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Mechanisms Underlying Visuo-Spatial Amelioration of Neglect After Prism Adaptation
ABSTRACT MECHANISMS UNDERLYING VISUO-SPATIAL AMELIORATION OF NEGLECT AFTER PRISM ADAPTATION Valentina Angeli1,2, Francesca Meneghello3, Flavia Mattioli4 and Elisabetta Làdavas1,2 (1Centro di Neuroscienze Cognitive, Cesena, Italy; 2Dipartimento di Psicologia, Università degli Studi di Bologna, Bologna, Italy; 3Ospedale San Camillo, Venezia, Italy; 4Ospedali Civili di Brescia, Brescia, Italy)
INTRODUCTION Neglect patients tend to ignore or fail to respond to stimuli in the contralesional side of space (Heilman et al., 2000). In the last 30 years different rehabilitation approaches have been attempted to improve the recovery of neglect (Pizzamiglio et al., 1992; Làdavas et al., 1994). One recent procedure, reported by Rossetti et al. (1998), shows that a single, short-lasting period of visuo-motor adaptation (PA) to the shift of the visual field was efficacious in ameliorating visual neglect in a group of patients, when tested two hours after PA. The main focus of interest of this paper concerns the relationship between the amelioration of neglect induced by PA (Farnè et al., 2002; Frassinetti et al., 2002) and disturbance of eye movement behaviour (Chédru et al., 1973). The hypothesis is that prismatic adaptation induces eye deviation to the left, which facilitates the exploration of the left neglected side of space. Thus, the present paper reports a detailed examination of eye movements (the first saccade landing location in a letter string and the spatial distribution of fixation time as a function of letter position in words and non-words) made by a group of patients with visual neglect, before and after prism adaptation on a reading task. In addition, in order to verify whether the hypothesized eye movement improvement is due to a simple bias induced by PA in the direction of the gaze or to a more complex interaction between sensory stimulation and oculomotor deviation, neglect dyslexia patients with and without hemianopia were studied. SUBJECTS AND METHODS Subjects Fourteen right brain-damaged patients with left hemispatial neglect participated to the study. Half of the patients presented with hemianopia and the remaining half did not show visual field deficits. The time post-illness was similar in the two groups of patients [RNH-: mean 7.1 (± 7.03 months); RNH+: mean 6.4 (± 4.93 months)] as well as the Cortex, (2004) 40, 155-156
severity of neglect, as documented by the absence of a significant effect of Group (p < .07), when the performance of RNH– and RNH+ were compared in several neglect cancellation tests (bells, lines, letters and stars). Apparatus and Procedure A fixation cross was displayed on the computer screen and, immediately after, a letter string was presented for a maximum of 4000 msec. Subjects were asked to read aloud the letter string as soon as possible. Eye movements were recorded during the reading task, by using an infrared corneal reflection oculometer. Patients performed the reading task twice: before and immediately after PA. In the prism adaptation session patients were required to perform a pointing task, to left, centre and right stimuli (for a total of 90 trials), while wearing base-left wedge prisms inducing a 10° adaptation to a right prismatic shift of the visual field. RESULTS Prismatic adaptation and after-effect: both RNH– and RNH+ showed a similar degree of adaptation (0.01 and 0.12°; p = n.s.) and aftereffect (– 4.6 and – 4.5°; p = n.s.). Reading improvement: RNH- patients showed a reduction of errors after the treatment [54% (ranging from 29% to 88%) vs 39% (ranging from 8% to 67%), p < .017], whereas RNH+ patients did not show any improvement [98% (ranging from 88% to 100%) vs 98% (ranging from 92% to 100%)]. Eye movement exploration: In RNH- patients, the interaction Session x Side was significant, showing an increase of the left side eye exploration [46% (ranging from 32% to 58%) vs 55% (ranging from 44% to 64%), p < .02] and a decrease on the right side [22% (ranging from 15% to 28%) vs 17% (ranging from 7% to 24%), p < .06]. By contrast, RNH+ patients did not show a significant improvement in the pattern of eye movements after the treatment. First saccade landing location: Session was the sole significant factor in RNH– patients (– 0.12°
