Elsevier

Cortex

Volume 45, Issue 5, May 2009, Pages 602-609
Cortex

Research report
Seeing the hand boosts feeling on the cheek

https://doi.org/10.1016/j.cortex.2008.03.008Get rights and content

Abstract

Tactile acuity improves when subjects look at the stimulated body part, even when vision does not provide any information relevant to touch. This “visual enhancement of touch” (VET), might involve modulation of primary somatosensory cortex (SI) processing by multimodal information related to the body. SI shows a characteristic somatotopic organization, with the face and hand represented laterally and adjacent to each other, and the foot represented more medially.

The aim of this study was to investigate whether VET is limited to the viewed body part, spreads to all body parts, or generalizes only to body parts represented in SI closely to the viewed body part. Tactile acuity was assessed in healthy subjects on the hand, face and foot, while subjects viewed either their stimulated hand, their foot or were blindfolded: viewing the hand, compared to blindfold condition, enhanced tactile sensitivity on the hand and also on the face, but not on the foot. Conversely, viewing the foot, compared to blindfold condition, improved touch only on the foot. Two control experiments assured this effect was due to viewing the body and not to directing visuo-spatial attention toward the location of tactile stimulation. The present results show that VET acts accordingly to a somatotopic gradient based on SI organization, suggesting that this multisensory effect may occur within SI. This finding might have a possible application to facilitate the recovery of tactile deficits in patients with a lesion of somatosensory cortices.

Introduction

Viewing the body can modulate tactile perception. Several studies showed that subjects are faster (Tipper et al., 1998, Tipper et al., 2001, Press et al., 2004) or more accurate in performing tactile tasks (Kennett et al., 2001, Taylor-Clarke et al., 2004, Serino et al., 2007) when looking at their stimulated body part, rather than at a neutral, non-bodily stimulus during tactile stimulation. Importantly, in these studies viewing the body did not provide any information relevant to the tactile task, since tactile stimuli were always invisible to the subjects. Instead, visual information related to the body might contribute to better define the context of tactile stimulation (i.e., the stimulated body part) thus enhancing primary tactile processing. This form of visual enhancement of touch (VET) might have also a possible application in the clinical field, since a recent study from our group showed that viewing the body enhances tactile performance in a population of brain damaged patients, selected for the presence of a somatosensory deficit (Serino et al., 2007). Thus, the effect of viewing the body might be useful for the rehabilitation of somatosensation after brain injury.

VET has been shown for different body parts, notably the arm (Kennett et al., 2001), finger (Taylor-Clarke et al., 2004) and face (Tipper et al., 2001). However, it is unknown whether the enhancement occurs only when viewing the specific body part that is touched, arises as a consequence of viewing any body part, which provides an arousing visual stimulus relevant to bodily sensation, or, finally, generalizes to other body parts, whose representations in somatosensory cortex (SI) overlap with the viewed body part. Answering this functional question could shed light on the functional characteristics of VET and on the brain mechanism subserving this effect. This information can be particularly useful to implement VET in rehabilitative programs for somatosensory deficits.

Indeed, the mechanism for VET could involve a modulation from brain regions representing the body onto primary somatosensory areas. Several brain areas, in pre-frontal, parietal (Lloyd et al., 2003, Ehrsson et al., 2004, Graziano, 1999, Graziano et al., 2000) and occipito-temporal (Downing et al., 2001, Downing et al., 2007) regions, are known to integrate visual, tactile and proprioceptive information specifically related to the body. These regions might project to primary somatosensory cortices modulating tactile processing. The modulation itself could occur in primary SI, since this area is responsible for tactile acuity (Brown et al., 2004). Accordingly, viewing the body enhanced SI evoked activity in electro-encephalography (Taylor-Clarke et al., 2002), and magneto-encephalography (Schaefer et al., 2005) studies. Moreover, transcranial magnetic stimulation over SI abolished VET (Fiorio and Haggard, 2005).

SI contains a characteristic body map or homunculus. The spatial organization of this map broadly follows the spatial layout of the body itself. Thus, neurons located close together in SI generally have receptive fields on adjacent parts of the body surface. An important exception is that the face and hand are both co-represented in a single lateral part of SI, rather than forming distinct representations (Penfield and Boldrey, 1937, Yang et al., 1993, Sato et al., 2005). Therefore, if VET occurs in SI, the visuo-tactile interaction underlying the effect might follow a specific somatotopic gradient.

To study this issue, we have tested tactile spatial sensitivity on the hand, face or foot of healthy volunteers, while they either viewed their hand, or were blindfolded (Experiment 1). An improvement of tactile spatial sensitivity when viewing the hand compared to the condition of no visual stimulation has been taken as an index of VET. The subjects were positioned so that the distance between hand and foot in external space matched the distance between hand and face. In this way, any effect due to the physical distance between viewed and touched body parts would be equal for the face and foot. We compared three alternative predictions. First, viewing any body part, might boost touch across the whole body surface (general enhancement hypothesis). If this is the case, viewing the hand should enhance touch on hand, foot and face. Alternatively, the cross-modal mechanism for VET might be body-part specific. That is, viewing a given body part might affect the response of SI neurons receiving input from that body part, but not the response of neurons receiving from other body parts (tuned neurons hypothesis). If this is the case, touch should improve only on the hand when viewing the hand. Finally, the enhancement might display the same somatotopic organization as SI itself, namely viewing a given body part would affect the response both of SI neurons tuned to that body part and of other neurons located in an adjacent SI region, even these neurons represent a different body part (SI organization hypothesis). In this case, viewing the hand should improve touch for both the hand and face, in virtue of their overlapping representations in SI, but not for the foot.

Section snippets

Subjects

Sixteen healthy subjects (six males, age 20–25, mean education 15 years of schooling), students from University of Bologna, participated to Experiment 1.

All subjects reported normal, or corrected to normal, vision and normal touch. They were naïve as to the proposal of the study. They gave their informed consent to participate to the study, which was performed with local ethical committee approval and in accordance to the Declaration of Helsinki.

Materials and procedure

Participants were seated in a dimly lit room with

Subjects

Ten naïve healthy volunteers participated in Experiment 2. Participants' gender, age and education (six males, age 21–30, mean education 14 years) were matched with those of Experiment 1.

Material and procedure

Materials, procedure and task were the same as in Experiment 1: subjects performed the 2PDT task on their right hand, right cheek and right foot. At variance with Experiment 1, in different blocks, subjects were requested to orient their head toward their stimulated foot: in one condition they viewed their foot

Subjects

A different group of 16 healthy naïve subjects, students from University of Bologna, participated to Experiment 2. Participants' gender, age and education (seven males, age 19–25; mean education 15 years) were matched with subjects of Experiment 1.

Materials and procedure

Materials, procedure and task were the same as in Experiment 1, with the following exceptions. Two-point discrimination task stimuli were delivered to the right hand only. Subjects viewed either a cardboard small box (30 × 20 × 10 cm) covering their hand

Subjects

Ten naïve healthy volunteers participated in Experiment 4. Participants' gender, age and education (three males, age 20–26, mean education 15 years) were matched with those of Experiments 1 and 2.

Material and procedure

Materials, procedure and task were the same as in previous experiments, with the following exceptions. Tactile stimuli were administered on the subjects' right foot. Subjects were requested to orient their head toward their stimulated foot: in one condition they viewed their foot (viewing foot, Fig. 1

General discussion

In the present study, we investigated whether VET acts according to a somatotopic gradient similar to the spatial organization of primary SI. Three alternative hypotheses were compared. Viewing a given body part might boost tactile sensation: (a) on all parts of the body (general hypothesis); (b) only on the touched body part (tuned neurons hypothesis), or (c) on body parts whose representations in SI overlap with the viewed body part (SI organization hypothesis).

To this aim, in Experiment 1,

Conclusion

Results from the present study suggest that viewing a touched body part induces a modulation of activity in the region of primary sensory cortex corresponding to the viewed body part. This signal spreads locally within adjacent representations in the SI body map, resulting in a somatotopic gradient of VET. This effect might have a possible application in the clinical practice to boost the recovery of somatosensory deficits due to lesions of primary somatosensory cortices.

Acknowledgements

We would like to thank Lena Schulte, for her help in data collection; and Augusto Ciaramelli for drawing the figures.

References (37)

  • M. Tanosaki et al.

    Tactile interference to the face affects magnetic responses elicited by electric thumb stimulation

    Clinical Neurophysiology

    (2003)
  • M. Taylor-Clarke et al.

    Vision modulates somatosensory cortical processing

    Current Biology

    (2002)
  • M. Taylor-Clarke et al.

    Persistence of visual–tactile enhancement in humans

    Neuroscience Letters

    (2004)
  • M. Brecht et al.

    Dynamic receptive fields of reconstructed pyramidal cells in layers 3 and 2 of rat somatosensory barrel cortex

    Journal of Physiology

    (2003)
  • P.E. Downing et al.

    A cortical area selective for visual processing of the human body

    Science

    (2001)
  • P.E. Downing et al.

    Functional magnetic resonance imaging investigation of overlapping lateral occipitotemporal activations using multi-voxel pattern analysis

    Journal of Neuroscience

    (2007)
  • J.R. Duhamel et al.

    Ventral intraparietal area of the macaque: congruent visual and somatic response properties

    Journal of Neurophysiology

    (1998)
  • H.H. Ehrsson et al.

    That's my hand! Activity in premotor cortex reflects feeling of ownership of a limb

    Science

    (2004)
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    This work has been supported by an MIUR grant to E.L.

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