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2.3 John Eccles and the ‘Liaison Brain’

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Eccles’s achievement

After studying medicine at Melbourne University, John Eccles (1903–1997) went to Oxford in 1925 as a graduate student to work with Sherrington, who was at that time engaged in research with Liddell on the characteristics of the myotatic reflex and with Creed on the flexion reflex. Eccles’s first experimental work was done with Creed. It was on the subject destined to dominate his research for over forty years: the mechanism of inhibitory synaptic transmission. After completing his DPhil in 1929, he joined Sherrington’s research group, and developed a technical improvement of the torsion myograph in preparation for a collaboration concerned with research on the flexion reflex and inhibition. These experiments were to see the last flowering of Sherrington’s scientific genius at the age of seventy-five. The work on the ipsilateral spinal flexion reflex introduced Eccles to the technique of stimulating nerves first with just a threshold conditioning volley, then at later intervals with a subsequent test volley in order to tease out the time course of the central excitatory and inhibitory states. This approach, when applied to the mechanism of transmission in the spinal cord, gave a very precise measure of the time course of the central excitatory and inhibitory states, or, as we now know, the excitatory and inhibitory postsynaptic potentials. This was shown by Eccles and his colleagues some twenty years later, when they made the first intracellular recordings of postsynaptic potentials in motoneurones. Subsequent studies of inhibitory synaptic transmission using intracellular electrodes were carried out by Eccles and his colleagues at successively higher levels of the central nervous system. These provided a functional microanatomy of the synaptic connections to be found in the cerebellum, the thalamus and the hippocampus. In this way Eccles completed the research programme described by Sherrington in The Integrative Action of the Nervous System half a century earlier.

Eccles’s interest in themind–brain problem

Eccles had entered the field of neuroscience as a result of an inspirational experience he had had at the age of eighteen that changed his life and aroused in him an intense interest in the mind–brain problem.12 In the 1970s, evidently stimulated by the work done by R. W. Sperry and his colleagues in the 1960s on the results of hemispherectomy, he turned at last to these philosophical questions of his youth, first in The Self and its Brain (1977), a book he wrote with Karl Popper, and subsequently in his Gifford Lectures of 1977–8, published in 1984 as The Human Mystery. He opened his Gifford Lectures with a handsome tribute to Sherrington’s Gifford Lectures forty years earlier. Eccles remarked that the general theme of Man on his Nature had been the defence of a form of dualism – a doctrine that was, by the 1970s, antipathetic to established philosophy. Nevertheless, it was a doctrine that Eccles deeply admired and, moreover, believed to have been given experimental confirmation by Kornhuber’s work on the electrical potential generated in the cerebral cortex prior to performing an intentional action and by Sperry’s work on split-brain patients. Hence, he aimed, in his own Gifford Lectures, to defend Sherrington’s conception, to ‘define the mind–brain problem more starkly’,13 and to bring to bear on the problem these most recent findings in neuroscience.

Popper’s influence

The general framework for Eccles’s reflections was furnished by Popper’s revival of a misconceived idea of the great nineteenth-century mathematical logician Gottlob Frege.14 Frege distinguished between the perceptible ‘outer world’ of physical objects, the private ‘inner world’ of mental entities, and a ‘third realm’ of thoughts (propositions) that are imperceptible by the senses, but nevertheless public and shareable. Popper followed suit, distinguishing between World 1 of physical things, World 2 of mental things, and World 3 of thoughts, theorems, theories and other abstracta. The conception is confused, since although we distinguish material objects from mental states, and both from propositions or theorems, these do not collectively constitute ‘worlds’ in any sense whatsoever. Furthermore, neither mental states nor propositions are denizens of a distinct ‘world’. There is only one world, which is described by specifying whatever is (contingently) the case. We do indeed talk of people’s mental states of cheerfulness or depression, or of their having toothache. But this does not imply that cheerfulness, depression or toothache are peculiar mental entities that exist in an ‘inner world’. These nominals (‘cheerfulness’, ‘depression’, ‘toothache’) merely provide an indirect way of talking of people being cheerful or depressed and of their tooth’s hurting – it introduces no new entities, merely new ways of talking about existing entities (e.g. about human beings and how things are with them). Similarly, we talk of propositions, theorems and other abstracta – but this too only appears to introduce new entities, and is really no more than a convenient way of talking about what is or might be said, asserted, or proved, etc. There is absolutely no need to succumb to Platonism and conjure new entities into existence and new worlds for them to inhabit. All talk of expressions standing for ‘abstract entities’ is a misleading way of saying that expressions that look as if they stand for concrete entities do not do so at all, but rather fulfil quite different functions. To be sure, this does not mean that there are no mental states, no cheerfulness, depression or anxiety, or that there are no propositions, no theories or theorems. On the contrary, it means that there are – only they are not kinds of entities.

