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Psychophysical 'perceptual maps' of heat and pain sensations by direct localization of CO2 laser stimuli on the skin

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  • Akademie für angewandte Bewegungswissenschaften gGmbH

Abstract

Brain activation patterns derived from neurofunctional methods are often implicitly regarded as being directly related to subjective perceptual experience in an iso- or at least homomorph manner, neglecting the operational differences between these two dimensions. This paper (a) introduces a method for assessing 'perceptual maps' of stimulation patterns presented to the body surface, providing a means to parametrically relate neural representation and subjective percept, and (b) applies this method to demonstrate the existence of 'somatotopic maps' of hot and painful stimulus patterns independent from mechanoceptive co-activation. Brief (90 ms) CO2 laser pulses were presented in an array of multiple stimulation sites on the dorsal forearms (N. radialis area, C7 dermatome) of healthy subjects. Perceived locations were indicated with a 3D tracker without touching the skin, and (mis-)localizations in distal-proximal direction were analyzed. Stimuli were localized with overall mean errors of 22 mm (SD: 16 mm) toward the wrist and 24 mm (SD: 18 mm) toward the elbow. Somatotopic representation of thermal-nociceptive stimuli could be demonstrated in all subjects, independent from mechanoceptive co-activation. The perceptual maps revealed striking individual (mis-)localization patterns, many subjects exhibiting 'stretched', some 'condensed' somatotopic representations. In estimating the mapping parameters from physical to perceptual space linear regressions generally provided a good fit (adj. R2>0.80 in 10 out of 12 subjects). Nonlinear models were advantageous in some subjects only. Our method can be useful in assessing inter-individual differences or experimentally induced shifts in somatotopic processing.
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... Haggard, 2011), tactile localization (e.g., Trojan et al., 2006;Mancini, Longo, Iannetti, & Haggard, 2011), and judgments of the configuration of landmarks within the hand (e.g., Longo, 2015a;Margolis & Longo, 2015). ...
Article
Our body is a volumetric, 3-dimensional object in the world, and we experience it as such. Existing methods for measuring the perceptual body image, however, have been based on judgments of 1-dimensional length or 2-dimensional images. We developed a new approach to the 3-D perceptual body image of the fingers by asking people to judge whether each finger would fit through rings of varying diameter. This task requires participants to conceptualize their finger as a volumetric object entering the ring. In two experiments, we used an adaptive staircase procedure to estimate the perceived size of each finger. There were systematic distortions of perceived 3-D finger size, with the size of index finger and (to a lesser extent) the middle finger underestimated. These distortions were unaffected by changes in hand posture. Notably, the pattern of distortions is qualitatively different from that found in previous research investigating 1-D finger length, suggesting that 3-D judgments of the body may differ in fundamental ways from 1-D judgments of individual body dimensions.
... Similar distortions have also been observed in tasks involving manipulating images of one's own face (D'Amour & Harris, 2017), judging the relative location of body landmarks Fuentes, Pazzaglia, Longo, Scivoletto, & Haggard, 2013;Fuentes, Runa, Blanco, Orvalho, & Haggard, 2013), drawings of one's face (Bianchi, Savardi, & Bertamini, 2008;Carbon & Wirth, 2014), judgments of arm length (Linkenauger, Witt, Bakdash, Stefanucci, & Proffitt, 2009), judgments of the relative lengths of body parts ( Linkenauger et al., 2015;Linkenauger, Kirby, McCulloch, & Longo, 2017;Sadibolova, Ferrè, Linkenauger, & Longo, 2019), and judgments of the internal configuration of landmarks within the hand (Ambroziak, Tamè, & Longo, 2018;Longo, 2015c;Margolis & Longo, 2015). Other studies have reported systematic distortions underlying somatosensory processing, for example in tactile localisation (Culver, 1970;Mancini, Longo, Iannetti, & Haggard, 2011;Medina, Tamè, & Longo, 2018;Sadibolova, Tamè, Walsh, & Longo, 2018;Steenbergen, Buitenweg, Trojan, Klaassen, & Veltink, 2012;Trojan et al., 2006) and tactile distance perception (e.g., Cholewiak, 1999;Fiori & Longo, 2018;Green, 1982;Longo, Ghosh, & Yahya, 2015;Longo & Golubova, 2017;Taylor-Clarke, Jacobsen, & Haggard, 2004). While the link between these distortions in healthy populations and those found in clinical disorders remains unknown, this body of research does demonstrate that distorted representations of the body are a ubiquitous part of ordinary mental life. ...