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vs.– 1°; p < .05) showing an increased tendency for the first saccade to land nearer the beginning of the string after the treatment. CONCLUSION The results showed that all the patients manifested both the adaptation and the after-effect. Moreover, RNH- patients showed an improvement of neglect dyslexia after PA, an increased left-sided exploration of the letter string and an increased amplitude of the first left-sided saccade. Thus due to the eye-hand coordination during the pointing task, a deviation of eye movements in the direction opposite to the prismatic shift, was found also in relation to the eye coordinate system. In contrast, RNH+ patients did not show any improvement of reading performance and the patterns of eye movement exploration before and after PA were not significantly different. These findings provide evidence that the oculomotor improvement found in RNH– is not due to a simple error induced by PA in the direction of gaze but can be better explained by a more complex interaction between sensory stimulation and oculomotor deviation. In RNH–, visual signal registration, although partial, may provide a signal to move the eye (and the focus of attention) toward the left-sided letters and, as a
consequence of the eye movement, detection of left-sided information improved. In contrast, in RNH+, the absence of a visual stimulation cannot trigger any reallocation of attention to its location and, as a consequence, no amelioration of neglect dyslexia was found. REFERENCES HEILMAN KM, WATSON RT and VALENSTEIN E. Neglect I: Clinical and anatomic issues. In M Farah, F Todd (Eds), Patient-based Approaches to Cognitive Neuroscience. Issues in Clinical and Cognitive Neuropsychology. Cambridge, MA: MIT Press, 2000, pp. 115-23. PIZZAMIGLIO L, ANTONUCCI G, JUDICA A, MONTENERO P, RAZZANO C and ZOCCOLOTTI P. Cognitive rehabilitation of the hemineglect disorders in chronic patients with unilateral right brain damage. Journal of Clinical and Experimental Neuropsychology, 14: 901-923, 1992. ROSSETTI Y, RODE G, PISELLA L, FARNÈ A, LI L, BOISSON D and PERENIN MT. Prism adaptation to a rightward optical deviation rehabilitates left hemispatial neglect. Nature, 395: 166-169, 1998. LÀVADAS E, MENGHINI G and UMILTÀ C. A rehabilitation study of hemispatial neglect. Cognitive Neuropsychology, 11: 75-95, 1994. FARNÈ A, ROSSETTI Y, TONIOLO S and LÀDAVAS E. Ameliorating neglect with prism adaptation: visuo-manual and visuo-verbal measures. Neuropsychologia, 40: 718-729, 2002. CHEDRU F, LEBLANC M and LHERMITTE F. Visual searching in normal and brain damaged subjects: Contribution to the study of unilateral inattention. Cortex, 9: 94-111, 1973. FRASSINETTI F, ANGELI V, MENEGHELLO F and LÀDAVAS E. Longterm amelioration of visuospatial neglect be prism adaptation. Brain, 125: 608-623, 2002. Valentina Angeli, Centro di Neuroscienze Cognitive, Via Comunale Sorrivoli 585 – 47023 Cesena (FC), Italy. E-mail: [email protected]
INTRODUCTION Neglect patients tend to ignore or fail to respond to stimuli in the contralesional side of space (Heilman et al., 2000). In the last 30 years different rehabilitation approaches have been attempted to improve the recovery of neglect (Pizzamiglio et al., 1992; Làdavas et al., 1994). One recent procedure, reported by Rossetti et al. (1998), shows that a single, short-lasting period of visuo-motor adaptation (PA) to the shift of the visual field was efficacious in ameliorating visual neglect in a group of patients, when tested two hours after PA. The main focus of interest of this paper concerns the relationship between the amelioration of neglect induced by PA (Farnè et al., 2002; Frassinetti et al., 2002) and disturbance of eye movement behaviour (Chédru et al., 1973). The hypothesis is that prismatic adaptation induces eye deviation to the left, which facilitates the exploration of the left neglected side of space. Thus, the present paper reports a detailed examination of eye movements (the first saccade landing location in a letter string and the spatial distribution of fixation time as a function of letter position in words and non-words) made by a group of patients with visual neglect, before and after prism adaptation on a reading task. In addition, in