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Frames of Reference for Mapping Tactile Stimuli in Brain-Damaged Patients

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Frames of Reference for Mapping Tactile Stimuli in Brain-Damaged Patients Frames of Reference for Mapping Tactile Stimuli in Brain-Damaged Patients Salvatore Aglioti Università di Verona, Italy Nicola Smania Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/11/1/67/1758506/089892999563256.pdf by guest on 18 May 2021 Policlinico Borgo Roma, Verona, Italy Andrea Peru Università di Verona, Italy Abstract ■ Twelve normal controls, twelve left-brain-damaged patients, detected contralesional stimuli with higher accuracy in crossed and thirty-six right-brain-damaged patients with or without than in anatomical position. This result suggests that, in these tactile extinction or tactile neglect were asked to report light patients, impairments in detecting contralesional stimuli can touches delivered to the left or the right hand or simultane- be due not only to sensory but also to spatial factors contingent ously to both hands. The hands could be in anatomic position upon the position of the hands. There was no interaction or one hand could cross over the other. Moreover, the two between the effect of crossing the hands and the hemispace hands could be in the left or the right hemispace or across the where the crossing took place. This suggests that coding the corporeal midline. Controls and nontactile-extinction groups position of a hand as left or right does not necessarily occur performed better when the hands were in anatomical than in in relation to the bodily midline, but it may arise from the crossed position. By contrast, patients with tactile extinction computation of the position of the other hand. ■ INTRODUCTION Toni, 1996), somatic stimuli are more likely to be coded in terms of egocentric reference frames. Within the ego- The process of coding sensory signals in space (and centric frame of reference, however, different anchors acting toward them) can take place in reference to for coding a given stimulus (or for implementing a given different systems of coordinates. Stimuli mapped accord- motor act toward the stimulus) may be used. In different ing to egocentric frames of reference are deªned in experimental conditions, for example, the center of the relation to the viewer’s body. Egocentric codes stem egocentric system may be localized at different loci from continuously updated static and dynamic somato- within the body architecture. Thus, it may be head-, sensory signals that tune the motor apparatus. They cor- shoulder-, trunk-centered, and so on (Colby, 1998). The respond to a sensorimotor mode of processing spatial position of the body relative to gravitational forces, the information and beneªt from a direct dialogue with the status of the systems monitoring the position of the physical world (Paillard, 1991). Stimuli mapped in allo- body in space (e.g., vestibular system and proprioceptive centric frames of reference are deªned in terms of ob- receptors) or subserving corporeal awareness, the posi- jects or other landmarks in the external world. tion of the locus where a stimulus is delivered in rela- Allocentric representations include both world- and ob- tionship to the corporeal midline, or other corporeal ject-centered frames of reference (Andersen, Snyder, Li, segments, may be other relevant variables (Pizzamiglio, & Stricanne, 1993; Behrmann & Moscovitch, 1994; Driver, Vallar, & Doricchi, 1997; Vallar, 1997). Insights into the Baylis, Goodrich, & Rafal, 1994; Olson & Gettner, 1995). type of coordinate systems for spatial analysis of sensory These representations can be described as memory signals come from studies of unilateral brain lesions based, internal constructs that extract features of the inducing behavioral disorders like neglect for the con- visual world that remain stable when the body moves tralesional space. It has been shown, for example, that (Paillard, 1991). Although visual stimuli may be coded in visual neglect may arise in reference to several coordi- terms of ego- or world-centered frames of reference nate systems such as the corporeal midline, the relative (Blouin et al., 1993; Gentilucci, Chiefª, Daprati, Saetti, & position of head and eyes with respect to the trunk, or © 1999 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 11:1, pp. 67–79 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/089892999563256 by guest on 28 September 2021 the retinal position with respect to gaze direction (Cal- stimuli in the extrapersonal and personal space (spatio- vanio, Petrone, & Levine, 1987; Farah, Brunn, Wong, Wal- topic frame-of-reference hypothesis), a consistent differ- lace, & Carpenter, 1990; Karnath, Schenkel, & Fischer, ence of accuracy in the different experimental situations 1991; Làdavas, 1987; Mennemeier, Chatterjee, & Heilman, should