Article
A large body of research has suggested that localisation of the hand in external space relies on distorted representations of the hand. We developed a paradigm for measuring implicit perceptual maps of the hand (Longo & Haggard, 2010, Proc Natl Acad Sci USA, 107, 11727–11732), which show systematic deviation from actual hand shape, including overestimation of hand width and underestimation of finger length. Recently, Coelho and Gonzalez (in press, Psychol Res) reported sex differences in these perceptual hand maps, with women showing greater overestimation of hand width, but less underestimation of finger length than men. In the current study, I conducted a meta-analysis of 19 experiments using this paradigm by myself and my colleagues. The results replicated the sex differences reported by Coelho and Gonzalez. Importantly, however, these sex differences were not apparent when actual hand size was included as a covariate in analyses, suggesting that they may, at least in part, be due to women having smaller hands on average than men.
... This finding could be linked to pruritogen-induced heat hyperalgesia, but it more likely represents an anatomical difference in heat sensitivity considering the uniform results in heat-evoked pain between intra-versus homotopical stimulation. [15][16][17] ...
Article
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Background Chronic itch is notoriously difficult to treat. Counter‐stimuli are able to inhibit itch, but this principle is difficult to apply in clinical practice, and the mechanisms behind counter‐stimulation‐induced itch suppression in humans are unclear. Objectives 1) To analyse the stimulus‐response effects of transient heat stimuli on histaminergic and non‐histaminergic itch; 2) to investigate whether the antipruritic effect depends on homotopic (peripheral mediation) versus heterotopic (central mediation) counter‐stimulation relative to the itch provocation site. Methods 18 healthy subjects (8 females, 25.7±0.8 y.o.) participated. Itch was evoked on pre‐marked areas of the volar forearms, by either histamine (1% solution), or cowhage (35‐40 spicules). In addition to the itch provocations (Experiment 1), 5‐seconds homotopic heat stimuli of 32, 40, 45 or 50°C were applied. In Experiment 2, heat stimuli were applied either homotopically, intra‐segmentally (next to the provocation site), or extra‐segmentally (dorsal forearm). Itch intensity was evaluated throughout the procedures using a digital Visual Analog Scale. Results Homotopic counter‐stimuli inhibited histaminergic itch by 41.27% at 45°C (p<0.01), and by 76.66% at 50°C (p<0.0001). Cowhage‐induced itch was less prone to counter‐stimulation and was only significantly diminished at 50°C by 43.60% (p=0.009). Counter‐stimulations applied heterotopically were not able to significantly inhibit itch. Conclusions Itch pathway‐specific effects of counter‐stimuli were observed between homo‐ and heterotopic stimulation. Histaminergic itch was robustly inhibited by short‐term homotopic noxious heat stimuli for up to 10 minutes. Non‐histaminergic itch was only weakly inhibited. The inhibitory effects exerted by the short‐term heat stimuli only occurred following homotopical counter‐stimulation. This article is protected by copyright. All rights reserved.
... Interestingly, even the localization of static, tactile events (e.g., a tap on the skin) is not always error-free. It has, for example, often been reported that a static tactile stimulus may be systematically misperceived at a different spatial location (Harrar & Harris, 2009;Ho & Spence, 2007;Longo, 2017;Mancini, Longo, Iannetti, & Haggard, 2011;Margolis & Longo, 2015;Steenbergen, Buitenweg, Trojan, & Veltink, 2014;Trojan et al., 2006; see Medina & Coslett, 2016, for a discussion). Even on the hand and fingers, locations that are very sensitive to two-point discrimination and localization (see Gallace & Spence, 2014;Stevens & Choo, 1996;Weinstein, 1968), systematic mislocalizations have been documented (e.g., Mancini et al., 2011;Margolis & Longo, 2015). ...
