Henry Head’s lifelong studies of cutaneous sensation

Background - early ideas on sensation

Cutaneous sensation is one of the five sensory modalities, touch, vision, hearing, smell and taste, recognised by Aristotle. Von Frey ⁴ described four primary cutaneous sensory modalities; touch, warmth, cold and pain. Pain differs, however, in that it arises from tissue damage, however slight. The notion of ‘cutaneous sensory modality’ derives from von Helmholtz ⁵ and Volkmann. ⁶ For example, punctate skin sensitivity to touch was described by Blix, ⁷ using a horse-hair, and similarly for temperature perception by Goldscheider. ⁸ Specific punkte for the four recognized cutaneous modalities were recognised in the 1890s, including schmerzpunkte for pain when testing at threshold intensity with fine needles. ⁴ Maximilian von Frey ^4,9 concluded that the four sensory modalities were each related to specific cutaneous receptors. He linked Pacinian corpuscles with pressure, Meissner corpuscles and basket endings around hair follicles with touch, Krause end-bulbs with cold, and Ruffini endings with warmth, leaving Merkel discs (hederiform endings) with an undetermined function. He thought pain was subserved by fine cutaneous nerve endings. Initial understanding of these four specific sensations, invoking Mueller’s Law of Specific Nerve Energies. ^{10 –12} Mueller ¹⁰ assumed direct central projections of modality-specific afferent nerve fibres to higher brain centres mediating conscious awareness. Nonetheless, how the psychophysical experience of the different sensations perceived in ordinary life was achieved was mysterious since it was evident that more complex sensory percepts, such as the ability to perceive weight, surface texture, recognition of objects, and qualities such as roughness, smoothness, liquid, wood, glass, and clothing, must be derived in some way from these four primary modalities. How could four specific sensory ‘modalities’ explain this? Head challenged these cable-like concepts of sensory connexions by introducing novel physiological concepts. ^13,14 He developed these ideas from a self-experiment involving nerve section. This, the first interventional study of human cutaneous sensation, was a unique and innovative landmark in science, ranking him as among the first of the modern clinician-neuroscientists. ¹⁵

Head’s novel theory of sensory perception was derived from his studies of returning sensation after nerve section and suturing. This represented a paradigm shift that caused a controversy that lingered for decades, ^14,16 until itself transformed by new ideas. ^11,17

Sir Henry Head MA MD FRCP FRS (1861–1940)

Head’s family were members of the Society of Friends, his father was an insurance broker at Lloyds and his mother’s family were vintners. ¹⁸ After schooldays at Charterhouse, where he excelled in Classics and Science, Head spent several months in 1880 at the University of Halle, learning colloquial German and studying histological methods. He proceeded to Trinity College, Cambridge, graduating in 1884 with a double first in Natural Sciences, and returned to central Europe to join Professor Ewald Hering (1834–1918) at the German University in Prague. There he worked on the technically difficult subject of respiratory reflexes (e.g., the Hering-Breuer reflex) leading to his first scientific publication - Head’s paradoxical reflex. ¹⁹ This work later became relevant to studies of the first breaths taken by infants. ²⁰ His experience of German science, of German musical and literary culture, and of the German language, profoundly influenced both his cultural tastes and his subsequent career. He returned to England in 1886 to study medicine at University College Hospital.

Head developed a lifelong interest in cutaneous sensation after working as House Physician at Queen Square, where he conceived the sensory system could be understood according to Jackson’s hierarchical ideas on the motor system. ¹⁴ During two years at the Victoria Park Hospital for Diseases of the Chest, he studied referred sensory symptoms associated with visceral pain ^{21 –23} and then, at the Rainhill Asylum, studied the sensory and pathological features of spinal root lesions due to Herpes Zoster infection (Figure 1). ²⁴ This gave rise to a map of the distribution of the cutaneous innervation of the human dorsal spinal roots that, taken with earlier work by Sir James Mackenzie, and Foerster’s later confirmatory studies, ²⁵ transformed clinical diagnosis. In 1896, after only 4 months as Registrar, he was appointed Assistant Physician to the London Hospital, to a vacancy following Hughlings Jackson’s retirement from active practice in 1894 under the London’s 20-year rule. Head’s clinical practice and teaching was characterized by a legendary insistence on accuracy in clinical assessment and in presentation of cases at the bedside. His examination of patients was almost obsessional, seeking precision in questioning his patient or in the physical examination. His teaching, always well prepared, was enthusiastic, clear and popular. Outside medicine he had wide-ranging interests and he and his wife were closely involved in contemporary artistic and literary trends. ^15,18 He was entertaining and stimulating in conversation, reflecting his wide knowledge and experience. ^18,26 Like Sir Charles Sherrington and Lord Brain, he published several small volumes of verse. ²⁷ These scientific and cultural interests continued after his retirement in 1919 with Parkinson’s disease. His work on sensation and its disorders, his studies of aphasia, and his work in the First World War on spinal injuries, especially on the automatic bladder with George Riddoch (1888–1947), his successor at the London Hospital, remain defining studies.

