http://informahealthcare.com/smr ISSN: 0899-0220 (print), 1369-1651 (electronic) Somatosens Mot Res, 2014; 31(3): 111–121 ! 2014 Informa UK Ltd. DOI: 10.3109/08990220.2014.888992

ORIGINAL ARTICLE

Gating of spontaneous somatic sensations by movement Rachel Beaudoin & George A. Michael Laboratoire EMC, Universite´ de Lyon, Universite´ Lyon 2, Lyon, France

Abstract

Keywords

Movement is known to attenuate the perception of tactile stimuli delivered on the moving part of the body, and this gating diminishes the greater the distance from the moving part. However, does it influence the perception of sensations occurring spontaneously without external triggers? In Experiment 1, participants were asked to focus on one hand while moving or not moving their thumb, and thereafter to map and describe the spatial and qualitative attributes of sensations perceived over the remaining, motionless part of the hand. The results show that movement reduces the frequency, spatial extent, and intensity of sensations, but also participants’ confidence about their spatial characteristics. As expected, gating decreased the greater the distance from the moving thumb. Furthermore, gating was greater for distal than proximal segments of the hand, suggesting a hierarchical proximo-distal suppression. Experiment 2 ruled out the possibility that these effects were due to tactile sensations elicited by movement. Possible mechanisms of gating in the case of spontaneous sensations are discussed.

Hands, interoception, movement, sensory gating, spontaneous sensations, tactile perception

Introduction A somatosensory experience is not always associated with a stimulus. Sensations can also be experienced spontaneously and reported in the absence of any external stimulus (i.e., spontaneous sensations; SPS). Paresthesias or hallucinations (Schmidt et al. 1990a; Gallace and Spence 2014) cannot capture the nature of SPS since, contrary to SPS, they are abnormal sensations experienced in the case of injury, and are limited to a narrow range of sensations usually described as pins and needles. SPS are normal phenomena since they are experienced by almost anybody and are quite diversified (Michael and Naveteur 2011). Indeed, different kinds of SPS may be perceived on the skin, like a tickle, tingle, or cooling, and others may originate deep within the body, like pulse sensations associated with heartbeats. What precisely makes a person consciously perceive them is not known. The very recent scientific investigation of these phenomena shows that they are tuned by factors such as attention and visual input (Naveteur et al. 2005; Michael and Naveteur 2011; Michael et al. 2012), and that processes lateralized to the right cerebral hemisphere, such as tactual spatial perception (Semmes 1965) and interoception (Cameron 2002; Craig 2003, 2004) are most probably involved. Through information they provide about the frontiers of the body and what is felt, SPS could contribute Correspondence: G. A. Michael, De´partement Psychologie Cognitive & Neuropsychologie, Laboratoire d’E´tude des Me´canismes Cognitifs, Universite´ Lyon 2, 5, Avenue Pierre Mende`s-France, 69676 Bron Cedex, France. Tel: +33 4 78 77 30 53. E-mail: George. [email protected]

History Received 16 November 2013 Revised 20 January 2014 Accepted 23 January 2014 Published online 5 March 2014

toward the creation/maintenance of a conscious image of the body, mainly during periods of rest and in the absence of external triggers (Michael et al. 2012). Here, we investigate whether rest allows SPS to be better perceived by analyzing the effect of an active finger movement. There is already an important corpus of papers suggesting that active movement attenuates the perception of exteroceptive sensations occurring on moving and neighboring parts of the human body (Papakostopoulos et al. 1975; Rushton et al. 1981; Schmidt et al. 1990b), but does movement influence the perception of SPS, as suggested through some anecdotal reports (Schmidt et al. 1990a)? Several studies have shown that the inflow of somatosensory information to the cerebral cortex is modified both before and during active movement. Known as ‘‘gating’’, this phenomenon suggests information is suppressed during active movement (Papakostopoulos et al. 1975; Abbruzzese et al. 1981; Rushton et al. 1981; Cohen and Starr 1987; Jones et al. 1989; Valeriani et al. 2001; Seki et al. 2003; Insola et al. 2004, 2010; Wasaka et al. 2007). All components of the somatosensory evoked cortical potentials (SEPs) and magnetic fields are diminished, even abolished, during active movement (Coquery et al. 1972; Papakostopoulos et al. 1975; Starr and Cohen 1985; Jones et al. 1989; Schmidt et al. 1990a; Rossini et al. 1999; Valeriani et al. 2001; Insola et al. 2004, 2010; Wasaka et al. 2007), and the attenuation of these cortical signals correlates with the attenuated perception of cutaneous stimulation during active (Schmidt et al. 1990a, 1990b) and passive (Coquery et al. 1972; Rushton et al. 1981; Jones et al. 1989; Rossini et al. 1999) movement. Descending

112

R. Beaudoin & G. A. Michael

and/or ascending mechanisms have been evoked as possible explanations. Peripheral feedback from the moving limb may diminish transmission of tactile information from the skin. Furthermore, motor commands may modulate cutaneous input at sites where afferent and efferent pathways converge. Some somatosensory afferents terminate in the dorsal column nuclei where corticofugal projections act to select some somatosensory input and ensure the adequate discrimination of tactile information (Marin˜o et al. 1999; Nun˜ez and Malmierca 2007). It was also shown that cortical somatosensory responses can also be decreased through observation of movement (Voisin et al. 2011), suggesting that gating involves high-level processes too. As far as the hand is concerned, gating is well marked when stimuli are delivered on the moving finger but gradually shrinks—and even disappears— towards more distant fingers (Rushton et al. 1981; Schmidt et al. 1990b). For instance, magnitude ratings for some sensations dropped by 48% when participants moved the finger receiving the stimulation and by 23% when an adjacent finger was moved. When a distant finger of the same hand was moved, the mean drop in magnitude was 19% (Schmidt et al. 1990b). Gating is thus graduated, such that the smaller the distance between the moving finger and the stimulated finger, the more pronounced gating will be (Williams et al. 1998). These characteristics of movement-dependent gating concern exteroceptive sensations. However, SPS may also be concerned since they are seemingly perceived better when at rest, when no movement is being performed (Michael and Naveteur 2011). Two previous studies (Michael and Naveteur 2011; Michael et al. 2012) showed that peripheral sensitivity, attention, and visual input might shape the perception of SPS. For instance, although SPS are reported over the entire surface of the hand, their frequency follows a proximo-distal gradient similar to the one described for the density of receptors (Johansson and Vallbo 1979b; Vallbo and Johansson 1984) and tactile sensitivity of the hand (Johansson and Vallbo 1979a). SPS are most frequent and occupy larger areas at the fingertips. Their frequency and surface gradually diminish toward the palm. This pattern is observed even in the complete absence of contact between the hand and any stimulus. Even though it is generally accepted that the amplitude of spontaneous impulses of a single cell is not strong enough to reach conscious perception (Singer 2001), spontaneous oscillatory activity of large cell assemblies at more central levels (Panetsos et al. 1998) may prove relevant in triggering spontaneous bodily sensations, similar to what happens in the case of tinnitus (Weisz et al. 2007). Manipulation of overt attention yielded one of the most interesting results. Attention extended the areas of sensitivity beyond the fingertips, thereby expanding the highly sensitive points. However, the effects of attention differed depending on whether or not visual input was available. It was suggested that attention and vision interact to enhance perception of SPS, and this is in agreement with findings that visual input may increase interoceptive awareness (Mirams et al. 2010) and tactile perception (e.g., Serino et al. 2007). Despite the assertion that, usually, SPS are better perceived during periods of rest (Michael and Naveteur 2011), the effects of active movement/rest on SPS have not been