Popper’s three-world doctrine impressed Eccles, and he formulated his dualism in terms of it. World 1, the material world of the cosmos, he declared, consists of mere material things and of beings that enjoy mental states. The latter, being a subset of the entities in World 1, he refers to collectively as ‘World 1 M’. This ‘world’ stands in reciprocal causal interaction with World 2 by means of what he terms ‘the liaison brain’ (HM 211).

The impact on Eccles of Kornhuber’s research on readiness potential

Research done by Kornhuber and his colleagues (see §1.6.1) on changes in electrical potential antecedent to a voluntary movement had revealed that the so-called readiness potential began up to 800 milliseconds before the onset of the muscle action potential, and led to a sharper potential, the pre-motion positivity, beginning at 80–90 milliseconds prior to the movement. The patterns of neuronal discharges eventually project to the appropriate pyramidal cells of the motor cortex and synaptically excite them to discharge, so generating the motor potential (a localized negative wave) just preceding the motor pyramidal cell discharge that initiates the movement. The question on which Kornhuber’s research seemed to throw light was: ‘How can willing of a muscular movement set in train neuronal events that lead to the discharge of pyramidal cells of the motor cortex and so to the activation of the neuronal pathways that lead to the muscle contraction?’ (HM 214). It is striking that Eccles took these discoveries to betoken empirical confirmation of mind–brain interaction of a kind (but in a different location) that had been envisaged by Descartes. He argued as follows:

What is happening in my brain at a time when the willed action is in the process of being carried out? It can be presumed that during the readiness potential there is a developing specificity of the patterned impulse discharges in neurons so that eventually there are activated the pyramidal cells in the correct motor cortical areas for bringing about the required movement. The readiness potential can be regarded as the neuronal counterpart of the voluntary intention. The surprising feature of the readiness potential is its very wide extent and gradual build up. Apparently, at the stage of willing a movement, there is a very wide influence of the self-conscious mind on the pattern of module operation. Eventually this immense neuronal activity is moulded and directed so that it concentrates onto the pyramidal cells in the proper zones of the motor cortex for carrying out the required movement. The duration of the readiness potential indicates that the sequential activity of the large numbers of modules is involved in the long incubation time required for the self-conscious mind to evoke discharges from the motor pyramidal cells … It is a sign that the action of the self-conscious mind on the brain is not of demanding strength. We may regard it as being more tentative and subtle, and as requiring time to build up patterns of activity that may be modified as they develop.(HM 217)

Cartesian problems recapitulated:

(1) Interaction

So, Eccles conceived of what he called ‘the dualist-interactionist hypothesis’ as helping to ‘resolve and redefine the problem of accounting for the long duration of the readiness potential that precedes a voluntary action’ (HM 217). Descartes, as we have noted, conceived of the mind as operating upon the pineal gland to generate the minute fluctuations in the animal spirits (the role-equivalent of neural transmitters) in the ventricle in which he thought the pineal gland was suspended. This, he held, enabled the acts of will of the mind to affect the motions of the animal spirits, which are then transmitted to the muscles. But the question of how an immaterial substance could actually interact causally with a material object such as the pineal gland to produce the appropriate minute motions was left totally unanswered. In much the same way, Eccles thought that the ‘self-conscious mind’ interacts causally with the pyramidal cells of the motor cortex, gradually (rather than instantaneously) getting them to discharge. But the question of how an immaterial entity such as the mind can interact causally with neurons was left equally unanswered.

