doi:10.

1093/brain/awp218 Brain 2009: 132; 2303–2305 | 2303

BRAIN
A JOURNAL OF NEUROLOGY

FROM THE ARCHIVES

The cerebral basis of consciousness. By W. Russell Brain. Brain 1950: 73; 465-479; and The physiological basis of
consciousness. 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

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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 its
whereabouts, 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 Figure 1 Walter Russell Brain, first Baron Brain (1895–1966).
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 ability to remember that he ever possessed a[nother] half of the
body, mainly sensorily, in relation to one another . . . [they] are body’. It follows that, in this situation, the intact cortex has
centres of universal coordination . . . or synthesizing centres’. adjusted and accepts that the half-body of which it is aware is
These cortical centres are no more than nodal points for onward now the whole. Taking forward his argument, Russell Brain reflects
distribution of sensory stimuli. Searching for an anatomical sub- on the observation of William Grey Walter (1910–77) that visual
strate to these nodal points, physiologists have identified area 1 in imagery reproduces electroencephalographic alpha rhythms
the post-central cortex which, other than for the face, has strictly identical to those observed when subjects view a real object,
contralateral representation, and area 2 that registers both sides of indicating that imagination and reality deploy the same neuronal
the body but with a preference for crossed structures. networks. Karl Lashley (1890–1958) has shown that blind animals
These principles are nicely illustrated by the clinical condition of trained to navigate a maze lose their way when the visual cortex is
anosagnosia in which loss of sensation is combined with failure to removed. Following head injury with frontal lobe damage, one of
recognize that the affected part exists at all: ‘we can only miss Russell Brain’s patients with ‘loss of revisualization’ could recognize
something if we remember that we once had it . . . the lesion in people, even after brief acquaintance, but never visualize them;
such cases has destroyed not only the patient’s present awareness nor could he remember details of a building plan (his trade)
of his body-image but also neurones which are essential to his without constant reference to the architect’s plans, or routes

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2304 | Brain 2009: 132; 2303–2305
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 widespread
neural 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 and
other 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
From the Archives
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
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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; and
physiological 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 any
particular 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
From the Archives
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.
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 minimal
pyramidal 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 peaceful
sleep. 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
Brain 2009: 132; 2303–2305 | 2305
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
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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 integrated
primarily 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 of
the 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