Tactile distance adaptation aftereffects do not transfer to perceptual hand maps

Highlights

• Perceptual hand maps have distorted structure toward medio-lateral hand axis.

• Similar perceptual distortions are observed for tactile distance perception on hand.

• Repeated tactile distance stimulation induces tactile distance aftereffect on hand.

• We found that this adaptation aftereffect had no effects on the perceptual hand maps.

• Distinct body representations may underlie the tactile perceptual distortions.

Abstract

Recent studies have demonstrated that mental representations of the hand dorsum are distorted even for healthy participants. Perceptual hand maps estimated by pointing to specific landmarks (e.g., knuckles and tips of fingers) is stretched and shrunk along the medio-lateral and the proximo-distal axes, respectively. Similarly, tactile distance perception between two touches is longer along the medio-lateral axis than the proximo-distal axis. The congruency of the two types of distortions suggests that common perceptual and neural representations may be involved in these processes. Prolonged stimulation by two simultaneous touches having a particular distance can bias subsequent perception of tactile distances (e.g., adaptation to a long distance induces shorter stimuli to be perceived even shorter). This tactile distance adaptation aftereffect has been suggested to occur based on the modulations of perceptual and neural responses at low somatosensory processing stages. The current study investigated whether tactile distance adaptation aftereffects affect also the pattern of distortions on the perceptual hand maps. Participants localized locations on the hand dorsum cued by tactile stimulations (Experiment 1) or visually presented landmarks on a hand silhouette (Experiment 2). Each trial was preceded by adaptation to either a small (2 cm) or large (4 cm) tactile distance. We found clear tactile distance aftereffects. However, no changes were observed for the distorted pattern of the perceptual hand maps following adaptation to a tactile distance. Our results showed that internal body representations involved in perceptual distortions may be distinct between tactile distance perception and the perceptual hand maps underlying position sense.

Introduction

We can effortlessly perceive the size and position of objects touching our body. If a spider lands on a hand, one can immediately perceive its size and location on the skin surface, even with eyes closed. Then, you could try to swat the spider with the opposite hand by estimating its spatial location in space. However, the estimation of tactile size on the body surface and the location of touch in external space are not simple processes. Longo, Azañón, and Haggard (2010) proposed a model of somatoperceptual information processing postulating that the location of touch is localized on the skin surface by referring touch to the superficial schema, which is a static mental representation mediating localization of somatic sensations on the body surface (Head & Holmes, 1911). This representation is assumed to be distinct from another form of body representation (the postural schema), which is a dynamic representation of the position of the body in space (Head & Holmes, 1911). A third body representation (the model of size and shape) was introduced by Longo et al. (2010) to describe a static, stored mental representation of the body size and shape. Notably, according to this somatoperceptual processing model, the model of size and shape) is needed both to estimate the metric properties of touch (e.g., the size of the spider, or distance between its legs) and to locate touches or body parts in space (see Fig. 1).

Intriguingly, a large body of research has demonstrated similar patterns of perceptual distortions for tactile distance perception and perceived locations of body landmarks or touches in space (for reviews see Longo, 2015, Longo, 2017a). For example, in the case of tactile distance perception, Longo and Haggard (2011) reported that the perceived distance between two touches on the hairy skin surface of a hand (hand dorsum) is approximately 40% longer when the stimuli are aligned with the medio-lateral axis (across the hand) compared to the proximo-distal axis (along the hand).

