Elsevier

Consciousness and Cognition

Volume 20, Issue 3, September 2011, Pages 603-617
Consciousness and Cognition

The tickly homunculus and the origins of spontaneous sensations arising on the hands

https://doi.org/10.1016/j.concog.2010.11.013Get rights and content

Abstract

Everyone has felt those tingling, tickly sensations occurring spontaneously all over the body in the absence of stimuli. But does anyone know where they come from? Here, right-handed subjects were asked to focus on one hand while looking at it (convergent focusing) and while looking away (divergent focusing) and subsequently to map and describe the spatial and qualitative attributes of sensations arising spontaneously. The spatial distribution of spontaneous sensations followed a proximo-distal gradient, similar to the one previously described for the density of receptive units. The intensity and spatial extent of the reported sensations were modulated by the focusing condition, especially in respect of the left hand. Convergent focusing acted upon the conscious perception of sensations by enhancing or suppressing them. To our knowledge, this is the first ever study of spontaneous sensations, and it offers considerable insight into their sources. The presence of the proximo-distal distributional gradient is a clear sign that receptive units are involved. The enhancement/suppression effects also confirm the involvement of attention. Finally, left-hand dominance suggests several right-hemisphere processes may be involved, such as spatial and tactile perception, and probably interoception.

Introduction

Everyone knows what it is like to feel spontaneous sensations (SPS), those tingling, tickly and other sensations usually perceived during periods of rest and without external triggers. But, does anybody know what causes them? To date, this question has never been investigated, even though there are good reasons to think they are the result of an interaction of several different factors. This study is a first step forward.

The fact that SPS occur all over the body and feel similar to sensations driven by external events and those received from inside the body suggests the skin and musculoskeletal apparatus (joints, tendons and muscles) as major sources. Mechanoreceptors (Johnson, 2001) and thermoreceptors (Green, 2004) are scattered over the surface of the body, producing an uneven distribution of tactile (Weinstein, 1968) and thermal (Stevens & Choo, 1998) sensitivities. The densities of cutaneous receptors also vary at local levels. As far as hands are concerned, there is considerable evidence that tactile (Johansson and Vallbo, 1979, Vallbo and Johansson, 1984) and thermal (Li, Petrini, Defrin, Madeleine, & Arendt-Nielsen, 2008) sensitivities are not the same all over, and yet combining the distribution of all the different types of receptors with that of joint receptors, muscle spindles and Golgi tendon organs (Burke, Gandevia, & Macefield, 1988) produces a proximo-distal gradient. There is an impressive accumulation of receptive units in the fingertips, but their density diminishes sharply over the rest of the fingers, and less sharply thereafter in the palm of the hand. Psychophysical studies have shown that, at least for tactile perception, sensitivity as assessed via various stimulus detection and discrimination procedures follows this gradient (Johansson and Vallbo, 1979, Vallbo and Johansson, 1976, Vallbo and Johansson, 1978). Most of the aforementioned receptive units show spontaneous activity at rest and at room temperature (Hulliger et al., 1979, Johansson and Vallbo, 1979, Knibestöl, 1975, Macefield et al., 1990, Ochoa and Torebjörk, 1983). One study even evidenced spontaneous ongoing activity in itch fibers as paralleled to intense localized itching (Schmelz et al., 2003). Could it be that SPS stem from the spontaneous activity of receptors? If so, two patterns of results were to be expected: (a) like the receptors, spontaneous sensations would be distributed over the whole hand, and (b) like the receptors, the densities would follow a proximo-distal gradient.

Studies focusing on the perception of sensory events offer several lines of evidence showing that attention is a prerequisite for their conscious perception (Posner, 1994). For instance, given the close relationship between attention and eye movements (Rizzolatti et al., 1987, Shepherd et al., 1986), it not surprising that directing one’s eyes towards the stimulated part of the body causes cutaneous perceptual thresholds to be lower (Naveteur & Honoré, 1995) than when they are directed away (see also Honoré et al., 1989, Kennett et al., 2001, Pierson et al., 1991, Press et al., 2004, Rorden et al., 2002, Serino et al., 2007). This is in keeping with the suggestions by Dehaene and Changeux (2005) that activity in both the attention system and brain sensory areas exerts a facilitatory effect on conscious perception of sensory external stimuli, as well as with the point made by Schubert and colleagues (2006), according to whom attention processes are instrumental for conscious perception of tactile stimuli. These studies support the idea of strong links between attention and conscious perception, but deal with sensations driven by external events, not SPS. The fact that SPS are usually perceived during rest periods (i.e., when attention is free to explore any event or sensation) and less so when we are occupied with other activities (i.e., when attention is oriented elsewhere), leads to the hypothesis that orienting attention to the part of the body being explored would enhance conscious perception of those sensations, whilst directing it away would reduce it. Thus it would parallel the influence of attention on somatosensory perception.

