2303The Cerebral Basis of Consciousness. by W. Russell

8/8/2019 2303The Cerebral Basis of Consciousness. by W. Russell

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BRAINA JOURNAL OF NEUROLOGY

FROM THE ARCHIVES

The cerebral basis of consciousness. By W. Russell Brain. Brain 1950: 73; 465-479; and The physiological basis ofconsciousness. A critical review by Russell Brain. Brain 1958: 81; 426–455.

In his presidential address to the Neurological Section of the Royal

Society of Medicine, delivered in October 1950, Russell Brain

(Fig. 1) aims to ‘make a broad survey of some aspect of

neurology . . .to consider how far the various pieces of the

jigsaw are fitting together, and what kind of picture they are

making. If the action of the nervous system is integrative, it is

doubly desirable that we should try to integrate knowledge of

it’. His topic is consciousness. This exists alongside awareness,

perception and emotion but is necessarily not independent of

these conscious states. What happens in the nervous system

when a conscious state is experienced must therefore be the

basis for studies of consciousness itself. Although their spatial

and temporal patterns of firing may vary, the character of

electrical conduction does not differ materially in pathways that

transmit the impressions of sensation, sight and hearing or any

other afferent impulses. The clue to consciousness lies more in

the fact that focal stimulation of the cerebral cortex can only be

perceived and localized to a specific part—say, the big toe—by

relating that structure to the entire body schema: ‘to perceive a

part of the body as pricked is to perceive it in relationship with the

whole of the rest of the body, pin-pointed as it were upon the

body-image. . .

we can appreciate touch without knowing itswhereabouts, but we cannot know a whereabouts that is vacant

of any sensory content’. It follows that electrical activity of the

sensory cortex must simultaneously cause widespread irradiation

of impulses throughout both hemispheres. John Hughlings-Jackson

(1835–1911) has already made the point that the ‘ . . .anatomical

substrata of subject-consciousness represent . . . all parts of the

body, mainly sensorily, in relation to one another . . . [they] are

centres of universal coordination . . .or synthesizing centres’.

These cortical centres are no more than nodal points for onward

distribution of sensory stimuli. Searching for an anatomical sub-

strate to these nodal points, physiologists have identified area 1 in

the post-central cortex which, other than for the face, has strictly

contralateral representation, and area 2 that registers both sides ofthe body but with a preference for crossed structures.

These principles are nicely illustrated by the clinical condition of

anosagnosia in which loss of sensation is combined with failure to

recognize that the affected part exists at all: ‘we can only miss

something if we remember that we once had it . . . the lesion in

such cases has destroyed not only the patient’s present awareness

of his body-image but also neurones which are essential to his

ability to remember that he ever possessed a[nother] half of the

body’. It follows that, in this situation, the intact cortex has

adjusted and accepts that the half-body of which it is aware is

now the whole. Taking forward his argument, Russell Brain reflects

on the observation of William Grey Walter (1910–77) that visual

imagery reproduces electroencephalographic alpha rhythms

identical to those observed when subjects view a real object,

indicating that imagination and reality deploy the same neuronalnetworks. Karl Lashley (1890–1958) has shown that blind animals

trained to navigate a maze lose their way when the visual cortex is

removed. Following head injury with frontal lobe damage, one of

Russell Brain’s patients with ‘loss of revisualization’ could recognize

people, even after brief acquaintance, but never visualize them;

nor could he remember details of a building plan (his trade)

without constant reference to the architect’s plans, or routes

Figure 1 Walter Russell Brain, first Baron Brain (1895–1966).

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when travelling even though he recognized the landmarks as each

was passed; and even his dreams were devoid of images despite

awareness of the narrative. The retention of ‘a propositional

memory of things which cannot be visualized . . .[provides] a pre-

cise experiment on the value of consciousness compared with

unconscious mechanisms in the visual sphere’. Other work

suggests that the ‘centre for revisualization’ is Brodmann area

19 but this is no more than the critical node in the widespreadneural network for imagery which is ‘set vibrating in an almost

infinite variety of patterns in space and time’.

The nervous system combines both category-specific (semantic,

in modern parlance) and particular (episodic) memories. Survival—

say of a mouse encountering a cat—depends on recognizing a

particular class without being distracted by the detailed variations

of its individual members: ‘the nervous system has solved

this . . .[by introducing] plasticity . . .so that [reaction] is not a

mosaic of all the individual features . . . but a pattern which con-

stitutes an abstraction . . .common to all individuals of the group’.

Small birds recognize a hawk solely from the features of outline

and movement. Russell Brain’s suggestion for the process that

abstracts the essential patterns of vision, music and speech, inter alia, is the derivation of perceptual concepts from ‘physiological

universals’. But he senses that consciousness must also have

an anatomical basis; and this is less easy to find. Certainly,

physiological universals involve the diencephalic nuclei, especially

the thalamus which has rich and widespread reciprocal connec-

tions to the cortex. The thalamus may filter impulses and

distinguish those signals for which localization will eventually be

needed—sensations referred to an anatomical part—from

experiences that are more generic such as emotions.