order to verify whether the hypothesized eye movement improvement is due to a simple bias induced by PA in the direction of the gaze or to a more complex interaction between sensory stimulation and oculomotor deviation, neglect dyslexia patients with and without hemianopia were studied. SUBJECTS AND METHODS Subjects Fourteen right brain-damaged patients with left hemispatial neglect participated to the study. Half of the patients presented with hemianopia and the remaining half did not show visual field deficits. The time post-illness was similar in the two groups of patients [RNH-: mean 7.1 (± 7.03 months); RNH+: mean 6.4 (± 4.93 months)] as well as the Cortex, (2004) 40, 155-156
severity of neglect, as documented by the absence of a significant effect of Group (p < .07), when the performance of RNH– and RNH+ were compared in several neglect cancellation tests (bells, lines, letters and stars). Apparatus and Procedure A fixation cross was displayed on the computer screen and, immediately after, a letter string was presented for a maximum of 4000 msec. Subjects were asked to read aloud the letter string as soon as possible. Eye movements were recorded during the reading task, by using an infrared corneal reflection oculometer. Patients performed the reading task twice: before and immediately after PA. In the prism adaptation session patients were required to perform a pointing task, to left, centre and right stimuli (for a total of 90 trials), while wearing base-left wedge prisms inducing a 10° adaptation to a right prismatic shift of the visual field. RESULTS Prismatic adaptation and after-effect: both RNH– and RNH+ showed a similar degree of adaptation (0.01 and 0.12°; p = n.s.) and aftereffect (– 4.6 and – 4.5°; p = n.s.). Reading improvement: RNH- patients showed a reduction of errors after the treatment [54% (ranging from 29% to 88%) vs 39% (ranging from 8% to 67%), p < .017], whereas RNH+ patients did not show any improvement [98% (ranging from 88% to 100%) vs 98% (ranging from 92% to 100%)]. Eye movement exploration: In RNH- patients, the interaction Session x Side was significant, showing an increase of the left side eye exploration [46% (ranging from 32% to 58%) vs 55% (ranging from 44% to 64%), p < .02] and a decrease on the right side [22% (ranging from 15% to 28%) vs 17% (ranging from 7% to 24%), p < .06]. By contrast, RNH+ patients did not show a significant improvement in the pattern of eye movements after the treatment. First saccade landing location: Session was the sole significant factor in RNH– patients (– 0.12°
156
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vs.– 1°; p < .05) showing an increased tendency for the first saccade to land nearer the beginning of the string after the treatment. CONCLUSION The results showed that all the patients manifested both the adaptation and the after-effect. Moreover, RNH- patients showed an improvement of neglect dyslexia after PA, an increased left-sided exploration of the letter string and an increased amplitude of the first left-sided saccade. Thus due to the eye-hand coordination during the pointing task, a deviation of eye movements in the direction opposite to the prismatic shift, was found also in relation to the eye coordinate system. In contrast, RNH+ patients did not show any improvement of reading performance and the patterns of eye movement exploration before and after PA were not significantly different. These findings provide evidence that the oculomotor improvement found in RNH– is not due to a simple error induced by PA in the direction of gaze but can be better explained by a more complex interaction between sensory stimulation and oculomotor deviation. In RNH–, visual signal registration, although partial, may provide a signal to move the eye (and the focus of attention) toward the left-sided letters and, as a
consequence of the eye movement, detection of left-sided information improved. In contrast, in RNH+, the absence of a visual stimulation cannot trigger any reallocation of attention to its location and, as a consequence, no amelioration of neglect dyslexia was found. REFERENCES HEILMAN KM, WATSON RT and VALENSTEIN E. Neglect I: Clinical and anatomic issues. In M Farah, F Todd (Eds), Patient-based Approaches to Cognitive Neuroscience. Issues in Clinical and Cognitive Neuropsychology. