I ask myself constantly, namely 'is this something observable in / relevant to EEG/MEG data / research in humans? The spatial AM patterns are (I believe) simply time series or induced power plots (left and right columns in the figure, respectively) of (gamma) band-pass filtered data. I think the classification with respect to the CS involves an ICA step (this isn't mentioned in HBMUTM). Clearly there is also some overlap with multivariate pattern analysis methods that are becoming popular in imaging.

The fact that the patterns are 'global', or at least cover large areas, implies some kind of connectivity between the different regions. There is a very revealing section in HBMUTM (pgs. 116-117) where Freeman likens his findings to those of a long list of scientists who have studied / are studying 'global processes underlying the unity of perception and action' - including Karl Pribram, Antonio Damasio, Jack Pettigrew, Paul Nunez, Stuart Hameroff & Roger Penrose, Dietrich Lehmann, Urs Ribary & Rodolfo Llinas, Catherine Tallon-Baudy, Mathias Muller, Francisco Varela, Steve Bressler, Moshe Abeles, and several others. So if like me you have an idea of the typical work attributed to these scientists, then you can get a bit more of an intuition as to what kind of phenomena Freeman thinks he is studying.

Interestingly, however, he does follow this up with the following comment:

"The formation of global AM patterns indicates that the sensorimotor and limbic areas of each hemisphere can rapidly enter into a cooperative state, which persists for perhaps a tenth of a second before dissolving to make way for the next state. This cooperation does not develop by entrainment of coupled oscillators into synchronous oscillations. as resonance is much too slow and the linear correlations between the waveforms from the different locations stay well above chance levels and do not fluctuate significantly. But it is not the level of correlation that changes with perception and action, but the global AM pattern, as the cooperation carries the entire hemisphere from one global chatoic attractor to the next. The genesis of macroscopic chaos by interacting brain parts does not require that they oscillate with identifical waveforms having linear correlations." (pg. 117)

My bolds and underlines this time. This caught my eye especially because my conception of global co-ordination amongst distributed brain systems absolutely does involve some combination of entrainment of coupled oscillators and resonance effects due to boundary conditions in contiguous synaptic action fields. I would say that is probably more or less the conventional view in the field at this point in time (anyone agree / / disagree here? ). Ok yes you can have synchrony without oscillations. But Freeman is suggesting something more radical here: abrupt and near-instantaneous transitions between globally coupled (and spatially amplitude-modulated) states; these are the 'frames' of sensation and perception. He sees this as no less than a paradigm shift, which perhaps makes it easier to appreciate why in more recent work he has been exploring different ways of modelling mass action borrowed from modern physics, such as percolation processes in cellular automata networks (with Robert Kozma), and (with Giuseppe Vitiello) as manifestations of spontaneous symmetry breaking. Deep.

Freeman's neurophilosophy and philosophy of neuroscience


According to the Stanford encyclopedia of philosophy:

"The literature distinguishes “philosophy of neuroscience” and “neurophilosophy.” The former concerns foundational issues within the neurosciences. The latter concerns application of neuroscientific concepts to traditional philosophical questions. Exploring various concepts of representation employed in neuroscientific theories is an example of the former. Examining implications of neurological syndromes for the concept of a unified self is an example of the latter."

In HBMUTM we see both of both of these. A number of intricate, albeit sometimes rather loose, positions are articulated on 'neurophilosophical' issues such as meaning, perception, consciousness, intentionality, and free will, amongst others. For me, though, the more interesting (but still rather eclectic) sentiments fall under the philosophy of neuroscience (/philosophy of psychology; these two often blur together) category. He states his agenda here early on:

"To relate the properties and operations of neurons and populations to the mental experience of meaning, I will contrast three modes of interpreting the experimental data we have from the neural and cognitive sciences about the nature of the mind. Within the general framework of the history of philosophy and psychology, there are three dominant views: materialist, cognitivist, and pragmatist, of which my theory falls into the pragmatist category." (pg. 23)

According to Freeman's scheme, materialists "view minds as physical flows, whether of matter, energy, of information, which have their sources in the world", cognitivists "argue that minds are made not of energy of matter, but of collections of representations that constitute symbols and images. They are software running on 'wetware'.", whereas pragmatists  "think that minds are dynamic structures that result from actions into the world." He attributes much of the pragmatist definition to Aquinas, and Aquinas' account of Aristotle's doctrine of 'active perception', "according to which the organism learns about the world and realizes its potential by its actions on the world." Also the similarities between the cognitivist and materialists are apparently due to the fact that  "over the past 50 years neurobiologists have borrowed  many of their interpretations of their data from cognitive scientists when they began to realize that the neuron doctrine wasn't working very well." 