Somatosens Mot Res, 2014; 31(3): 111–121

Figure 1. During the movement condition of Experiment 1, participants were asked to execute a rapid lateral movement of their thumb (i.e., radial flexion/extension) without touching their index finger and while focusing on the rest of the hand.

investigated yet. Interestingly, the literature on gating has focused mostly on some kinds of tactual (e.g., flutter, pressure, etc.) and pain perception, but disregarded non-painful thermoperception (i.e., warming, cooling), and sensations originating deep within the hands (e.g., pulse sensations associated with heartbeats). Does gating change the perception of such kinds of sensations when they arise spontaneously, in the absence of any external trigger? At this aim, in Experiment 1, we asked participants to move or not their thumb of one hand (Figure 1) while focusing on the whole hand. They were then asked to map on a response protocol the characteristics (surface, intensity, quality) of any SPS they felt over the remaining motionless parts of the hand, and to rate their confidence about their spatial characteristics. The hypothesis was that SPS would be better perceived at rest than during active movement due to gating. Furthermore, gating would be graded, with SPS being more suppressed for fingers near the thumb (i.e., the index) and less or not suppressed far from it (i.e., small finger). SPS on the moving finger, that is, the thumb, were not assessed because they could be confounded with exteroceptive tactile sensations evoked on that finger during movement. Since movement also elicits tactile sensations, Experiment 2 tended to isolate the contribution of a continuous tactile stimulation in the absence of any movement.

Experiment 1 Participants Experiment 1 was conducted in accordance with the Helsinki Declaration. Participants were excluded if they were not right-handers (i.e., if the laterality score was less than 0.50),

DOI: 10.3109/08990220.2014.888992

had a history of neurologic or psychiatric disease, had taken psychoactive substances (e.g., marijuana, antidepressants, anxiolytics, etc.) in the 3 months preceding the test session, and if they reported no SPS in more than 50% of the tested conditions. Out of the 60 undergraduates from the University of Lyon 2 who took part in the present investigation, 12 were excluded on the basis of these criteria, all of them males. The mean age of the remaining 48 undergraduates (43 females, 5 males) was 22 ± 0.49 (age range: 18–39), their mean body mass index was 21.6 ± 0.41 kg/m2 (range: 16.8–28.8 kg/m2), they were all right-handers according to the Edinburgh laterality inventory (0.78 ± 0.02; Oldfield 1971), and all gave their written informed consent for their participation prior to the test. Protocol and procedure Participants were split into groups of four to five. They performed the test in a quiet room with an ambient temperature of 20  C. Upon entering the room, each participant was asked to take a seat behind a desk, read and sign the consent text, supply information about gender, age, height, and weight, and complete the Edinburgh laterality inventory (Oldfield 1971). The next step consisted of the main SPS investigation. All participants were facing the experimenter. The experimenter started by describing what SPS are, that they are normal phenomena, and provided a list of eleven sensations that might be felt (beat/pulse, itch, tickle, numbness, skin stretch, tingle, warming, cooling, muscular stiffness, flutter, and vibration). The list was constructed on the basis of the lists used by Ochoa and Torebjo¨rk (1983) and Macefield et al. (1990) to study sensations evoked by microstimulation. They were told that, in each trial, they would be allowed to focus attention on one hand in search for SPS while moving their thumb or while holding the thumb motionless. The experimenter then showed the required movement. It consisted of a continuous and regular radial flexion/extension of the thumb executed as quickly as possible without touching the index finger (Figure 1). Each participant was then required to reproduce this movement in order to control whether its execution was correct. Participants were then asked to remove any jewelry from their hands and wrists. For the sake of homogeneity of the glabrous surface of the skin, all participants were required to spend 15 s cleansing their hands with an antiseptic gel (AniosgelÕ 85 NPC, &3 ml per participant) in order to remove any external agents that might interfere with the task. A minimum latency of 15 s was respected between the cleansing operation and the start of the test (Naveteur et al. 2005). The experimenter then distributed to each participant one pencil, a sheet of paper (white, 80 g, 21  29.7 cm2), and a separated four-page protocol containing, on each page, one standardized reduced picture of a hand (the distance between the tip of the middle finger and palm/ wrist frontier was 11.2 cm), the list of the eleven SPS, and two visual analogue scales (i.e., two continuous horizontal lines without markers on each extreme end) for the confidence ratings. The beginning of the test session was then announced. For visual stimuli not to interfere with the procedure, participants were required to invert the four-page protocol and to put it away from them on their desk, along with the

Gating of spontaneous somatic sensations by movement

113

pencil. Participants were asked to place the white sheet of paper on one side in relation to the body midline. They then placed their tested hand palm down on the paper, without any pressure exerted and with the fingers slightly apart. They placed their other hand out of sight, in their lap. A ‘‘start’’ signal given verbally by the experimenter marked the beginning of each trial following which participants directed their gaze toward their tested hand for a period of 10 s. During that time, they focused on the whole hand, moved their thumb or not, depending on the test condition, and kept their attention on the tested hand so they could detect and report any sensations that might occur. They were also told it was possible no sensations would occur. Four separate conditions were tested: (a) moving thumb left hand, (b) moving thumb right hand, (c) fixed thumb left hand, and (d) fixed thumb right hand. All participants completed all four conditions once, balanced in a Latin-square order. The experimenter announced the end of this period with a ‘‘stop’’ signal. Participants were then immediately asked to take the fourpage protocol and to indicate whether or not they had detected any sensations in the tested hand, other than in their thumb. If they had, they were asked to (a) map the extent and topography of the sensations by shading in the areas where sensations had occurred on the picture of the tested hand; (b) estimate their overall perceived intensity on a 10-point scale (1 ¼ just perceptible; 10 ¼ very intense but not painful). They were also told that if they could attribute different intensities to each sensation they were free to do so; (c) indicate their level of confidence in the location and extent of the perceived sensations on two 10-cm visual analogue scales (not confident to very confident); and (d) identify the sensations using the list of descriptors, with the possibility of course of choosing more than one or even adding descriptors that were not listed. The whole session lasted approximately 45 min.

