Thresholds of cutaneous afferents related to perceptual threshold across the human foot sole

Journal of Neurophysiology 114(4)　2144–2151:jn.00524.2015 · August 2015

Abstract

it is well established that cutaneous feedback from the soles of the feet is fundamental in the control of upright stance. Previous work has shown foot sole cutaneous feedback to play a role in standing balance (Roll et al. 2002), gait (Eils et al. 2004; Perry et al. 2001), automatic postural adjustments (Inglis et al. 1994; Perry et al. 2000), as well as in the modulation of lower (Fallon et al. 2005) and upper limb (Bent and Lowrey 2013) muscle activity and vestibular reflexes (Muise et al. 2012). What remains unclear is the capacity of individual types of foot sole cutaneous afferent classes to transmit distinct tactile cues to the central nervous system and what impact this feedback has on balance control.

Tactile sensibility from the glabrous skin of the foot sole and hand arises from four classes of low-threshold cutaneous mechanoreceptors located in the dermal and epidermal layers of the skin. Each class is sensitive to unique features of tactile stimuli and demonstrate distinctive firing characteristics in response to indentation forces, skin stretches, textures, and vibrations (Aimonetti et al. 2007; Johansson et al. 1982; Johnson and Hsiao 1992). Cutaneous afferent firing characteristics and receptive field (RF) properties establish the classification of each subtype as fast adapting (FA) or slowly adapting (SA), and type I (small, distinct borders) or type II (large, undefined borders). The development of microneurography by Vallbo and Hagbarth in the 1960s allowed for the direct comparison between primary afferent activity and perceptual experience (Hagbarth and Vallbo 1967). Pioneering work in the hand found light touch perceptual threshold to most closely resemble the firing thresholds of FA afferents (Johansson and Vallbo 1979). In the most sensitive hand regions (fingers and lateral border), a small amount of activity from FAI afferents, even single spikes, was capable of evoking a percept. Further support for a one-to-one relationship between afferent firing has been demonstrated through the electrical microstimulation of individual cutaneous afferents. Using this technique, researchers have demonstrated that specific tactile sensations can be evoked from the activity of single cutaneous afferents, e.g., flutter (FAI), vibration (FAII), and pressure (SAI) (Macefield et al. 1990; Ochoa and Torebjörk 1983). These findings are in line with the lower envelope principle in that perception can be set by minimal activity in the most sensitive afferents (Parker and Newsome 1998).

Previous work that has investigated tactile perception has focused almost exclusively on cutaneous feedback from the hand. The fingers have been shown to have lower perceptual thresholds compared with the palm, despite similar afferent firing thresholds (AFTs) between these regions (Johansson and Vallbo 1979). This led the authors to postulate that cutaneous feedback is not weighted equally across the body, and that central mechanisms may integrate input from the fingertips with more fidelity than the palm of the hand. The higher density of afferents in the fingertips may increase the probability of activating highly sensitive afferents leading to the disparity in perception between these regions. However, Johansson and Vallbo (1979) argued this was not the case since subsensory stimuli at the palm still evoked firing in cutaneous afferents. Their investigation suggests that perceptual threshold can be set by the firing capacity of the most sensitive primary cutaneous afferents in some regions (e.g., in the fingers) while additional factors may raise perceptual threshold in less sensitive skin regions (e.g., in the palm).

The soles of the feet are not as sensitive as the hands, where in the feet, both perceptual thresholds (Hennig and Sterzing 2009) and cutaneous AFTs (Kennedy and Inglis 2002) are reportedly higher. Perceptual threshold differences have been reported across the foot sole (Hennig and Sterzing 2009; Kekoni et al. 1989; Strzalkowski et al. 2015) while mechanoreceptor density is thought to be evenly distributed (Kennedy and Inglis 2002). A direct comparison between foot sole cutaneous afferent firing and perceptual sensitivity has not been made at the foot sole, and the neural mechanisms underlying regional differences in perceptual threshold are not well understood.

Mechanical properties of the skin have been shown to differ across the sole of the foot (Strzalkowski et al. 2015) and between the foot sole and hand (Hoffmann et al. 1994). The ability of skin to deform and transmit force will presumably impact afferent firing, and differences in skin properties have been proposed to account for disparities between cutaneous afferent firing and perceptual thresholds between these regions (Kekoni et al. 1989; Kennedy and Inglis 2002; Kowalzik et al. 1996). While an attempt has been made to link mechanical properties with afferent firing in the glabrous skin of raccoons (Pubols and Pubols 1983), and with perceptual threshold in the foot (Strzalkowski et al. 2015), the influence of skin mechanics on the actual firing of foot sole cutaneous afferents has not been investigated.

The aim of the present study was to investigate the relationship between tactile perceptual threshold and cutaneous AFTs across the human foot sole. Skin hardness within each afferent's RF was also investigated to better understand the potential influence of skin mechanics on afferent firing and perceptual threshold. In following with previous work in the hand, FA afferents were expected to be more sensitive to light touch (i.e., fire at lower forces) compared with SA afferents, and have firing thresholds most similar to perceptual thresholds across the foot sole. AFTs are expected to increase with skin hardness and, at least partially, account for perceptual threshold differences across the foot sole.