Welcome to the touch dome!

ThisHistorical Perspective article celebrates the 600th volume of The Journal of Physiology, recognizing the most highly cited papers published in the Journal. Here I discuss the significance of a landmark study published in 1969 by Ainsley Iggo and Alan Muir, from the Departments of Anatomy and Physiology at The University of Edinburgh. A graduate of Otago University in New Zealand, and having received training in neurophysiology under the tutelage of Jack Eccles, Iggo arrived in Edinburgh (after a 2-year stint in Aberdeen) in 1952 (Iggo, 2001). The paper of interest here, titled The structure and function of a slowly adapting touch corpuscle in hairy skin, built on his work with Muir (his student) in which they had characterized the ‘touch dome’ mechanoreceptors in the hairy skin of the cat. After shaving the hairy skin these domes can be readily seen as punctate elevations of the epidermis, which are usually (but not always) associated with a single hair. The sensory axons that supply these endings are known as the slowly adapting type I (SAI) afferents, and histological evidence showed that the mechanoreceptors are the Merkel cell receptors, now known asMerkel cell–neurite complexes. SAI afferents possess small, well-defined receptive fields composed of several ‘hot spots.’ Iggo and Muir showed that each touch dome is innervated by a single myelinated axon that branches to end as Merkel discs, although a given parent axon can supply several touch domes. Subsequent work in humans, in which single-unit recordings were made via tungsten microelectrodes inserted into the lateral antebrachial cutaneous nerve, demonstrated that the receptive fields of SAI afferents in hairy skin are composed of two to four ‘hot spots’ of maximal sensitivity, each no doubt corresponding to the location of the receptor terminal from a single axon that branches from the parent axon (Vallbo et al., 1995). In the glabrous skin of the hand there are no touch domes; here, the Merkel cell–neurite complexes are associated with the patterned elevations of the epidermis that form the fingerprint ridges. Nevertheless, the receptive fields of these SAI afferents are composed of several distinct subfields spread across multiple ridges, such that the receptor endings underlying each of these ‘hot spots’ can detect mechanical events at individual fingerprint ridges (Jarocka et al., 2021). Iggo and Muir performed an extensive analysis of the physiology of the ‘touch spot’ receptors. Earlier studies by Brown and Iggo (1963) demonstrated that, after crushing the parent nerve, the characteristic slowly adapting discharge of the afferent only returned once the axon had regrown into the touch dome and the Merkel cell complex had reformed. Iggo and Muir showed that while the receptors responded well to punctate indentation of the touch dome, they were particularly sensitive to light stroking across the receptive field, a feature exhibited by SAI afferents recorded in humans. And, like human SAI afferents, these slowly adapting receptors in the cat do not exhibit a spontaneous discharge in the absence of ongoing mechanical stimulation. This is in contrast to another class of slowly adapting receptor that Iggo and his team were investigating, which often was spontaneously active. The latter they referred to as SAII (slowly adapting type II) afferents, to differentiate them from the ‘touch spot’ afferent units (SAI). SAII afferents have a much lower dynamic sensitivity to indentation forces than the SAI afferents, and during the static phase of an applied compressive force exhibit a very narrow range of interspike intervals. And, unlike the SAI afferent, the SAII has a single zone of maximal sensitivity; the same is true for these receptors in humans (Vallbo et al., 1995). Histological evidence would identity the Ruffini ending – a spindle-shaped structure oriented parallel to the skin surface and with a single large myelinated axon – as the mechanoreceptor responsible for the SAII afferent’s firing properties, including its sensitivity to lateral skin strain. These findings were described in a paper published in our sister journal, Experimental Physiology, which at the time was known as The Quarterly Journal of Experimental Physiology (Chambers et al., 1972). One of the conclusions that Iggo and Muir made from their study was that there is modality specificity in tactile afferents, as evidenced from the different firing properties of the SAI and SAII afferents, and that this is determined by structural differences in the mechanosensitive endings themselves – not the spatiotemporal code of impulses conveyed by the sensory axons. In other words, there was a ‘labelled line’ of sensory information from tactile afferents (indeed, from all afferents in the somatosensory system) such that the brain ‘knows’ from where the sensory information originated because of the structural and hence functional differences across afferent species. However, this conclusion has been questioned. For example, it was recently shown that the temporal pattern of afferent spikes does indeed provide information on the quality of a mechanical stimulus: percepts of vibratory flutter – attributed to the inputs of fast-adapting type I (FAI) afferents, which innervate Meissner corpuscles – can be induced by selective stimulation of fast-adapting type II (FAII) afferents, which innervate the Pacinian corpuscles, with a low-frequency stimulation pattern (Birznieks et al., 2019). In other words, the spatiotemporal pattern of impulses in a single tactile afferent can provide the brain with potentially ambiguous information. Of course, one has to accept that the physiological transduction of a mechanical stimulus into this train of impulses is dependent on the specializations of the mechanoreceptor and its microenvironment, and this was another contribution Iggo and Muir made in their paper. The authors provided a rich histological analysis of the Merkel discs and associated Merkel cells. They showed that the surface