The tickly homunculus and the origins of spontaneous sensations arising on the hands
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)
- et al.
Response characteristics of peripheral mechanoreceptive units in man: Relation to the sensation magnitude and to the subject’s task
Electroencephalography and Clinical Neurophysiology
(1986) - et al.
Lateral differences in tactile directional perception
Neuropsychologia
(1978) Right and left cerebral hemisphere damage and tactile perception: performance of the ipsilateral and contralateral sides of the body
Neuropsychologia
(1974)- et al.
Hemispheric specialization for tactile perception opposed by contralateral noise
Cortex
(1988) - et al.
Somatotopic organization of the ventral and dorsal finger surface representations in human primary sensory cortex evaluated by magnetoencephalography
NeuroImage
(2002) Spatial ability and lateralization in the haptic modality
Brain and Cognition
(1998)- et al.
Tactile perception of direction in relation to hemispheric locus of lesion
Neuropsychologia
(1971) - et al.
The cognitive and neural correlates of “tactile consciousness”: A multisensory perspective
Consciousness and Cognition
(2008) - et al.
Activation of somatosensory cortical areas varies with attentional state: An fMRI study
Behavioural Brain Research
(2002) - et al.
Sympathetic arousal and self-attention: The accessibility of interoceptive and exteroceptive arousal cues
Journal of Experimental Social Psychology
(1989)
Are there discrete distal–proximal representations of the index finger and palm in the human somatosensory cortex? A neuromagnetic study
Clinical Neurophysiology
Distal to proximal representation of volar index finger in human area 3b
NeuroImage
Reduction of cutaneous reaction time by directing eyes towards the source of stimulation
Neuropsychologia
The roles and functions of cutaneous mechanoreceptors
Current Opinion in Neurobiology
Asymmetry in the human primary somatosensory cortex and handedness
NeuroImage
Noninformative vision improves the spatial resolution of touch in humans
Current Biology
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
High resolution topographical mapping of warm and cold sensitivities
Clinical Neurophysiology
The human pulvinar and attentional processing of visual distractors
Neuroscience Letters
Hot colors: The nature and specificity of color-induced nasal thermal sensations
Behavioural Brain Research
Controlling attentional priority by preventing changes in oculomotor programs: A job for the premotor cortex?
Neuropsychologia
Cool coors: Color-induced nasal thermal sensations
Neuroscience Letters
Right-hemisphere superiority in tactile pattern-recognition after cerebral commissurotomy: Evidence for nonverbal memory
Neuropsychologia
The effects of consensus-breaking and consensus-pre-empting partners of reduction in conformity
Journal of Experimental Social Psychology
How to detect an electrocutaneous shock that is not delivered? Overt spatial attention influences decision
Behavioural Brain Research
The assessment and analysis of handedness: The Edinburgh inventory
Neuropsychologia
Direction of gaze during vibrotactile choice reaction time tasks
Neuropsychologia
Reorienting attention across the horizontal and vertical meridians: Evidence in favor of a premotor theory of attention
Neuropsychologia
Enhanced tactile performance at the destination of un upcoming saccade
Current Biology
Finger representations in human primary somatosensory cortex as revealed by high-resolution functional MRI of tactile stimulation
NeuroImage
A non-tactual factor in astereognosis
Neuropsychologia
Can vision of the body ameliorate impaired somatosensory function?
Neuropsychologia
Spatial organisation in passive tactile perception: Is there a tactile field?
Acta Psychologica
A test for spatial correlation for binary data
Statistics & Probability Letters
Cortical asymmetries of the human somatosensory hand representation in right- and left-handers
Neuroscience Letters
Perceptual asymmetries in the somatosensory system: A dichaptic experiment and critical review of the literature from 1929 to 1986
Cortex
Vision modulates somatosensory cortical processing
Current Biology
Spatial properties and interhemispheric differences of the sensory hand cortical representation: A neuromagnetic study
Brain Research
Interoception
Biological Psychology
Skin mechanoreceptors in the human hand: Neural and psychophysical thresholds
Tactile perception of direction in relation to handedness and familial handedness
Neuropsychologia
The relevance of spontaneous activity for the coding of the tinnitus sensation
Progress in Brain Research
Stop-signal inhibition disrupted by damage to right inferior frontal gyrus in humans
Nature Neuroscience
Rubber hands ‘feel’ touch that eyes see
Nature
Responses to passive movement of receptors in joints, skin and muscle of the human hand
Journal of Physiology
Regional brain activation due to pharmacologically induced adrenergic interoceptive stimulation in humans
Psychosomatic Medicine
A neural basis for visual search in inferior temporal cortex
Nature
Hemispheric lateralization of somatosensory processing
Journal of Neurophysiology
Human feelings: Why are some more aware than others?
Trends in Cognitive Sciences
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