Results Sensations were reported by all participants in at least two conditions. Of the 48 participants, 15 reported SPS in only two tested conditions (31.3%), 20 reported them in three tested conditions (41.7%), and 13 reported them in all tested conditions (27%). The mean movement velocity as measured after the test from 28 of the 48 participants during a supplementary period of 10 s was 2.06 ± 0.26 cycles per second (range: 1.5–2.7). Topography This analysis was carried out in order, first, to observe the spatial distribution of SPS over the hand and, second, to detect significant differences in this spatial distribution between the fixed and the moving conditions. Shaded areas on each printed hand were projected onto a 140  140 grid with 1 mm2 resolution and then converted into binary codes (0 ¼ unshaded cell; 1 ¼ shaded cell). The result, for each subject and test condition, was individual maps of spatially distributed binary codes representing the shaded areas. Four frequency maps (one per condition) were obtained by superimposing the 48 individual binary maps, with the value in each cell representing the percentage of participants having

114

R. Beaudoin & G. A. Michael

Somatosens Mot Res, 2014; 31(3): 111–121

Figure 2. Topographical analyses of sensations in Experiment 1. The hands are shown palm down. The colored scale of the reduced flanker hands represents the percentage of participants having reported sensations. The central hand is an exact probability map based on the difference between the fixed and the moving condition. Only clusters significant at p50.001 are presented. Reddish cells denote the dominance of the fixed condition whilst bluish cells denote the dominance of the moving condition.

shaded it in (flanker hands in Figure 2). Topographical statistics were compiled by means of cell-by-cell comparisons between the moving and fixed conditions, with the exact test for the significance of change (Liddell 1983)1 producing significance maps (the central hand in Figure 2) depicting the cells where movement triggered reliable changes. The alpha level was set to 0.05 bicaudal. The significance maps resulting from the abovementioned comparisons were subsequently subjected to binary conversion (0 ¼ non-significant; 1 ¼ significant) and a spatial scan procedure for binary data (Kulldorff 1997) was subsequently used. This consists in a circular window that scans the maps, detects, and localizes significant clusters. On the basis of previous simulations (Michael et al. 2012), the maximal radius was set at 6 cells (representing a maximal scanned surface of 113 cells). Only significant clusters at p50.001 level bicaudal are presented here. For more technical and methodological details, see Michael and Naveteur (2011) and Michael et al. (2012). All spatial analyses were carried out using homemade software. No statistical differences were found between the hands. As may be seen from the flanker hands (Figure 2), SPS were reported over the whole hand, but were not distributed uniformly. The most frequent sources were located at the fingertips and the least frequent source was the palm. As suggested by both the flanker hands and the central significance map, movement produced less frequent sensations than the fixed condition. This effect concerned each of the fingers and, in most cases, all phalanges, but mainly the distal phalanx. It is noteworthy that no suppression of sensations was found in the palm. When the number of cells where suppression was observed was compared across fingers, we found a significant difference (2(3) ¼ 436; p50.000001) in that the effect was somewhat graduated from the index (168 cells) to the middle (121 cells) and ring fingers (138

cells), and to the little finger (29 cells) thereafter. The reduction in SPS was thus greater close to the moving thumb and quite small at a greater distance from it. Relative surface The aim of this analysis was to investigate the effect of movement on the spatial extent of the reported SPS as a function of the finger segments, and as a function of the fingers. Based on the individual maps of spatially distributed binary codes used in the topographical analyses, we first divided the surface of the glabrous skin of the hand (thumb excepted) into 13 anatomical segments (12 phalanges and 1 palmar segment) following the estimations of Johansson and Vallbo (1979b). The number of shaded cells within a given segment (distal phalanx, intermediate phalanx, etc.) was then divided by the number of cells constituting the whole segment and multiplied by 100 in order to obtain the percentage of shaded areas. The results are presented in Figure 3. These values were then subjected to an analysis of covariance, with the movement condition (moving vs. fixed), tested hand (left vs. right), and anatomical segment (distal, intermediate, proximal, and palm) as within-subject factors; age, body mass index, and laterality index were used as covariates because our previous investigations showed that they correlate with some of the SPS characteristics. The main effect of movement was significant (F(1,44) ¼ 12.62; p50.00093). Perceived SPS were more extensive when the hand was fixed (10.7%) rather than moving (7.6%). The main effect of segment was significant (F(3,141) ¼ 12.48; p50.001). The extent of SPS increased from the palm to the distal phalanx, revealing a proximo-distal gradient (palm: 7.2%; proximal: 6.8%; intermediate: 11.4%; distal: 17%). Newman–Keuls post hoc comparisons revealed that the difference between the

DOI: 10.3109/08990220.2014.888992

Gating of spontaneous somatic sensations by movement

115

reached 3 points. Only the main effect of movement was significant (F(1,47) ¼ 11.92; p50.002) insofar as sensations were perceived as more intense in the fixed condition (3.4 points) than the moving condition (2.2 points). Confidence ratings Confidence ratings were rank-transformed and submitted to an analysis of covariance with the movement condition (moving vs. fixed) and tested hand (left vs. right) as within-subject factors; age, body mass index, and laterality index were used as covariates. The participants were more confident about locating the sensations when the tested hand was fixed (6.11 points) than when it was moving (3.93 points; F(1,47) ¼ 15.61; p50.00028). A similar result was observed as regards confidence about the spatial extent of the sensations (fixed: 5.16 points; moving: 3.68 points; F(1,47) ¼ 9.93; p50.003). No other reliable results were found. Figure 3. Relative surfaces (mean percentage ±1 SEM) of sensations reported in Experiment 1 on segments of the hands (panel A) and fingers (panel B) in the moving and fixed conditions, respectively.

distal and intermediate phalanx was significant (p50.003), as well as the difference between the intermediate and the proximal phalanx (p50.04). However, the difference between the proximal phalanx and the palm was not significant. The interaction between the anatomical segment and the movement condition was significant (F(1,47) ¼ 4.4; p50.04; Figure 3A). Newman–Keuls post hoc comparisons showed that the degree of suppression due to movement was not the same for each anatomical segment. Sensations decreased by 8% for the distal phalanx (fixed: 21%; moving: 13%; p50.00007), by 5% for the intermediate phalanx (fixed: 14%; moving: 9%; p50.024), and by 5% for the proximal phalanx, but that difference was not significant (fixed: 9%; moving: 4%; p40.14). No change was found in the palm (fixed: 7%; moving: 7%; p40.9). These results suggest that the most sensitive part of the hand, that is, the distal phalanx, is the most affected during movement. No other reliable results were found. A second analysis2 was performed with the movement condition (moving vs. fixed), tested hand (left vs. right), and finger (index, middle, ring, and small) as within-participant factor, and the same covariates as before. There was a significant effect of movement (F(1,47) ¼ 4.4; p50.041). Despite the absence of interaction between movement and finger, suppression during thumb movement was quite large and significant for the index (fixed: 15.5%; moving: 8.3%; p50.003), middle (fixed: 14.6%; moving: 7.7%; p50.005), and ring (fixed: 15.4%; moving: 8.2%; p50.003) fingers. Suppression was also observed on the little finger, yet significance was not reached (fixed: 12.7%; moving: 9.9%; p40.14; Figure 3B). Intensity Perceived intensities were rank-transformed and submitted to an analysis of covariance with the movement condition (moving vs. fixed) and tested hand (left vs. right) as withinsubject factors; age, body mass index, and laterality index were used as covariates. The mean perceived intensity