be observed. We attempted to tell these two 1994). Most of the studies, however, have investigated components apart by testing whether or not the accu- what reference frames are used for building complex racy of left- and right-brain-damaged patients in detecting spatial maps of the extrapersonal space from visual in- tactile stimuli delivered to their contralesional hand formation. By contrast, the issue of what reference changed according to the relationships of the two hands frames are used for transforming tactile and propriocep- and the hemispace in which the hands are positioned. tive signals in spatial higher-order maps of peripersonal We used different stimulation conditions whereby single Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/11/1/67/1758506/089892999563256.pdf by guest on 18 May 2021 and personal space have hitherto been largely unad- or double light touches delivered to the left or right dressed. hand or both hands had to be detected (1) when the In patients with neglect and tactile extinction, hands were in anatomical (Figure 1, right column) or in Moscovitch and Behrmann (1994) delivered somatic crossed position (Figure 1, left column) and (2) when stimuli to the ulnar (on the side of the little ªnger) and the hands were on opposite sides of the corporeal the radial (on the side of the thumb) surface of the left midline (Figure 1, upper part) or in the right or the left or the right wrist. The hand, always kept on the same hemispace (Figure 1, middle and lower parts, respec- side of the corporeal midline, was tested in both the tively). palm up and the palm down position; thus, each stimu- In particular, we examined whether crossing the lated point was coded as ipsilesional or contralesional hands brought about any changes in accuracy and if such according to the palm down or palm up position. Stimuli changes were related to the corporeal midline or also to delivered to the point coded as contralesional were other anchors for segmenting the personal space; ªnally, omitted regardless of palm orientation position, suggest- we tested whether the presence of the crossing effect ing a role for higher-order frames of reference in tactile was speciªcally related to the presence and degree of extinction. We have previously shown that the capability tactile extinction. To do so, we examined ªve groups of of right-brain-damaged (RBD) patients with neglect and experimental subjects: non brain-damaged subjects (C), tactile extinction to detect somatic stimuli delivered to left-brain-damaged patients (LBD), RBD patients without the left hand changed according to its location (Smania tactile extinction (RBD TE minus), RBD patients with & Aglioti, 1995). The number of correct detections for tactile extinction (RBD TE), and RBD patients with more stimuli delivered to the left hand was higher when this severe tactile extinction (RBD TE plus). hand crossed the corporeal midline than when it was in anatomical position. The effect turned out to be quite RESULTS clear under both single and double stimuli conditions and suggested that, in these patients, somaesthetic Nonbrain-Damaged Control Patients deªcits are linked not only to sensory factors but also to Under single stimuli conditions, C scored 100% of the a defective computation of body-centered coordinates, hits. Their performance in double stimulation condition, perhaps based upon the sagittal midplane. Although ego- however, was not errorless (Table 1). Correct reports in centric codes for left and right hemispaces are typically the double stimulation condition were entered in a 3 deªned in terms of the corporeal midline, this may not (hemispace: left hemispace, right hemispace, across the be the only anchor for coding as left or right the stimuli bodily midline) × 2 (hand: left and right) × 2 (position delivered to the body. An interesting issue is whether or of the hands: anatomical and crossed) repeated measures not the increase in accuracy of the contralesional hand analysis of variance (ANOVA). The signiªcance of the is related to the bodily midline or if it also occurs when position (F(1, 11) = 7.95, p = 0.017) was due to the the hands are crossed within one hemispace. In this higher accuracy in anatomical than in crossed position condition, coding the position of a stimulated hand may (percentage of the hits, 98 and 89.8, respectively). Nei- take place in relation to the other hand and not only in ther hemispace nor hand were signiªcant (F(1, 11) < 1 relation to the bodily midline. in both cases). The number of correct detections, in fact, Both somatotopic and spatial components may under- was comparable in the three space conditions (93.8% lie the somatosensory deªcits observed in brain- left hemispace, 93.9% across the midline, and 94.1% right damaged patients. If these deªcits are related
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