Signals from the receptive organs are naturally processed in the corresponding areas of the somatosensory cortex, the interface between receptors and attention. The body representation in the somatosensory cortex is highly modulated by attention, as evidenced through single unit recordings in monkeys (Hsiao et al., 1993, Hyvärinen et al., 1980) and brain imaging techniques in humans (Hämäläinen et al., 2002, Mima et al., 1998, Noppeney et al., 1999). For instance, directing attention to the stimulated area of the body induces reliable changes in the firing rates of single neurons (Hsiao, O’Shaughnessy, & Johnson, 1993), influences magnetic field strengths (Iguchi et al., 2002, Mima et al., 1998), and enlarges activated areas (Hämäläinen et al., 2002). Furthermore, there is evidence that somatosensory representation of the digits shifts according to the direction of spatial attention (Noppeney et al., 1999). Another interesting observation, made with single unit recordings in animals (Hsiao et al., 1993) and brain imaging in humans (Hämäläinen et al., 2002; Iguchi et al., 2005), is that attention regulates the cortical representation of hands by enhancing task-relevant inputs and suppressing other noise inputs. This enhancement-suppression combination is a known attention-related phenomenon (Chelazzi et al., 1993, LaBerge, 1995) and might also be expected to modulate the cortical coding of SPS; it is still unclear whether such coding takes place within the somatosensory cortex. Interestingly, there is evidence of large-scale, low frequency spontaneous neuronal fluctuations in the human somatosensory cortex during rest (Nir et al., 2008), although the functional significance of these neuronal events is not well understood.

To sum up, the putative presence of a proximo-distal gradient, and enhanced perception of spontaneous sensations arising in some locations and suppression of others when attending to the tested hand, would constitute behavioral evidence of attentional modulation of cortical somatosensory coding of signals spontaneously triggered by receptors. Furthermore, as exteroceptive tactile perception changes with age (Stevens & Patterson, 1995), it may be expected that the description of SPS change also with age. But as age influences body mass (Kuczmarski, Kuczmarski, & Najjar, 2001), it can be expected that the description of SPS changes also with body mass. We examined these issues by asking subjects to focus on one hand for a short time, either while looking at it or while looking at a salient item in the opposite direction, and then to map the intensity, location and extent of any spontaneous sensations they felt. The results back all of our hypotheses and even offer an additional argument about lateralized cortical processes.

Section snippets

Subjects

The study was conducted in accordance with the Helsinki Declaration. Subjects were excluded if they were not right-handers (i.e., if the Edinburgh score was smaller than 0.50), had a history of neurologic or psychiatric disease, had taken psychoactive substances (e.g., marijuana, antidepressants, anxiolytics, etc.) in the 3 months leading up to the testing session, and if they reported no SPS in more than two of the four tested conditions. Of the 84 undergraduates from the University of Lyon

Control experiment

Except from the effects of laterality and focusing on SPS, one of the main findings of the main Experiment is the presence of a proximo-distal gradient (Table 1 and Fig. 3), a gradient which is similar to the one observed when all receptive units are taken together (Burke et al., 1988, Johansson and Vallbo, 1979, Li et al., 2008, Vallbo and Johansson, 1984), and especially when considering mechanoreceptors (Vallbo & Johansson, 1984). The possibility that some of the reported sensations were

Global distribution and proximo-distal gradients

The first results of interest were the reporting of sensations over the whole glabrous surface of the hands, and the existence of a proximo-distal gradient, whatever the tested condition, and whether the hand was placed palm-down (palm in contact with the table) or palm up (palm without contact with any stimulus). The number of subjects reporting spontaneous sensations was highest over the distal phalange. Numbers dropped sharply over the intermediate phalange, and then more gently over the

Conclusions

This paper began with the statement that everyone knows what SPS feel like. We would like to end by stating that the multiplicity and complexity of processes underlying such perceptions are obvious from our results. What is of interest here is that directing of attention and gaze modulates the intensity, spatial extent and spatial distribution of these perceptions, even though they are by no means evoked experimentally. This is encouraging because it leaves the door wide open for the scientific

Acknowledgments

Special thanks to Éric Ortéga for his patience and dexterity during the creation of the software of spatial analyses. This study was supported by an ANR BLAN07-3-203520 grant to the first author, as well as a Dermscan Group convention.

References (99)

  • I. Hashimoto et al.

    Are there discrete distal–proximal representations of the index finger and palm in the human somatosensory cortex? A neuromagnetic study

    Clinical Neurophysiology

    (1999)
  • Y. Hlushchuk et al.

    Distal to proximal representation of volar index finger in human area 3b

    NeuroImage

    (2004)
  • J. Honoré et al.

    Reduction of cutaneous reaction time by directing eyes towards the source of stimulation

    Neuropsychologia

    (1989)
  • K.O. Johnson

    The roles and functions of cutaneous mechanoreceptors

    Current Opinion in Neurobiology

    (2001)
  • P. Jung et al.