Types of sensations The variety of the reported sensations was analyzed with chisquare tests. All eleven proposed sensations were reported at least once, but the number of times each sensation was reported was not the same (2(10) ¼ 161; p50.000001). Tingling was the most frequent sensation (18.3%), followed by beat/pulse (14.5%), numbness (13.6%), and muscle stiffness (10.7%). The least frequent sensations were warming (9.2%), flutter (8.3%), tickle (8.1%), cooling (5.4%), vibration (3.4%), and skin stretch and itch (2.2%). Other sensations (pressure and electric flux) accounted for 4%. No noticeable differences were found as a function of movement, apart from a dramatic drop in the total number of sensations reported (fixed: 289; moving: 158; 2(1) ¼ 38.4; p50.000001). However, when SPS were clustered in distinct categories, movement had no effect on thermal sensations (warming plus cooling; fixed: 28; moving: 37; 2(1) ¼ 1.3; p40.26), but seemed to decrease sensations originating deep within the hands (beat/pulse plus muscle stiffness; fixed: 77; moving: 36; 2(1) ¼ 14.9; p50.0001) and surface tactile/mechanical sensations (all the remaining sensations except from numbness and itch; fixed: 128; moving: 70; 2(1) ¼ 17; p50.00004).

Experiment 2 The movement of the thumb executed by participants in Experiment 1 produces tactile sensations too. It is therefore difficult to conclude whether the effects observed were due to movement per se or to continuous distracting tactile sensations elicited by that movement. This is why Experiment 2 was carried out with the unique aim to assess, in the absence of any movement, the effect of a tactile stimulus on the thumb during the test. Furthermore, in order to exclude the effect of the contact between the glabrous surface of the hand and any other surface, the hands were tested palm up. Participants Participants were not the same as in Experiment 1. Experiment 2 was conducted according to the Helsinki Declaration. As before, participants were excluded if they

116

R. Beaudoin & G. A. Michael

were not right-handers (i.e., if the laterality score was less 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 preceding the test session, and if they reported no SPS in more than 50% of the tested conditions. Of the 35 students from the University of Lyon 2 who took part in the present investigation, 4 were excluded on the basis of these criteria, all males. The mean age of the remaining 31 undergraduates (25 females, 6 males) was 20.5 ± 2.3 (age range: 18–27), their mean body mass index was 22.3 ± 4.3 kg/m2 (range: 17–35 kg/m2), they were all right-handers according to the Edinburgh laterality inventory (0.82 ± 0.17; Oldfield 1971), and all gave their written informed consent for their participation prior to the test.

Somatosens Mot Res, 2014; 31(3): 111–121

the annulus was put on only the tested hand. The response procedure was the same as in Experiment 1, except that confidence ratings were not collected. At the end of the test, participants were asked to put on once again the annulus and to rate—for each hand separately—the intensity of the tactile sensation it elicited on a 10-point scale (1 ¼ just perceptible; 10 ¼ very intense).

Results Out of the 31 participants, 7 reported SPS in two conditions (22.6%), 12 reported them in three conditions (38.7%), and 12 reported them in all conditions (38.7%). The annulus elicited tactile sensations that were as intense over the left as over the right hand (left ¼ 4.08 ± 0.5; right ¼ 3.76 ± 0.48; Wilcoxon signed ranks test Z ¼ 1.25; p40.21).

Protocol and procedure The experiment was run collectively in three- to four-member groups in a quiet room with an ambient temperature ranging from 20 to 23  C. The procedure was identical to the one described in Experiment 1. Each participant received two white rubber annuluses that could be worn on the proximal phalanx of the left and right thumb, respectively. The diameter of the annulus was determined during a pilot study conducted on 25 participants (20 females, 5 males; age range: 17–45 years). This pilot study showed that the mean diameter of the right thumb was 1.94 ± 0.16 cm and that of the left thumb was 1.93 ± 0.16 cm. Nine annuluses for each hand were then constructed, five based on the mean diameter (weight left: 0.103 g; weight right: 0.104 g), two based on the mean minus two standard deviations (weight left: 0.093 g; weight right: 0.095 g), and two based on the mean plus two standard deviations (weight left: 0.121 g; weight right: 0.121 g). This diversity allowed giving each participant two annuluses that would best fit his/her thumbs. Participants were seated with their back supported on the back of a large chair. The leg ipsilateral to the tested hand was laterally abducted by about 60 degrees from the midline. Participants placed a smooth 25  25 cm2 piece of white cotton tissue on their thigh and had their arm resting on the inner side of their thigh. The hand was placed palm up so only a dorsal part of it, fingers excluded, was in contact with the thigh. The fingers were slightly spaced. The hand that was not tested was placed on the edge of the chair, on the external side of the leg contralateral to the tested hand. The standardized picture of the hand on which participants had to shade the areas were sensations occurred, was presented palm up. A ‘‘start’’ signal given verbally by the experimenter marked the beginning of each trial following which participants directed their gaze toward their tested hand for a period of 10 s. During that time, they focused on the whole hand and kept their attention there so they could detect and report any sensations that might occur. They were also told it was possible no sensations would occur. Two variables were manipulated, the tested hand and the annulus-present condition. Thus, four separate conditions were tested during which the tested hand was held motionless: (a) annulus absent left hand, (b) annulus absent right hand, (c) annulus present left hand, and (d) annulus present right hand. All participants completed all four conditions once, balanced in a Latin-square order. In the two annulus-present conditions,