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Figure 1.

An offprint ²⁴ from Brain with Head’s annotation to “RM”. The inscription in English (with interposed Greek [Gk] and Latin words, rarely used in English, but listed in the Oxford English Dictionary) reads “Herein we’ve settled Hoti’s business - Properly based oun - given the doctrine of the Euclitic De”. (Hoti [Gk] – an assertion; oun [Gk] - accordingly, consequently; Euclitic De – a religious or emotionally held concept; De - about God). One senses here a glimpse of Head’s personality?

WHR Rivers MA MD FRCP FRS (1864–1922)

Rivers qualified in medicine from St Bartholomew’s Hospital in 1882. He travelled widely as a ship’s surgeon, then as House Physician at Barts in 1889, and at Queen Square in 1890. He was enthused by anthropology and psychology following a visit to Kaepelin in Heidelberg, and at Jena. In 1891 he was appointed as medical psychologist at the Bethlem Hospital. He lectured on psychology at UCH and Barts and, in 1893, Professor Sir Michael Foster, who had come to recognise the validity of psychology as a research subject allied to physiology, appointed him as Lecturer in “physiology of the sense-organs” at St John’s College, Cambridge. In 1898 he undertook psycho-anthropological studies with the Torres Straits Expedition, and then in 1901–1902, with the Toda people in the Nilgiri Hills, Tamil Nadu, and in 1907–1908 the Melanesian peoples of the Solomon Islands. These studies led to publications that secured his academic reputation, leading to his foundational role in the academic discipline of human psychology in Britain. In 1902 he was elected to a Fellowship at St John’s and from 1903 he collaborated with Head in studying the recovery of sensation after peripheral nerve lesion. During a period of nearly 5 years they worked together (Figure 2) in Rivers’ rooms at St John’s at weekends, away from Head’s busy clinical practice at the London Hospital. Later, during and after the First World War, Rivers’ psychological experience was influential at the Craiglockhart War Hospital in the rehabilitation of soldiers with war neuroses (shell shock). ²⁸

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Figure 2.

Head and Rivers at St John’s College, Cambridge. Note the plaster model of Head’s arm and the concentrated air of the two experimenters (London Hospital Archives).

Head’s novel concepts of cutaneous sensation

Rivers and Head ¹³ studied the pattern of returning sensation to different types of sensation in Head’s forearm following surgical section and resuture of the dorsal cutaneous sensory branch of his left radial nerve. This operation was carried out by Head’s surgical colleague at the London Hospital, Mr Dean, at Dean’s home, assisted by Mr James Sherren, also a London Hospital surgical colleague, on April 25th 1903. That Head chose a colleague with psychological and neurological expertise for the work of sensory testing is probably due to his experience of the psychological effects of visceral pain. ^{21 –23} The clinical testing procedure (Figure 2) was precise but onerous. It continued during a period of 4 years and 8 months, until December 13th 1907, in 167 separate all-day sessions. Further, in 1908 Head re-visited von Frey in Wurzburg so that von Frey could himself examine Head’s forearm, and he could learn von Frey’s views on his theories (p819). ¹⁴ Head’s observations were essentially introspective, and subsequent critics concluded that the dualist concept of cutaneous sensation he developed lacked independent anatomical or behavioural corroboration. ¹⁶ Indeed, there was difficulty exactly replicating some aspects of his findings. ^8,29,30