Article
We report two experiments designed to investigate how the implied motion of tactile stimuli influences perceived location. Predicting the location of sensory input is especially important as far as the perception of, and interaction with, the external world is concerned. Using two different experimental approaches, an overall pattern of localization shifts analogous to what has been described previously in the visual and auditory modalities is reported. That is, participants perceive the last location of a dynamic stimulus further along its trajectory than is objectively the case. In Experiment 1, participants judged whether the last vibration in a sequence of three was located closer to the wrist or to the elbow. In Experiment 2, they indicated the last location on a ruler attached to their forearm. We further pinpoint the effects of implied motion on tactile localization by investigating the independent influences of motion direction and perceptual uncertainty. Taken together, these findings underline the importance of dynamic information in localizing tactile stimuli on the skin.
... Similar distortions have also been observed in tasks involving manipulating images of one's own face (D'Amour & Harris, 2017), judging the relative location of body landmarks Fuentes, Pazzaglia, Longo, Scivoletto, & Haggard, 2013;Fuentes, Runa, Blanco, Orvalho, & Haggard, 2013), drawings of one's face (Bianchi, Savardi, & Bertamini, 2008;Carbon & Wirth, 2014), judgments of arm length (Linkenauger, Witt, Bakdash, Stefanucci, & Proffitt, 2009), judgments of the relative lengths of body parts ( Linkenauger et al., 2015;Linkenauger, Kirby, McCulloch, & Longo, 2017;Sadibolova, Ferrè, Linkenauger, & Longo, 2019), and judgments of the internal configuration of landmarks within the hand (Ambroziak, Tamè, & Longo, 2018;Longo, 2015c;Margolis & Longo, 2015). Other studies have reported systematic distortions underlying somatosensory processing, for example in tactile localisation (Culver, 1970;Mancini, Longo, Iannetti, & Haggard, 2011;Medina, Tamè, & Longo, 2018;Sadibolova, Tamè, Walsh, & Longo, 2018;Steenbergen, Buitenweg, Trojan, Klaassen, & Veltink, 2012;Trojan et al., 2006) and tactile distance perception (e.g., Cholewiak, 1999;Fiori & Longo, 2018;Green, 1982;Longo, Ghosh, & Yahya, 2015;Longo & Golubova, 2017;Taylor-Clarke, Jacobsen, & Haggard, 2004). While the link between these distortions in healthy populations and those found in clinical disorders remains unknown, this body of research does demonstrate that distorted representations of the body are a ubiquitous part of ordinary mental life. ...
... Fuentes et al., 2013;, nociception (e.g. Mancini et al., 2011;Trojan et al., 2006) and touch (e.g. Steenbergen et al., 2012). ...
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Body image disturbance is a key symptom of Anorexia Nervosa (AN). Previous studies found that women with AN overestimate their body size in comparison with healthy controls (HC), at least for unimodal measures involving either only visual input (e.g. distorted photographs technique) or only tactile input (e.g. tactile distance tasks). Distorted body representations are hypothesized to cause this misperception in AN. We here tested whether this overestimation remains present in a novel one-point-localization (OPL) task involving the mapping of a tactile stimulus onto a visual image. Two experiments compared the ability of 27 women with AN and 40 HC to accurately localize a tactile stimulus on a live image of their body. Women with AN and HC did not differ in their performance. Instead, participants in both groups showed systematic distortions in their localization performance. This study suggests that the mapping of a tactile stimulus does not involve a distorted body representation in women with AN compared to HC.
... The distortions we show for the body structural description contribute to a growing literature showing that far from being a sure sign of pathology, distorted body representations are a normal part of healthy cognitive life (for a recent review see Longo, 2017). As mentioned in the introduction, recent results have revealed large and stereotyped distortions underlying perceptual abilities including position sense (e.g., Ferrè, Vagnoni, & Haggard, 2013;Lopez, Schreyer, Preuss, & Mast, 2012), tactile distance perception (e.g., Anema, Wolswijk, Ruis, & Dijkerman, 2008;Taylor-Clarke, Jacobsen, & Haggard, 2004), localization of somatosensory stimuli (e.g., Mancini, Longo, Iannetti, & Haggard, 2011;Medina, Tamè, & Longo, in press;Trojan et al., 2006), and even more abstract processes such as the conscious body image (e.g., Fuentes, Longo, & Haggard, 2013;Linkenauger et al., 2015;Longo & Haggard, 2012). ...