Topography Data processing and analyses were the same as in Experiment 1. As may be seen from the flanker hands (Figure 4), even if the hand was not in contact with any object, SPS were reported over the whole hand and followed a proximo-distal gradient. As suggested by both the flanker hands and the central significance map, the presence of the annulus increased the frequency of sensations over the fingers and produced a small but reliable suppression of sensations in the palm. When the number of cells where amplification was observed was compared across fingers, we found a significant difference (2(3) ¼ 80.95; p50.000001) in that the effect was not graduated but was still not similar over the index (12 cells), the middle (58 cells), ring finger (8 cells), and the little finger (9 cells). Finally, in agreement with our previous investigations (Michael and Naveteur 2011; Michael et al. 2012), SPS were more frequent in the left hand. Relative surface Relative surface values were subjected to an analysis of covariance, with the annulus-present condition (absent vs. present), tested hand (left vs. right), and anatomical segment (distal, intermediate, proximal, and palm) as withinparticipant factors. Age, body mass index, and laterality index were used as covariates. The main effect of hand segment was significant (F(3,90) ¼ 2.7; p50.05). The extent of SPS increased from the palm to the distal phalanx, revealing a proximo-distal gradient (palm: 9%; proximal: 9.1%; intermediate: 11.7%; distal: 15.1%). No other significant effect was found. A second analysis was carried out with the annulus-present condition (absent vs. present), tested hand (left vs. right), and finger (index, middle, ring finger, and little finger) as within-participant factors, and with the same covariates. No significant effect was obtained. Intensity Perceived intensities were rank-transformed and submitted to an analysis of covariance with the annulus condition (absent vs. present) and tested hand (left vs. right) as withinparticipant factors. Age, body mass index, and laterality index were used as covariates. The mean perceived intensity reached 2.5 points. The main effect of hand was significant

DOI: 10.3109/08990220.2014.888992

Gating of spontaneous somatic sensations by movement

117

Figure 4. Topographical analyses of sensations in Experiment 2. The hands are shown palm up. The colored scale of the reduced flanker hands represents the percentage of participants having reported sensations. The central hand is an exact probability map based on the difference between the two tested conditions. Only clusters significant at p50.001 are presented. Left: The difference between the left and the right hands. Reddish cells denote the dominance of the left hand and bluish cells denote the dominance of the right hand. Right: The difference between the annulus-present and the annulus-absent conditions. Reddish cells denote the dominance of the annulus-present condition whilst bluish cells denote the dominance of the annulus-absent condition.

(F(1,30) ¼ 5.01; p50.033) since sensations were perceived as more intense over the left (2.9 points) than the right (2.2 points) hand. The main effect of the presence of the annulus was not significant (F(1,30) ¼ 0.004; p40.95), and this was the case for the annulus presence  hand interaction (F(1,30) ¼ 0.19; p40.66). Overall, the intensity of SPS was smaller than that of the tactile sensation elicited by the annulus itself (Wilcoxon signed ranks test Z ¼ 2.6; p50.01), and no correlation was found between these two ratings ((29) ¼ 0.19; p40.38). Types of sensations The variety of the reported sensations was analyzed with chisquare tests. All eleven proposed sensations were reported at least once, but the frequency with which each sensation was reported was not the same (2(10) ¼ 117.3; p50.000001). Tingling was the most frequent sensation (21.5%), followed by beat/pulse (14.5%), vibration (13.6%), muscle stiffness (10.4%), and numbness (7.3%). The least frequent sensations were flutter (8.8%), warming (7.6%), skin stretch (7.6%), cooling (5.7%), tickle (1.6%), and itch (1.6%). The total number of sensations reported increased when the annulus was put on (absent: 125; present: 192; 2(1) ¼ 14.16; p50.0002). If anything, Experiment 2 shows that continuous tactile stimulation of the thumb during the 10-s period of the test increases the frequency, intensity, number, and variety of SPS. A secondary finding was that the proximo-distal gradient in SPS was present once again even if, this time, there was no contact between the glabrous surface of the hand and any stimulus. Furthermore, this gradient was similar in extent to the gradient observed in Experiment 1.

Discussion Movement weakens the perception of SPS occurring on the hands. This decrease is obvious in respect of the frequency,

spatial extent, intensity, and variety of SPS. Furthermore, movement reduces not only the perception of SPS characteristics, but also participants’ confidence about the location and spatial extent of such sensations. Our findings are thus consistent with the literature on gating (Papakostopoulos et al. 1975; Abbruzzese et al. 1981; Rushton et al. 1981; Cohen and Starr 1987; Valeriani et al. 2001; Insola et al. 2004, 2010; Wasaka et al. 2007), and confirm the hypothesis that rest is critical for enabling SPS to be better perceived (Michael and Naveteur 2011), even though they are also perceived during movement, albeit less well. Gating therefore operates at the level of both exteroception and interoception. Effects of distance from the moving finger An analysis of the other characteristics of gating of SPS by movement yields some interesting results. Based on previous research on exteroception, SPS occurring on fingers at a distance from the moving finger were expected to be the least suppressed (graduated suppression, Rushton et al. 1981; Schmidt et al. 1990b; Williams et al. 1998). A graduated pattern, albeit not perfect, was observed mostly in the areas exhibiting changes in the frequency of SPS, but also on the spatial extent of SPS. The explanation for the absence of a perfect and linearly graduated pattern may lie with methodological differences. Our own data analyses differ from those of other studies (Rushton et al. 1981; Schmidt et al. 1990b; Williams et al. 1998) to the extent that we examined both spatial extent and topography, allowing for a more detailed investigation of the whole hand, and of each hand segment, combined with a comparison between segments. Other studies examined the effects of only some parts of the hand, which may be one reason why such a pattern was probably missed. Second, we may hypothesize that, unlike exteroceptive sensations for which peripheral factors are more critical (Song and Francis 2013), more central and less peripheral factors could be involved in SPS. Due to the high sensitivity

118

R. Beaudoin & G. A. Michael

of the fingers determined by peripheral factors (Johansson and Vallbo 1979a), gating of exteroceptive sensations by movement would be more confined to the finger next to the moving one, with peripheral sensitivity not allowing gating to extend to more distant fingers. On the other hand, gating at the cortical level is probably less selective owing to the lower central processing capacity. Indeed, the fact that a participant’s capacity to discriminate stimuli on the glabrous surface of the hand is less than the discriminative capacity of glabrous skin receptors led Vallbo and Johansson (1984), Schady et al. (1983), and others to suggest that central processing is less precise than processing taking place at peripheral levels. In other words, movement would affect all fingers to a large degree if SPS were mostly of cortical origin, which is one of the main hypotheses posited in our previous studies (Michael and Naveteur 2011; Michael et al. 2012). Alternatively, because the precision with which SPS are perceived is lower than that for exteroceptive sensations, movement could probably have the power to exert a more powerful effect on the perception of such vague and diffuse sensations. Another interpretation, albeit not supported by research on somatosensory gating (Harper and Hollins 2012), is that attention could have been directed toward the moving thumb and withdrawn from the motionless part of the hand, leading to a reduced perception of SPS. Our previous investigations showed indeed that attention tunes perception of SPS (Michael and Naveteur 2011; Michael et al. 2012). Yet, there are some arguments that run counter to this account. First, in those studies the effects of attention almost always interacted with the tested hand in such a way that they were stronger and, in some cases, exclusively visible over the left hand. Second, attention seemed to increase SPS in the fingers and to inhibit them in the palm. Thus, if the movement withdrew attention from the fingers, then an increment of SPS should be expected in the palm due to decreased inhibition. None of these phenomena were observed in Experiment 1 and, in agreement with some recent findings on exteroception (Harper and Hollins 2012), this minimizes the role of attention at least as a central factor of the observed gating effects. However, the results of Experiment 2 may, at least partly, be accounted for by attention effects. Attention could have been directed away from the tactile stimulus and toward the remaining hand segments leading to an increase in the frequency of perceived SPS over the fingers and a small decrease of their frequency in the palm. A last interpretation of the graduated pattern found in Experiment 1 is that active movement of the thumb may produce concomitant involuntary movements of the whole hand, resulting therefore in a rather homogenous suppression of SPS. In that case, SPS should also be suppressed in the palm. However, our topographical analyses and the analyses of the spatial extent detected no changes in the palm, such that this last explanation does not receive any support. Gating in the proximo-distal direction As expected, and in agreement with two previous investigations (Michael and Naveteur 2011; Michael et al. 2012), we observed a proximo-distal gradient in the frequency and extent of SPS. This was observed when the tested hand was in