It was from this detailed study that the concept of protopathic and epicritic sensibilities entered the neurological vocabulary where, in some respects, it has remained embedded. In essence, Head explained his psychophysical experience during Rivers’ repeated sensory examinations by conceiving novel physiological systems within peripheral sensory nerves. Epicritic sensibility, subserving light touch, temperature discrimination and precise localization of tactile stimuli was conceived as controlling and holding in check protopathic sensations, that consisted primarily of extremes of temperature, and pain. ^13,14 Deep sensibility, a third form of sensation independent of cutaneous receptors, was also recognised.The protopathic/epicritic dualist concept did not sit comfortably with the four modalities enshrined in the psychophysics of sensory investigation by von Frey, ⁷ but Brown-Séquard’s separation of spinothalamic and posterior column sensibilities ^2,3 was reminiscent of Head’s dualist concept, even if there was dubious logical utility in combining evidence based on spinal cord pathology with Head’s two-system theory of sensation. The latter was derived from a regenerating peripheral nerve lesion, not CNS pathology, as forcefully emphasized by Walshe in his devastatingly critical review, ¹⁶ published after Head’s death. Head’s observations after nerve injury, therefore, did not reflect normal function in a peripheral sensory nerve, or even its return. ^14,16,26 A particular criticism was that Head was unaware of the regenerative potential of undamaged nerve fibres derived from nearby nerve fibres sprouting into the denervated area of skin. ^29,30 His clinical sensory observations, nonetheless, were precise and important in signifying recovery, as even Walshe was at pains to note. ¹⁶ Descriptions of patients with various traumatic nerve lesions led to an expansion of Head’s theoretical ideas, ^{31 –33} and emphasized the importance of central processing of afferent information by the brain. ^5,34,35 In considering Head’s work more than 100 years later it is salutary to reflect on the absence of any of the now universally available ancillary aids to diagnosis. The only basis for diagnosis and research at that time was clinical examination (Figure 3).

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Figure 3.

Head’s out-patient consulting room at the London Hospital about 1900. Note the urine testing bench at the back with Snellen’s visual acuity chart. Head sat in the chair occupied by the nurse in the picture, and his patient on the stool. The room is lit by a gasolier and to modern eyes appears dark and uninviting (London Hospital Archives).

What assessments did Rivers and Head make?

The comfortable arrangement in Rivers’ rooms at St John’s College, Cambridge is shown in Figure 2. Head closed his eyes during the examinations, ‘in order to avoid any distraction or false impressions’. ^13,14 A precise testing protocol was followed. A metal bar warmed in a hot water bath was used to test thermal sensation, a pin to test pain and a wisp of fine cotton wool for touch and tactile movement across hairy skin, taking care to avoid causing pressure deformation of the skin. ^13,14 They tested and timed vibration perception with a tuning fork, and measured threshold to two-point discrimination with a pair of compasses (dividers). Rivers drew the evolving sensory changes on Head’s arm week by week, using India ink, and photographed the results. They mapped the return of sensory spots to touch, temperature and pain, and commented on their fatigability and their variation from week to week. They quantified light touch at different tactile forces using a set of von Frey hairs prepared by von Frey himself (Figure 4). ¹⁴ Von Frey had calibrated the set of test hairs by measuring the pressure required to bend each hair on a balance and dividing the result (gm) by the total area of the tip of the hair, giving pressure/unit area. This value was then divided by the radius of a circle corresponding to the elliptical cross-section of the tip of the hair, giving tension/mm; this was the measure recommended by von Frey, whom Head had visited at Wurzburg. ¹⁴ Rivers and Head ¹³ noted that ‘protopathic’ sensibility returned before ‘epicritic’ sensibility. The experimental method was therefore essentially a subjective psychophysical description, without possibility of independent corroboration, and coloured by Head’s personality as the sole respondent.

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Figure 4.