    Asymmetry in the human primary somatosensory cortex and handedness

    NeuroImage

    (2003)
  • S. Kennett et al.

    Noninformative vision improves the spatial resolution of touch in humans

    Current Biology

    (2001)
  • M.F. Kuczmarski et al.

    Effects of age on validity of self-reported height, weight, and body mass index: Findings from the third National Health and Nutrition Examination Survey, 1988–1994

    Journal of the American Dietetic Association

    (2001)
  • X. Li et al.

    High resolution topographical mapping of warm and cold sensitivities

    Clinical Neurophysiology

    (2008)
  • G.A. Michael et al.

    The human pulvinar and attentional processing of visual distractors

    Neuroscience Letters

    (2004)
  • G.A. Michael et al.

    Hot colors: The nature and specificity of color-induced nasal thermal sensations

    Behavioural Brain Research

    (2010)
  • G.A. Michael et al.

    Controlling attentional priority by preventing changes in oculomotor programs: A job for the premotor cortex?

    Neuropsychologia

    (2001)
  • G.A. Michael et al.

    Cool coors: Color-induced nasal thermal sensations

    Neuroscience Letters

    (2008)
  • B. Milner et al.

    Right-hemisphere superiority in tactile pattern-recognition after cerebral commissurotomy: Evidence for nonverbal memory

    Neuropsychologia

    (1972)
  • W. Morris et al.

    The effects of consensus-breaking and consensus-pre-empting partners of reduction in conformity

    Journal of Experimental Social Psychology

    (1975)
  • J. Naveteur et al.

    How to detect an electrocutaneous shock that is not delivered? Overt spatial attention influences decision

    Behavioural Brain Research

    (2005)
  • R.C. Oldfield

    The assessment and analysis of handedness: The Edinburgh inventory

    Neuropsychologia

    (1971)
  • J.M. Pierson et al.

    Direction of gaze during vibrotactile choice reaction time tasks

    Neuropsychologia

    (1991)
  • G. Rizzolatti et al.

    Reorienting attention across the horizontal and vertical meridians: Evidence in favor of a premotor theory of attention

    Neuropsychologia

    (1987)
  • C. Rorden et al.

    Enhanced tactile performance at the destination of un upcoming saccade

    Current Biology

    (2002)
  • R. Schweizer et al.

    Finger representations in human primary somatosensory cortex as revealed by high-resolution functional MRI of tactile stimulation

    NeuroImage

    (2008)
  • J. Semmes

    A non-tactual factor in astereognosis

    Neuropsychologia

    (1965)
  • A. Serino et al.

    Can vision of the body ameliorate impaired somatosensory function?

    Neuropsychologia

    (2007)
  • A. Serino et al.

    Spatial organisation in passive tactile perception: Is there a tactile field?

    Acta Psychologica

    (2008)
  • S. Sim

    A test for spatial correlation for binary data

    Statistics & Probability Letters

    (2000)
  • P. Sörös et al.

    Cortical asymmetries of the human somatosensory hand representation in right- and left-handers

    Neuroscience Letters

    (1999)
  • D.C. Summers et al.

    Perceptual asymmetries in the somatosensory system: A dichaptic experiment and critical review of the literature from 1929 to 1986

    Cortex

    (1990)
  • M. Taylor-Clarke et al.

    Vision modulates somatosensory cortical processing

    Current Biology

    (2002)
  • F. Tecchio et al.

    Spatial properties and interhemispheric differences of the sensory hand cortical representation: A neuromagnetic study

    Brain Research

    (1997)
  • D. Vaitl

    Interoception

    Biological Psychology

    (1996)
  • A.B. Vallbo et al.

    Skin mechanoreceptors in the human hand: Neural and psychophysical thresholds

  • N.R. Varney et al.

    Tactile perception of direction in relation to handedness and familial handedness

    Neuropsychologia

    (1975)
  • N. Weisz et al.

    The relevance of spontaneous activity for the coding of the tinnitus sensation

    Progress in Brain Research

    (2007)
  • A.R. Aron et al.

    Stop-signal inhibition disrupted by damage to right inferior frontal gyrus in humans

    Nature Neuroscience

    (2003)
  • M. Botvinick et al.

    Rubber hands ‘feel’ touch that eyes see

    Nature

    (1998)
  • D. Burke et al.

    Responses to passive movement of receptors in joints, skin and muscle of the human hand

    Journal of Physiology

    (1988)
  • O.G. Cameron et al.

    Regional brain activation due to pharmacologically induced adrenergic interoceptive stimulation in humans

    Psychosomatic Medicine

    (2002)
  • L. Chelazzi et al.

    A neural basis for visual search in inferior temporal cortex

    Nature

    (1993)
  • R.C. Coghill et al.

    Hemispheric lateralization of somatosensory processing

    Journal of Neurophysiology

    (2001)
  • A.D. Craig (Bud)

    Human feelings: Why are some more aware than others?

    Trends in Cognitive Sciences

    (2004)
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