Somatosens Mot Res, 2014; 31(3): 111–121

contact with a stimulus (Experiment 1) or not (Experiment 2). In Experiment 1, suppression due to movement was greatest in the distal phalanx and diminished towards the palm, giving the gradient a milder slope. Thus, the most sensitive part of the hand was the most affected by suppression during movement. Previous studies on exteroception reported graded effects of gating by movement in a hand-to-elbow direction (e.g., Williams et al. 1998) but, to our knowledge, no such effect was ever reported within the frontiers of the hand. Most of the studies on gating tested only one part of the hand (e.g., one phalanx), whereas our study analyzed the whole hand and, therefore, allowed for comparisons between fingers and between phalanges. The phenomenon is consistent with the putative functional role of gating during movement, according to which irrelevant sensory inputs during movement could be prevented from reaching consciousness (Coquery et al. 1972; Rushton et al. 1981; Schmidt et al. 1990b), therefore allowing for optimized movement execution and control. Insofar as the fingertips contain the majority of receptive units (Vallbo and Johansson 1984), they receive and transmit most sensory information. Such a massive flow of sensory information would have been highly annoying if it had not been reduced during movement execution and control. Consequently, it is perhaps to be expected that sensations over the fingertips are the most suppressed during movement. An alternative explanation for such a finding is perhaps that the more sensitive a body part is, the larger, more complex, and richer its representation at a cortical level. This heterogeneity between different body parts would also apply to the individual segments of the hand, such that the cortical representation of the fingertips would be larger than that of the other segments (Penfield and Jasper 1954). It was suggested that the representation of tactile receptors with small receptive fields conferring maximal tactile acuity (such as those found on the fingertips) occupy a larger area at a cortical level (Brown et al. 2004). If we now posit the existence of an inhibitory mechanism that operates uniformly over the whole hand, and if the cortical representation of the fingertips were larger, then inhibition would inevitably be more widespread and stronger as regards the cortical representation of those parts of the hand. Putative mechanisms of gating of SPS by movement All empirical investigations of SPS reported up to date were behavioral (Naveteur et al. 2005; Michael and Naveteur 2011; Michael et al. 2012; and the present study), so whether these experiences have a peripheral or central origin is based only on the characteristics of behavioral reports. Moreover, such evidence suggests that SPS may have both peripheral and central origins. This suggests that gating of SPS could be achieved through different mechanisms depending on the level at which they arise. Most of the receptive units of the hand exhibit spontaneous activity at rest (e.g., Johansson and Vallbo 1979b) and some of them have such a low sensitivity threshold that a single impulse in one afferent fiber produces conscious sensory experiences (Johansson and Vallbo 1979a; Ochoa and Torebjo¨rk 1983). Yet, whether spontaneous impulses produce conscious experiences is not known. If SPS are at least partly due to such impulses, then they can be compared with

DOI: 10.3109/08990220.2014.888992

sensations evoked by stimuli applied extraneously and, in such a case, gating of SPS by movement could be similar to gating of exteroceptive sensations. For instance, during movement, those neurons controlling thumb movement might suppress neurons in the somatosensory cortex involved in the decoding of impulses (Cohen and Starr 1987) that produce SPS. Another possibility is that movement decreases the modulatory action of corticofugal fibers on incoming impulses. Fibers originating from the fifth layer of the somatosensory and motor cortices terminate in the gracile and cuneate nucleus of dorsal column where they regulate somatosensory inputs (Marin˜o et al. 1999; Nunez and Malmierca 2007). These hypotheses maintain that movement would result in decreased perception of SPS either through decreased decoding of impulses or through failures to amplify them. If, on the other hand, SPS have a mainly cortical origin, then inhibition of the somatosensory cortex by the motor cortex during movement (Cohen and Starr 1987) or direct activation of the somatosensory cortex by movement (Fromm and Evarts 1982) would be more plausible candidate mechanisms. Neurons activated during movement may directly suppress activity of those cortical somatosensory neurons involved in the activation and the bringing into consciousness stored information about the nature, intensity, and distribution of somatic information associated with the image of the body (Kinsbourne 1998; Michael et al. 2012). Gating of interoception by movement? We have previously suggested that SPS may be partly related to interoceptive processes (Michael and Naveteur 2011; Michael et al. 2012) since they are essential for conscious awareness of the body (Cameron 2002). If we take a closer look at the qualitative aspects of SPS that underwent change, it is noteworthy that movement diminished reliably those SPS that could be classified as surface tactile/mechanical and those classified as originating deep within the hand. This finding makes this investigation the first one to report gating of interoception, either in its broad sense (i.e., including both categories) or its narrow sense (i.e., only the second category; Vaitl 1996; Cameron 2002; Craig 2003). It is not clear to the authors why thermal sensations did not undergo any change. One possibility is that these sensations do not interfere with movement and, therefore, there is no real need to suppress them. Given the overall decrement in the spatial extent, the intensity and the variety of SPS, one might ask whether people with heightened or disordered awareness of bodily sensations (e.g., anxiety, depression, somatoform disorders; Brown 2004; Brown et al. 2010; Paulus and Stein 2010) perceive SPS differently and whether they could benefit from the attenuation of interoceptive sensations. Indeed, in some instances they interpret normal bodily sensations as being the symptoms of serious medical diseases because of heightened or distorted attentional focus on them (Barsky et al. 1988). This, of course, opens the gates for further investigations of SPS, their determinants, and their disturbances. Tactile stimulation and SPS Moving the thumb does not produce only pure movement. Tactile sensations are elicited too. Do such sensations