(2) Reifying the mind

Both thinkers erred in conceiving of the mind as an entity of some kind. Had they heeded Aristotle in thinking of the mind, or more accurately, of the psuche-, not as an entity but as an array of powers or potentialities, they would have been much closer to the truth, and would not have become enmeshed in insoluble problems of interaction. For it patently makes no sense to ask how one’s abilities to do the various things one can do interact with one’s brain.

(3) Misconceptions about the will

Both thinkers erred in imagining that voluntary movements are movements produced or caused by antecedent acts of will.15 For although there are such things as acts of will – namely, acts performed with great effort to overcome one’s reluctance, aversion or difficulties in acting in adverse circumstances – obviously the vast majority of our ordinary voluntary actions involve no ‘act of will’ in this sense at all. We shall examine this conception in chapter 9.

Eccles was further confused over the object of the alleged act of will, which is variously characterized as (i) a muscular movement, (ii) an action or (iii) a movement of a limb.

Confusions about the object of the alleged act of will

It is, of course, possible to intend to move a muscle – for example, to flex a muscle – but that is something we rather rarely intend to do, and although the movement of muscles is involved in all our positive, physical acts ( by contrast with acts of omission and mental acts), what we intend, and what we voluntarily perform, are actions (such as raising our arm, writing a letter, saying something, picking up a book, reading a book, and so on), and not the constitutive muscle movements of these actions, of which we are largely unaware. But it is easy to see why a neuroscientist who is attracted to dualism should confuse the objects of the will. For, according to the dualist conception, the mind has causally to affect the brain, and the causal powers of neural events in the brain causally affect muscle contraction.

Problems of volitional interaction between mind and brain

This raises yet a further insoluble problem for the dualist. The ‘self-conscious mind’ is supposed to influence the pattern of module operation, gradually moulding and directing it so that it concentrates on the pyramidal cells in the proper zones of the motor cortex for carrying out the intended movement. But how does the ‘self-conscious mind’ know which pyramidal cells to concentrate on, and how does it select the proper zones of the motor cortex? For it would need such knowledge in order to execute such actions. And it is certainly not knowledge of which the self-conscious mind is conscious. To these questions there can be no answers, any more than the nineteenth-century innervationist ideo-motor theories of voluntary movement (chapter 9), favoured by such eminent scientists as Helmholtz and Mach (and psychologists such as Bain and Wundt), could answer the question of how the mind, in addition to having images of kinaesthetic sensations that allegedly accompany voluntary movements, directs the currents of energy going from the brain to the appropriate muscles. ( There must be appropriate feelings of innervation – of ‘impulse’ or ‘volitional energy’, they thought, otherwise the mind could never tell which particular current of energy, whether the current to this muscle or the current to that one, was the right one to use.)

Eccles’s conception of the implications of Sperry’s discoveries about results of split-brain operations

A second piece of empirical research encouraged Eccles in his advocacy of interactionist dualism. Sperry’s discoveries concerning the capacities of split-brain patients were striking. He himself took them to vindicate some form of mind–brain interactionism:

Conscious phenomena in this scheme are conceived to interact with and to largely govern the physiochemical and physiological aspects of the brain process. It obviously works the other way round as well, and thus a mutual interaction is conceived between the physiological and the mental properties. Even so, the present interpretation would tend to restore the mind to its old prestigious position over matter, in the sense that the mental phenomena are seen to transcend the phenomena of physiology and biochemistry.16