In a persuasive passage, Russell Brain argues that consciousness

adjusts automaticity and immediacy by adding space and time

distance receptors, or delays, into reflex responses. Sir Charles

Sherrington’s (1857–1952) introduction to the reissue of The

Integrative Action Of The Nervous System (1947), his last word

on the nervous system, makes the point: ‘. . . the brain is always

the part of the nervous system which is constructed upon and

evolved upon the ‘‘distance-receptors’’‘. Russell Brain extends

this concept to suggest that emotions are the manifestation in

consciousness of the motive power that sustains action in time;

short-term, as in the response to hunger, or lifelong, as in the

commitment to medical research; and, in animals, pouncing on

prey versus caring for the young. Russell Brain reflects how

the recall of events requiring a delayed reflex response involves

faithful representation by the cortex of the outside world through

symbolism and imagery. These images may bring aesthetic andother pleasurable dividends but primarily they determine response

and action; and they depend on memory. He points out that

memory is not exclusively a primate attribute: the worker honey-

bee on returning to the hive indicates to other workers a new

source of food by a dance in which ‘the direction of action of

gravity is symbolic of the direction of incidence of the sun’s rays’.

Finally, does unconsciousness, in which the quantum more than

the content is lost, help us to understand consciousness?

Everything suggests that consciousness is impaired, to varying

degrees and with different consequences, when function is altered

in the brainstem either through structural damage or electrical

discharges.

Having organized his thoughts on the nature of conscious

states, 8 years later Russell Brain feels that he should now tackle

both its anatomical and physiological bases. Taking forward the

discussion at a symposium from 1954 on ‘Brain mechanisms and

consciousness’ edited by ED Adrian (1889–1977) in which ideas

were rehearsed on ‘experienced integration’, ‘dynamic abstrac-

tion’, ‘momentary distributions of patterns’ and ‘cortical electro-

genesis’ as constituents of consciousness, Russell Brain (now editor

of Brain) focuses on the role of the brainstem central reticular

formation. But he has difficulty in defining this anatomical and

physiological entity linked to wakefulness and electroencephalo-

graphic arousal. What impresses Russell Brain is that the reticular

formation shows evidence for delayed activation linked to impulses

in ascending brainstem sensory pathways that relay in the thala-

mus en route to the cortex. Barbiturate anaesthetics appear to

disconnect this central processing, and hence awareness and

arousal, from the crude appreciation of incoming sensations.

Transection of the ascending reticular formation results in pro-

longed sleep. Conversely, stimulation of the ascending reticular formation leads to desynchronization of the electroencephalogram

and waking. Others consider this view of consciousness, arousal

of the ascending reticular formation associated with centripetal

sensory stimulation, to be limited and argue for more complex

multi-directional activity as consciousness waxes and wanes:

‘a slackening of activity of any region of the brain must result in

a lowering of excitatory state in areas or nuclei – including the

reticular formation – and so the whole of the synergic structures

are gradually affected. Doubtless ‘‘the functional depression’’ of

the reticular formation . . . plays a predominant, if not always an

initial, role in this process of cumulative ‘‘defacilitation’’‘.

Attempts at tracing the descending pathways that contribute

to consciousness show many inputs to the brainstem; andphysiological studies suggest that, whatever their origin, these

act tonically and competitively on the reticular formation:

‘responses to a flashing light recorded from the occipital cortex

of the cat were almost abolished when the animal was given fish

to smell’ and ‘the arrival of sensory impulses at a specific cortical

area [is] capable of exciting corticofugal impulses which have an

inhibitory effect upon the afferent pathways of other sensory

modalities’. In the same way, perception depends on selecting

from amongst a plethora of extraneous sensory stimuli in order

to focus on a single object or event whilst nevertheless attending

to the many additional components that contribute to an experi-

ence: ‘attention [uses] the discriminative power of the cortex to

focus consciousness upon a certain perceptual experience at anyparticular moment’.

Sleep differs from the unconsciousness of coma, in that it is

rapidly reversible and can be considered as a generalized with-

drawal of attention; waking involves the cortex in assessing an

afferent input and, if it is judged important, signalling on to the

diencephalon with ensuing arousal. In sleep and waking, there is

therefore reciprocal inhibition and facilitation of the cortex and

reticular formation. Sleep inhibits muscle tone and so, in turn,

reduces afferent stimulatory proprioceptive activity thereby

minimizing sensory disturbance of the slumbering ascending

2304 | Brain 2009: 132; 2303–2305 From the Archives



reticular formation. It follows that sleep and waking are enabled or

prevented by behaviours that generally depress or alert the ner-

vous system. For Russell Brain, the existence of a diencephalic

hypnagogic centre described by Walter Rudolph Hess

(1881–1973) seems improbable except insofar as the diencephalon

relays information conducted reciprocally between the brainstem

and the cortex.