This tripartite comparison forms a consistent thread that runs throughout the entire book, and is regularly returned to in the light of the particular content being discussed at various points. With respect to the core scientific topics of the book, spatial AM patterns in sensory cortices:

"...the data on the AM patterns can be interpreted in different ways, depending on your choice of philosophical premises."


According to the materialist view:


"these AM patterns reflect information processing....an odorant stimulus delivers information to the receptors, which process it by transducing it to action potentials. These pulses are transmitted to the bulb, where the information is bound into patterns and held, while it is being relayed by the tract to the cortex. The information stored in the cortex from previous stimuli is retreived and sent back to the bulb, where a comparison is made by correlation of the newly recieved AM pattern with each of a collection of retrieved AM patterns...The classification process is completed when the best match is found to identify an odourant. That best AM pattern is sent to other parts of the brain, where it serves to select and guide a fixed action pattern as a response to the stimulus."


for cognitivists:

"...each AM pattern represents an odourant. It is a symbol that signifies the presence of a source of food or danger. The receptor action potentials represent the features of the odourant, and the process by which the bulbar action potential are brought into synchrony through their synaptic interactions to represent an odour is feature binding. The integration of the features by a higher-order neuron makes it fire, and its activity represents that object that has the features.

...This approach cannot deal with the lack of invariance of AM patterns with respect to stimuli.


and for pragmatists:

"...the AM patterns are an early stage in the construction of meaning. They correspond to the 'affordances' advanced by J.J. Gibson in ecological psychology, by which an animal 'in-forms' itself as to what to do with or about an odourant, such as whether to eat the food or run from the predator giving the odorant information. They cannot be representations of odorants, because it is impossible to match them either with stimuli or with pulse pattens from receptor activation that convey stimuli to the cortex....They cannot be information, because that is discarded in the spatial integration performed by divergent-convergent pathways...They reveal the wings of attractors that are selected by the sensory pulses, each having a crater in the olfactory attractor landscape.
...In colloquial terms, the ingredients received by brains from their sensory cortices with which to make meanings are produce by the cortices. They are not direct transcriptions or impressions from the environment inside or outside the body. All that brains can known has been synthesized within themselves, in the form of hypotheses about the world and the outcomes of their own tests of the hypotheses..."

(pgs. 91-93) 

I personally find what Freeman is attempting to do here fascinating, but still can't help grinding my teeth a bit when reading it. I think the main reason for this reaction is that Freeman is (quite intentionally) mixing the history of philosophy (/ ideas) with current (/recent) debates and paradigms in psychology and neuroscience. In tracing the intellectual history of pragmatist thought, Freeman wants to thread an intellectual line from Aristotle through Aquinas to James, Gibson, Thelen, and himself (borrowing along the way from Dewey, Heidegger, Piaget, Merleau-Ponty). I think this is commendable and am not against such a project in principle, but unfortunately in practice what he ends up describing is times in danger of being somewhat incoherent - and, even worse, somewhat artificial. This is what I mean by mixing the history of ideas in philosophy with current debates in the sciences: yes there is a lively and thriving debate in psychology between cognitivists and dynamicists / enactivist / embodied cognition (any of which would be a more meaningful label than 'pragmatist' for the kind of ideas Freeman is describing), but I don't think it goes back to Aristotle or Aquinas. Similarly, I don't see the cognitivist/materialist distinction as really reflecting any current (or past, for that matter) debates in psychology or neuroscience, or the philosophy of psychology or neuroscience, that I'm aware of. I'm not sure how an 'information processing' perspective on brain function that doesn't invoke any concept of representations (as seems to be the case for Freeman's materialists) would work. And the perception-action cycle that for Freeman appears to go right to the heart of the pragmatist worldview ("Materialists and cognitivists view perception as a passive process that begins when a stimulus gives information that is transduced by receptors into a burst of neural activity, which cascades through the brainstem and thalamus into a sensory cortex...Pragmatists view perception as an active process, holding that humans and other animals maintain a stance of attention and expectation." (pg 101) has been right at the heart of cognitive psychology from very early one, as in e.g. the seminar work of Ulric Neisser in the 60s and 70s. I am sympathetic with some of Freeman's anti-representationalist sentiments, but I think the case is better articulated elsewhere (e.g. Chris Eliasmith, Tim van Gelder). 

Despite these gripes (make of them what you will), one thing that's certain is that it's always stimulating to hear people with strong opinions and different ideas. They probably bring out both the best and the worst in a writer/scientist/philosopher/person. I fear my opinions on Freeman's scientific and philosophical contributions may well fluctuate, as my own understanding and opinions develop themselves. One thing is certain though: they make you bloody well think.





Signing off,

john