It is therefore unsurprising that Eccles thought that Sperry’s work had dramatic implications. ‘It is my thesis’, he wrote, ‘that the philosophical problem of brain and mind has been transformed by these investigations of the functions of the separate dominant and minor hemispheres in the split-brain subjects’ (HM 222). The ‘most remarkable discovery’, Eccles held, was that all the neural activities in the right hemisphere ‘are unknown to the speaking subject, who is only in liaison with the neuronal activities in the left [dominant] hemisphere’. To be sure, the right hemisphere is ‘a very highly developed brain’, but it ‘cannot express itself in language, so is not able to disclose any experience of consciousness that we can recognize’. The dominance of the left hemisphere, he argued, is due to its verbal and ideational abilities, and ‘its liaison to self-consciousness ( World 2)’ (HM 220). For what Sperry’s work shows, Eccles averred, is ‘that only a specialized zone of the cerebral hemispheres is in liaison with the self-conscious mind. The term liaison brain denotes all those areas of the cerebral cortex that potentially are capable of being in direct liaison with the self-conscious mind.’17

Eccles’s conception of the liaison brain and Descartes’s conception of the pineal gland compared

Descartes thought that the pineal gland was the point of contact of the mind and the brain, and that the mind apprehends what is before the eyes of the body in virtue of the images that come from the two eyes and are united on the pineal gland. Eccles thought that the liaison brain was the point of contact with the mind, where the nerve impulses from the sense-organs are, in some sense, made available to the mind. But there is an interesting difference between the two doctrines. Descartes thought that the pineal gland itself – that is, a part of the brain – fulfils the task of the Aristotelian and scholastic sensus communis, the task of synthesizing and unifying the data of the separate senses. In this respect, his thought was more up to date than Eccles’s, since contemporary neuroscientists think likewise that the ‘binding problem’ is solved by the brain (rather than by the mind).18 For Singer’s discoveries19 of coherent oscillatory firings in disparate parts of the brain concomitant with perceptual experience suggest that the simultaneity of these manifold neuronal activities and their connections to other areas of the cortex are necessary conditions for a perceiver to have the kind of unified perceptual experience we have. Eccles, by contrast, defended what he called ‘the strong dualist hypothesis’ that

the self-conscious mind is actively engaged in reading out from the multitude of active modules at the highest levels of the brain, namely in the liaison areas that are largely in the dominant cerebral hemisphere. The self-conscious mind selects from these modules according to attention, and from moment to moment integrates its selection to give unity even to the most transient experience. Furthermore, the self-conscious mind acts upon these modules, modifying the dynamic spatio-temporal patterns of the neuronal events. Thus the self-conscious mind exercises a superior interpretative and controlling role upon the neuronal events both within the modules and between the modules. A key component of the hypothesis is that the unity of conscious experience is provided by the self-conscious mind and not by the neuronal machinery of the liaison areas of the cerebral cortex. Hitherto it has been impossible to develop any neurophysiological theory that explains how a diversity of brain events comes to be synthesized so that there is a unified conscious experience … My general hypothesis regards the neuronal machinery as a multiplex of radiating and receiving structures ( modules). The experienced unity comes, not from a neurophysiological synthesis, but from the proposed integrating character of the self-conscious mind. I conjecture that in the first place the raison d’être of the self-conscious mind is to give this unity of the self in all its conscious experiences and actions.(HM 227f.)

How does the mind engage in this activity of synthesis (or ‘binding’)? Eccles suggested that the mind

plays through the whole liaison brain in a selective and unifying manner. The analogy is provided by a searchlight. Perhaps a better analogy would be some multiple scanning and probing device that reads out from and selects from the immense and diverse patterns of activity in the cerebral cortex and integrates these selected components, so organizing them into the unity of conscious experience … Thus I conjecture that the self-conscious mind is scanning the modular activities in the liaison areas of the cerebral cortex … From moment to moment it is selecting modules according to its interests, the phenomena of attention, and is itself integrating from all this diversity to give the unified conscious experience.(HM 229)

Four flaws in Eccles’s conception

The metaphors are striking, and have echoes in current neuroscientific theory.20 Nevertheless, Sperry’s discoveries have none of the dramatic implications that Eccles imputed to them. There are four flaws in Eccles’s conception to which we wish to draw attention.