As a clinician, Russell Brain wants to enhance his analysis of

consciousness through clinical examples but, curiously, this is

much the least coherent part of his review. W.H., aged 46

years, lapsed rapidly into a state of parasomnia [a term introduced

by Sir Geoffrey Jefferson (1886–1961) in 1944] with minimalpyramidal signs and died 11 days later; at autopsy there was

evidence for embolic infarction involving the left thalamus and

the brainstem bilaterally down to the junction of the anterior

and posterior corpora quadrigemina (Fig. 2). Self-evidently, this

lesion had destroyed the centre for consciousness. But the physiol-

ogy of consciousness may be better explained by studying

reversible coma, whatever its cause. Lesions around the third ven-

tricle induce a state of akinetic mutism; expanding hemisphere

lesions cause coma by compressing the midbrain through the

tentorium (coning); hypothalamic lesions cause restless and

uneasy sleep from which arousal is possible with alterations of

temperature and respiratory and cardiovascular rhythms; and

posterior fossa lesions result in coma that best resembles peacefulsleep. Even more intriguing are paroxysmal disturbances of

consciousness. On narcolepsy, Russell Brain engages a debate

we have previously rehearsed (see Brain 2008: 131; 2532–5) in

hinting at the difference of view between WA (William) Adie

(1886–1935) and (Samuel Alexander) Kinnier Wilson (1878–

1937), but he does not arbitrate; and he has little to say on

hallucinations other than those that are associated with disordered

consciousness. Hughlings-Jackson regarded grand mal and petit

mal seizures as ‘highest level fits’; and although modern electro-

physiology has implicated the thalamic intralaminar nuclei in

generating these attacks, the consensus is that a unilateral focus

fires into a more centrally placed (deep) structure—the centrifugal

downward spread mimicking the onset of sleep. This leads Russell

Brain to distinguish features of fits directly attributable to the focal

electrical discharge from those dependent upon ‘epileptic decon-

trol’ in which parts of the nervous system become unruly when

temporarily disconnected from the control of higher centres.

Now, Sir Russell Brain rehearses Sir Henry Head’s (1861–1940)

concept of brain ‘vigilance’, developed to explain why the

response of the nervous system varies with quality and complexity

of the stimulus more than its static amount—such diverse and

varying modes of activity demanding a state of vigilance or

choice in the response to stimulus. According to this analysis,

vigilance is consciousness. Head argued that regional pathology

may detach specific mental activities, such as perception and emo-

tion, and the psychical functions with which they are associated

from overall activity of the mind, i.e. consciousness. Brain is not

impressed and he rationalizes vigilance as an idea that, as his own

last word on neurology, Sir Henry Head had no time to refine or

develop in more detail. Nonetheless, Sir Charles Sherrington did

seem to accept and apply Head’s concept of vigilance.Satisfied with the concept of consciousness in terms of referen-

cing perception to the body schema, and accepting its anatomical

and physiological basis in reciprocal connectivity between the

cortex and the brainstem reticular formation, Russell Brain wants

to identify the separate contributions of these anatomical struc-

tures to consciousness. He distinguishes situations in which there is

disorder of the content of consciousness from the underlying state

of attention, vigilance or level of consciousness itself; and he spec-

ulates on the nature of referring present experience to the past

and transferring this to a concept of the future, as in memory and

imagination, as an integral part of consciousness. Integration is lost

with unconsciousness; and perceptual, emotional and temporal

integration are altered in epilepsy. But is consciousness integratedprimarily in the cortex or the reticular formation and is one

‘higher’, in Jacksonian terms, than the other? Both Hughlings-

Jackson and Sherrington write of ‘higher’ in terms of most

recent in evolutionary terms and synonymous with an expanded

cerebral cortex. For them, the cortex is the acme of evolution. It

created the organ of mind and provides the anatomy of conscious-

ness, making man ‘supreme amongst the paragon of animals’. But

Russell Brain is not comfortable with a formulation that elevates

the cortex as the seat of higher function detached from the unity

of the nervous system or from his preferred integrator of con-

sciousness: ‘is there any meaning in asking whether the cortex

or the diencephalon of an artist or a poet . . . is . . .‘‘higher’’ . . .we

should. . .

conceive of the relationship between these two parts ofthe brain . . .as an integrative unity . . . such as that represented by

the yin and the yang symbols of Taoism intertwined in their

self-embracing circle’. As papers in the present issue illustrate

(pages 2531 and 2541), consciousness and unconsciousness

remain enigmatic; and no more comprehensible to clinicians,

scientists and philosophers of the nervous system working now

than they were for Russell Brain writing in the 1950s.

Alastair Compston

Cambridge

Figure 2 Coronal section at the level of the anterior corpora

quadrigemina showing necrosis involving the tegmentum on

both sides and on the left side (the right in the figure)

extending ventrally to involve the medial one-third of the

substantia nigra and the medial one-fourth of the crus Loyez

stain.

From the Archives Brain 2009: 132; 2303–2305 | 2305

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2303The Cerebral Basis of Consciousness. by W. Russell