Similar distortions have been reported for perceived locations of body landmarks in space. For example, Longo and Haggard (2010) asked participants to judge the location of the knuckles and tips of their fingers by placing the tip of a long baton on a board on top of the occluded hand. Using the relative relationships among the judged landmarks, Longo and Haggard (2010) depicted an implicit geometric structure of the hand underlying position sense (hereafter, perceptual hand maps). They found that the shape of these maps were stretched toward the medio-lateral axis and shrunk along the proximo-distal axis, similar to the pattern of distortions found for perceived distances on the dorsum of the hand. Similar distorted patterns have been observed for perceptual hand maps estimated by localisation of locations cued by visual markers on a hand silhouette (Longo, Mancini, & Haggard, 2015), by touch (Longo, 2017b; Longo et al., 2015; Longo & Morcom, 2016; Mattioni & Longo, 2014), and by verbal estimates of the perceived distance between two sequential touches applied to the hand (Longo & Golubova, 2017). The similar patterns of perceptual distortions obtained for tactile distance perception and perceived locations of body landmarks or tactile localization on the hand, might imply the use of a common internal “distorted” body representation (a model of size and shape). However, Longo and Morcom (2016) found that magnitudes of the perceptual distortion toward the medio-lateral axis in tactile distance perception and localization permeances on the hand dorsum were not positively correlated. They proposed that the internal body representations underlying perceptual distortions might be distinct for tactile distance perception and perceptual hand maps. However, it is also possible that an internal body representation is shared but obscured, given that task demands and resulting response patterns are distinct for tactile distance perception and perceptual hand maps underlying position sense. Further investigation is therefore required to test whether there is a common internal body representation underlying distortions for tactile distance perception and perceptual hand maps by using a single measurement.

For this purpose, the current study focused on perceptual adaptation aftereffects. Adaptation has been extensively used to induce perceptual changes, and in principle, modulate neural responses for particular attributes of a stimuli. For example, after prolonged exposure to a haptic object of a particular size (e.g., a large ball), subsequent smaller objects are perceived even smaller (Kappers and Bergmann Tiest, 2013; Maravita, 1997; Uznadze, 1966). Recently, Calzolari, Azañón, Danvers, Vallar, and Longo (2017) reported that adaptation to tactile distances produces corresponding aftereffects. They stimulated the participants' hand dorsum with long (4 cm) or short (2 cm) tactile distances with a two-points stimulus. Repeated stimulation of 60 s (each stimulation is around 1 s) was initially applied and 10 s top-up stimulations were introduced to maintain the effects. After adaptation, perceived tactile distance changed on the stimulated skin surface such that the long adaptation stimulus induced the perception of a subsequent distances to be perceived shorter than it is and vice versa for the shorter adaptation stimulus. It is also notable that the adaptation to the long distance on the medio-lateral axis cancelled the perceptual distortion of tactile distance (i.e., distances on the medio-lateral axis perceived larger than those on the proximo-distal axis) so that the distance perception across the medio-lateral and proximo-distal axes became more similar. Furthermore, tactile distance adaptation aftereffects did not transfer across different orientations or even across regions within the hand. Such selectivity suggests that tactile distance adaption aftereffects might induce changes in relatively early perceptual and neural somatosensory processing (Calzolari et al., 2017).

If a common internal representation (the model of size and shape) is involved in the emergence of distortions both for tactile distance perception and for perceptual hand maps underlying position sense and if adaptation could affect this internal representation, then adaptation to tactile distances might modulate both tactile distance perception and perceptual hand maps. To test this possibility, we repeatedly presented a long or short tactile stimulus to induce tactile distance adaptation on the participant's hand dorsum (Fig. 2A). In addition to the tactile distance judgment task used to measure adaptation aftereffects (Fig. 2B), we asked participants to localize either a tactile event on the hand (Experiment 1) or a proprioceptive location on the hand cued through vision (Experiment 2; Fig. 2C) after adaptation (localization tasks). If a common internal body representation underlies both the distortions of tactile distance perception and the perceptual hand maps underlying position sense, we would predict that the long and short adaptation along the medio-lateral axis would result in smaller and larger magnitudes, respectively, of the perceptual distortion toward the medio-lateral axis of perceptual hand maps. However, we found no effects of the tactile distance adaptation on the patterns of perceptual distortions on the implicit geometric structure of the hand estimated by the localization tasks in both experiments, indicating that tactile distance adaptation aftereffects do not transfer to the perceptual hand maps underlying position sense.