Gating of spontaneous somatic sensations by movement

119

contribute to the gating of SPS and if yes, to what degree? Experiment 2 showed that, in the absence of any movement, the continuous presence of a rubber annulus on the thumb during the 10-s periods of testing produced effects that went in an opposite direction to what was observed with movement: it increased the frequency and the variety of SPS. Therefore, the results of Experiment 1 cannot be attributed to tactile sensations elicited by movement, but rather to movement itself. An interesting finding in Experiment 2 was that the presence of the tactile stimulus did not change the perceived intensity of SPS, and the perceived intensity of that tactile stimulus did not correlate with the intensity of SPS. This suggests that the origin of these two phenomena might be different and gives some support to the idea that SPS are more likely to be interoceptive cues (Naveteur et al. 2005; Michael and Naveteur 2011; Michael et al. 2012). Lateral effects As mentioned earlier, our previous investigations suggested that perception of SPS depends on processes that are lateralized to the right cerebral hemisphere (Naveteur et al. 2005; Michael and Naveteur 2011; Michael et al. 2012). This was proposed because an overall dominance of the left hand is found in right-handers. A similar dominance was found in Experiment 2 of the present study, and this strengthens the right-hemisphere hypothesis. Whether the absence of such a dominance in Experiment 1 comes from the introduction of movement is not clear. Limits and conclusions One of the limits of the present study is the women:men ratio. Would the results be the same if the number of women and men were the same? In other words, do women and men perceive SPS equally well? Even though gender was not a factor of interest for our investigation, and even though the similarity in the women:men ratio between the present study and our two previous investigations allows us to make direct comparisons and facilitates the interpretation of the results, it might be expected that women behave somehow differently than men. Indeed, one frequent, albeit not universal finding of studies on interoceptive awareness is that men perform better than women (e.g., Katkin et al. 1981). Future research should specifically target gender differences in the perception of SPS. Another limit is inherent to the methodology of the investigation of SPS. The possibility that some of the effects of movement on SPS were due to the contact between the hand and the table surface cannot be ruled out. However, such an explanation cannot account for the absence of effect of movement on the palm, which was the hand segment that made the greatest contact with the table. We are, therefore, confident that our results mainly reflect the way movement modifies the perception of SPS. Our findings on SPS suggest movement may exert similar influences as in the case of exteroceptive sensations, in other words it reduces our perception of SPS. We also found that gating of SPS by movement concerns all fingers that are not moving, which suggests that inhibitory activity at a cortical level is probably widespread and massive compared to inhibition that may occur at more peripheral levels. Finally,

120

R. Beaudoin & G. A. Michael

gating is differently modulated as a function of the phalanx. Will future research on somesthesis and exteroception obtain the same result as for SPS? Understanding at what level— peripheral, central, or both—our perception of SPS is established is an exciting prospect, but one difficult to fathom because all we have are behavioral data. Future research using psychophysiological and imaging techniques would yield some seminal answers to this riddle.

Acknowledgements We would like to express our gratitude to Madeline Mechin for her valuable help in collecting some of the data presented here. This work was supported by the LABEX CORTEX (ANR-11-LABX-0042) of Universite´ de Lyon, within the program ‘‘Investissements d’Avenir’’ (ANR-11-IDEX-0007) operated by the French National Research Agency (ANR).

Declaration of interest The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper.

Notes 1. Paired proportions can be compared using Liddell’s exact test (Liddell 1983), which is preferable to the more classically used McNemar’s chi-squared test because it overrides the requirements of minimal cell values and minimal number of participants. Liddell’s exact test is a special case of the sign test. The b count in a 2  2 table is treated as a binomial variable from the sample b + c, where b represents the present–absent cell and c the absent–present cell. Test statistic F ¼ b/(c + 1) and it follows the Fischer distribution with n and d degrees of freedom, n being the total number of observations and d being the absent–absent cell. In this study, F-values were calculated for each individual cell during comparisons of two binary maps. 2. A more global analysis of variance taking into account both the fingers and anatomical segments could not be performed because it is not possible to divide the palm into sub-segments equivalent to the phalanges.

References Abbruzzese G, Ratto S, Favale E, Abbruzzese M. 1981. Proprioceptive modulation of somatosensory evoked potentials during active or passive finger movements in man. J Neurol Neurosurg Psychiatry 44: 942–949. Barsky A, Goodson J, Lane R, Cleary P. 1988. The amplification of somatic symptoms. Psychosom Med 50:510–519. Brown PB, Koerber HR, Millecchia R. 2004. From innervation density to tactile acuity 1. Spatial representation. Brain Res 1011:14–32. Brown RJ. 2004. Psychological mechanisms of medically unexplained symptoms: An integrative conceptual model. Psychol Bull 130: 793–812. Brown RJ, Danquah AN, Miles E, Holmes E, Poliakoff E. 2010. Attention to the body in nonclinical somatoform dissociation depends on emotional state. J Psychosom Res 69:249–257. Cameron OG. 2002. Visceral sensory neuroscience. New York: Oxford University Press. Cohen L, Starr A. 1987. Localization, timing and specificity of gating of somatosensory evoked potentials during active movement in man. Brain 110:451–467. Coquery J-M, Coulmance M, Leron M-C. 1972. Modifications des potentiels e´voque´s corticaux somesthe´siques durant des mouvements actifs et passifs chez l’homme. Electroencephal Clin Neurophysiol 33: 269–276. Craig AD (Bud). 2003. Interoception: The sense of the physiological condition of the body. Curr Opin Neurobiol 13:500–505.