Article
Previous studies showed stereotyped distortions in hand representations. People judge their knuckles as farther forward in the hand than they actually are. The cause of this bias remains unclear. We tested whether both visual and tactile information contribute to the bias. In Experiment 1, participants judged the location of their knuckles by pointing to the location on their palm with: (1) a metal baton (using vision and touch), (2) a metal baton while blindfolded (using touch), or (3) a laser pointer (using vision). Distal mislocalisations were found in all conditions. In Experiment 2, we investigated whether judgments are influenced by visual landmarks such as creases. Participants localized their knuckles on either a photograph of their palm or a silhouette. Distal mislocalisations were apparent in both conditions. These results show that distal biases are resistant to changes in stimulus information, suggesting that such mislocalisations reflect a conceptual mis-representation of hand structure.
... This tendency would fit with the results of the present study. Interestingly, when no motion was present, the elbow and wrist served as 'anchors', resulting in an elongated representation of the forearm (Trojan et al. 2006), of potential interest also for the findings by Brugger and Meier (2015). The elongated representation would be consistent with overestimated trajectories in the visual (Actis- Grosso, & Stucchi, 2003;Hubbard, & Motes, 2002) modality. ...
Article
Full-text available
The displacement of the final position of a moving object in the direction of the observed motion path, i.e. an overestimation, is known as representational momentum. It has been described both in the visual and the auditory domain, and is suggested to be modality-independent. Here, we tested whether a representational momentum can also be demonstrated in the somatosensory domain. While the cognitive literature on representational momentum suggests that it can, previous work on the psychophysics of tactile motion perception would rather predict an underestimat ion of the perceived endpoint of a tactile stimulus. Tactile motion stimuli were applied on the left and the right dorsal forearms of 32 healthy participants, who were asked to indicate the subjectively perceived endpoint of the stimulation. Velocity, length and direction of the trajectory were varied. Contrary to the prediction based on the representational momentum literature, participants in our experiment significantly displaced the endpoint agai nst the direction of movement (underestimation). The results are thus compatible with previous psychophysical findings on the perception of tactile motion.Further studies combining paradigms from classical psychophysics and cognitive psychology will be needed to resolve the apparently paradoxical predictions by the two literatures. Full text: http://rdcu.be/tjFI
... Several previous studies have attempted to construct perceptual maps of the body, for example by measuring patterns of proprioceptive localization of body parts (e.g., , localization of individual somatic stimuli in both skincentered (e.g., Mancini, Longo, Iannetti, & Haggard, 2011;Rapp, Hendel, & Medina, 2002) and external (e.g., Longo, Mancini, & Haggard, 2015;Trojan et al., 2006) frames of reference, and localization of body parts relative to an anchor part (e.g., Fuentes, Pazzaglia, Longo, Scivoletto, & Haggard, 2013). In each of these cases, perceptual maps were constructed directly, in the sense that participants were asked to make overt judgments of perceived location in some external frame of reference. ...
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A large body of research has shown spatial distortions in the perception of tactile distances on the skin. For example, perceived tactile distance is increased on sensitive compared to less sensitive skin regions, and larger for stimuli oriented along the medio-lateral axis than the proximo-distal axis of the limbs. In this study we aimed to investigate the spatial coherence of these distortions by reconstructing the internal geometry of tactile space using multidimensional scaling (MDS). Participants made verbal estimates of the perceived distance between two touches applied sequentially to locations on their left hand. In Experiment 1 we constructed perceptual maps of the dorsum of the left hand, which showed a good fit to the actual configuration of stimulus locations. Critically, these maps also showed clear evidence of spatial distortion, being stretched along the medio-lateral hand axis. Experiment 2 replicated this result and showed that no such distortion is apparent on the palmar surface of the hand. These results show that distortions in perceived tactile distance can be characterized by geometrically simple and coherent deformations of tactile space. We suggest that the internal geometry of tactile space is shaped by the geometry of receptive fields in somatosensory cortex.
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