(a) The travelling case of von Frey hairs, prepared by Professor Maximilian von Frey, of Wurzburg, for Head’s 1903 experiment. ¹³ The metal case is covered in a sturdy red linen fabric - black on the back – and is kept closed with a simple brass sliding pin system at the right lower corner. On the front it is stamped “C. ZEISS JENA.” (b) The hairs are porcine bristles. Each hair is labelled in gm/mm² representing the bending strain required to generate a sensation of touch. Red postal sealing wax fixes each hair to its roughly made wooden holder. A black silk edging to the closing surfaces of the box has worn away. The background to each compartment is a roughly shaped piece of white card. Head acknowledged the provenance of this test system in a footnote on page 16 of his book ‘Studies in Neurology’. ¹⁴

Conceptualising sensory systems

Further understanding of sensory systems arose not from repeated clinical studies, or from intellectual critiques of Head’s work but from electrophysiological exploration of the nervous system, a method unknown in Head’s time. Erlanger and Gasser ³⁶ working at Washington University in St Louis, Missouri, found that nerve conduction velocity was correlated with nerve fibre size, and that unmyelinated fibres conducted much more slowly than myelinated fibres. ³⁷ They classified peripheral nerve fibres as Aα, Aβ, Aδ, B and C types, according to their markedly differing conduction velocities. These differences in a sensory nerve implied hitherto unrecognised specificity between peripheral receptors and the spinal cord. ^38,39 Further complexity is introduced, for mechanoreceptors, by fast or slow adapting properties, sensitive respectively to deformation of skin, or to continuous mechanical stimulation. Fast adapting receptors conduct through fast A fibres, but some slowly adapting mechanoreceptors conduct through C fibres. Vibration is dependent on rapidly adapting Pacinian corpuscles in deeper tissues. ¹¹ Thermoreceptors, also conducting through C fibres, respond in relation to skin temperature, i.e., warm or cool stimuli are not absolute measures of temperature. Pain is perceived through C fibre networks in the dermis, as well as by excessive stimulation of other receptors. ⁴⁰ Pain receptor biology is complex, with specific sensitivity to various kinds of painful stimuli. It is the mix of sensory information arising from these receptors that is sorted in the spinal cord for projection to the brain. In human subjects microneurographic recordings have confirmed the specificity of sensory afferents, while allowing brain synthesis of multiple inputs to construct sensory percepts’ in consciousness ⁴¹ and real-time integration of information from tactile afferents in manipulation of objects between the fingers. ⁴²

Head, ^13,14 of course, was unaware of these features of the peripheral sensory nervous system. Clinical experience nonetheless suggested that the central nervous system, principally thalamus and cortex, modulated sensory perception and with Gordon Holmes, he devoted much thought to this problem. ⁴³ Melzack and Wall ^17,44 subsequently suggested that small and large fibre sensory input to the spinal cord was gated or, at least, partially sorted in the dorsal horns, on the basis of the earlier arrival of fast-conducting afferents, thus leading to the distinctive, if partial, separation into the two ascending spinal sensory pathways. ⁴⁴ This modern conception of the dual system of spinal sensory afferents owed much to Head’s posited epicritic and protopathic systems. Their lingering occasional usage by clinical neurologists is therefore not entirely inappropriate. In addition, Head ¹⁴ developed a theoretical concept of central sensory projections to explain the abnormal positive and negative sensory experiences seen in clinical practice, set against a notion of a cerebral ‘schema’ of perception, built and modified by ongoing sensory experience, that represented a state of sensory consciousness. ^45,46 In seeking to understand Head’s attempt to develop a general theory of human cutaneous sensation one must remember how powerful was the influence of Hughlings Jackson’s hierarchical concept of the organisation of the nervous system, with its notion of a cortical synthesis of movement, an influence that Head freely acknowledged. ¹⁴ The self, he thought, is constructed on the basis of the present in the context of past experience. ¹⁴ In summarising his ideas he wrote (page 831) ¹⁴ that sensory:

“impressions are sorted, combined and controlled within the central nervous system until they are sufficiently integrated to underlie sensation: the final product is simpler than its constituent elements. There are no basic physiological activities corresponding to ‘primary sensations’. The afferent impressions produced by the action of an external stimulus are highly complex, and are subject to the integrative action of the central nervous system before they can become fitted to subserve sensation.”

The author has received no financial support or other inducement in the writing of this paper.

The material in this paper has not been submitted or published elsewhere.

The illustrations are taken from objects and images in the author’s personal collection. Figure 2 is reproduced by permission of the Archives of the Royal London Hospital.