Somatosens Mot Res, 2014; 31(3): 111–121

Craig AD (Bud). 2004. Human feelings: Why are some more aware than others? Trends Cogn Sci 8:239–241. Fromm C, Evarts EV. 1982. Pyramidal tract neurons in somatosensory cortex: Central and peripheral inputs during voluntary movement. Brain Res 238:186–191. Gallace A, Spence C. 2014. In touch with the future: The sense of touch from cognitive neuroscience to virtual reality. Oxford: Oxford University Press. Harper DE, Hollins M. 2012. Is touch gating due to sensory or cognitive interference? Pain 153:1082–1090. Insola A, Le Pera D, Restuccia D, Mazzone P, Valeriani M. 2004. Reduction in amplitude of the subcortical low- and highfrequency somatosensory evoked potentials during voluntary movement: An intracerebral recording study. Clin Neurophysiol 115: 104–111. Insola A, Padua L, Mazzone P, Valeriani M. 2010. Effect of movement on SEPs generated by dorsal column nuclei. Clin Neurophysiol 121: 921–929. Johansson RS, Vallbo A. 1979a. Detection of tactile stimuli. Thresholds of afferent units related to psychophysical thresholds in the human hand. J Physiol 297:405–422. Johansson RS, Vallbo AB. 1979b. Tactile sensibility in the human hand: Relative and absolute densities of four types of mechanoreceptive units in glabrous skin. J Physiol 286:283–300. Jones SJ, Halonen J-P, Shawkat F. 1989. Centrifugal and centripetal mechanisms involved in the ‘‘gating’’ of cortical SEPs during movement. J Neurol Sci 128:195–204. Katkin ES, Blascovich J, Goldband S. 1981. Empirical assessment of visceral self-perception: Individual and sex differences in the acquisition of heartbeat discrimination. J Pers Soc Psychol 40: 1095–1101. Kinsbourne M. 1998. Awareness of one’s own body: An attentional theory of its nature, development, and brain basis. In: Bermu´dez J, editor. The body and the self. Cambridge, MA: MIT Press. pp 205–223. Kulldorff M. 1997. A spatial scan statistic. Commun Statist 26: 1481–1496. Liddell FDK. 1983. Simplified exact analysis of case-referent studies: Matched pairs; dichotomous pairs. J Epidemiol Community Health 37:82–84. Macefield G, Gandevia S, Burke D. 1990. Perceptual responses to microstimulation of single afferents innervating joints, muscles and skin of the human hand. J Physiol 429:113–129. Marin˜o J, Martinez L, Canedo A. 1999. Sensorimotor integration at the dorsal column nuclei. New Physiol Sci 14:231–237. Michael GA, Naveteur J. 2011. The tickly homunculus and the origins of spontaneous sensations arising on the hands. Conscious Cogn 20: 603–617. Michael GA, Deleuze A, Humblot M, Simon B, Dupuy M-A, Naveteur J. 2012. Interacting effects of vision and attention in perceiving spontaneous sensations arising on the hands. Exp Brain Res 216: 21–34. Mirams L, Poliakoff E, Brown RJ, Lloyd DM. 2010. Vision of the body increases interference on the somatic signal detection task. Exp Brain Res 202:787–794. Naveteur J, Honore´ J, Michael GA. 2005. How to detect an electrocutaneous shock that is not delivered? Overt spatial attention influences decision. Behav Brain Res 165:254–261. Nun˜ez A, Malmierca E. 2007. Corticofugal modulation of sensory information. Adv Anat Embryol Cell Biol 187:1–74. Ochoa J, Torebjo¨rk R. 1983. Sensations evoked by intraneural microstimulation of single mechanoreceptor units innervating the human hand. J Physiol 342:633–654. Oldfield RC. 1971. The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia 9:97–113. Panetsos F, Nun˜ez A, Avendan˜o C. 1998. Sensory information processing in the dorsal column nuclei by neuronal oscillators. Neuroscience 84:635–639. Papakostopoulos D, Cooper R, Crow HJ. 1975. Inhibition of cortical evoked potential and sensation by self-initiated movement in man. Brain 104:465–491. Paulus MP, Stein MB. 2010. Interoception in anxiety and depression. Brain Struct Funct 214:451–463. Penfield W, Jasper H. 1954. Epilepsy and the functional anatomy of the brain. London: Churchill.

DOI: 10.3109/08990220.2014.888992

Rossini PM, Babiloni C, Babiloni F, Ambrosini A, Onorati P, Carducci F, Urbano A. 1999. ‘‘Gating’’ of human short-latency somatosensory evoked cortical responses during execution of movement. A high resolution electroencephalography study. Brain Res 843: 161–170. Rushton DN, Rothwell JC, Craggs MD. 1981. Gating of somatosensory evoked potentials during different kinds of movement in man. Brain 104:465–491. Schady WJL, Rorebjo¨rk HE, Ochoa JM. 1983. Cerebral localisation function from the input of single mechanoreceptive units in man. Acta Physiol Scand 119:277–285. Schmidt RF, Schady WJL, Torebjo¨rk HE. 1990a. Gating of tactile input from the hand, I. Effects of finger movement. Exp Brain Res 79: 97–102. Schmidt RF, Schady WJL, Torebjo¨rk HE. 1990b. Gating of tactile input from the hand, II. Effects of remote movements and anaesthesia. Exp Brain Res 79:103–108. Seki K, Perlmutter SI, Fetz EE. 2003. Sensory input to primate spinal cord is presynaptically inhibited during voluntary movement. Nat Neurosci 6:1309–1316. Semmes J. 1965. A non-tactual factor in astereognosis. Neuropsychologia 3:295–315. Serino A, Farne` A, Rinaldesi ML, Haggard P, La`davas E. 2007. Can vision of the body ameliorate impaired somatosensory function? Neuropsychologia 45:1101–1107. Singer W. 2001. Consciousness and the binding problem. Ann NY Acad Sci 929:123–146.

Gating of spontaneous somatic sensations by movement

121

Song W, Francis JT. 2013. Tactile information processing in primate hand somatosensory cortex (S1) during passive arm movement. J Neurophysiol 110:2061–2070. Starr A, Cohen L. 1985. ‘‘Gating’’ of somatosensory evoked potentials begins before the onset of voluntary movement in man. Brain Res 348: 183–186. Vaitl D. 1996. Interoception. Biol Psychol 42:1–27. Valeriani M, Insola A, Restuccia D, Le Pera D, Mazzone P, Altibrandi MG, Tonali P. 2001. Source generators of the early somatosensory evoked potentials to tibial nerve stimulation: An intracerebral and scalp recording study. Clin Neurophysiol 112:1999–2006. Vallbo AB, Johansson RS. 1984. Properties of cutaneous mechanoreceptors in the human hand related to touch sensation. Hum Neurobiol 3:3–14. Voisin JI, Rodrigues EC, He´tu S, Jackson PL, Vargas CD, Malouin F, Chapman CE, Mercier C. 2011. Modulation of the response to a somatosensory stimulation of the hand during the observation of manual actions. Exp Brain Res 208:11–19. Wasaka T, Kida T, Nakata H, Akatsuka K, Kakigi R. 2007. Characteristics of sensori-motor interaction in the primary and secondary somatosensory cortices in humans: A magnetoencephalography study. Neuroscience 149:446–456. Weisz N, Dohrmann K, Elbert T. 2007. The relevance of spontaneous activity for the coding of the tinnitus sensation. Prog Brain Res 166: 61–70. Williams SR, Shenasa J, Chapman CE. 1998. Time course and magnitude of movement-related gating of tactile detection in humans. I. Importance of stimulus location. J Neurophysiol 79:947–963.

Copyright of Somatosensory & Motor Research is the property of Taylor & Francis Ltd and its content may not be copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written permission. However, users may print, download, or email articles for individual use.

Gating of spontaneous somatic sensations by movement.

Movement is known to attenuate the perception of tactile stimuli delivered on the moving part of the body, and this gating diminishes the greater the ...
940KB Sizes 2 Downloads 3 Views