(1) The phenomena resultant upon hemispherectomy were misdescribed

First, the phenomena were misdescribed. It is not just the neural activities of the right hemisphere that are unknown to the subject – all the activities of the brain are unknown to subjects, who do not, after all, perceive their own brains (and, even if they could, do not have electron microscopes for eyes). It is true that the right hemisphere cannot ‘express itself in language’, any more than the right leg – because there is no such thing as a part of a human being expressing itself in language (see §§3.1–3.4). So the left hemisphere cannot ‘express itself in language’ either. The right hemisphere is not able ‘to disclose any experience of consciousness’ that we can recognize, because there is no such thing as a subordinate part of a human being being conscious. As will be argued in detail in chapter 3, it is only human beings (and other animals) who are conscious (or unconscious), and conscious of (or not conscious of) various things – not their subordinate parts. The left hemisphere is equally lacking in ‘any experience of consciousness’. Finally, the left hemisphere has no ‘verbal and ideational abilities’, although the verbal and ideational abilities of normal human beings are causally dependent upon the normal functioning of the left hemisphere.21

(2) The ‘self-conscious mind’ is not an entity of any kind

Second, the so-called self-conscious mind is not an entity of any kind, but a capacity of human beings who have mastered a reflexive language. They can therefore ascribe experiences to themselves and reflect on the experiences thus ascribed (see §14.6). But the ‘self-conscious mind’ is not the sort of thing that can intelligibly be said to be ‘in contact with’ the brain ( let alone with something denominated ‘the liaison brain’).

(3) Incoherence in Eccles’s hypothesis

Third, Eccles’s main hypothesis is unintelligible. If the self-conscious mind were, per impossibile, ‘actively engaged in reading out’ from areas in the dominant hemisphere and ‘selecting from these modules according to attention’, then the self-conscious mind would have to perceive or be aware of the neural modules in question (otherwise how could it ‘read them out’?), and know which ones to select for its purpose (otherwise the wrong ones might constantly be selected). Or, to put matters more lucidly, for any of this story to make sense, human beings would have to be aware of the neural structures and operations in question, and, from moment to moment, decide which ones directly to activate, and, of course, have the capacity to do so. But we possess no such knowledge and no such capacity.

(4) The very notion of the self-conscious mind presupposes the unity of experience

Finally, it is confused to suppose that the raison d’être of the ‘self-conscious mind’ is to engender the unity of the self and, as our contemporaries would put it, ‘solve the binding problem’. For any talk of a person or of a human being as having a mind already presupposes the unity of experience and cannot be invoked to explain it.

Eccles’s errors cannot be rectified by substituting the brain for his conception of the ‘self-conscious mind’

Eccles’s dualism was misconceived. Contemporary neuroscientists are eager to dissociate themselves from his doctrines and to dismiss his ideas as silly. This is misguided. Eccles had the courage to face difficult problems and to pursue his ideas about them to their logical conclusions. That his ideas are wrong is true, and much can be learned from the errors in question. It is, however, a sad mark of how little many neuroscientists have learned from Eccles’s struggles that they apparently believe that the problems that Eccles’s interactionist dualism was designed to answer can be solved by substituting the brain for Eccles’s ‘self-conscious mind’. Problems regarding how the mind can bring about movements of the muscles and limbs by acts of will are not solved by supposing, as Libet does (see §9.2), that it is the brain that decides what muscles and limbs to move. Although it is misguided to suppose that the mind is in liaison with the left hemisphere, it is no less misconceived to suppose, as do Sperry, Gazzaniga and Crick (see §17.3), that the hemispheres of the brain know things, have beliefs, think and guess, hear and see. For these are functions of human beings and other animals, not of brains or half-brains (which enable human beings to exercise those functions). And, as we have noted, although it is confused to suppose that the mind scans the brain, it is equally confused to suppose that the brain must scan itself in order to generate awareness or self-consciousness – as if it lay in the nature of self-consciousness that it necessarily involves a self-scanning process, if not of the mind, then of the brain. In short, the lessons that can be learned from Eccles’s failure have largely yet to be learned. We shall endeavour to show this in some detail in later chapters.

Philosophical Foundations of Neuroscience

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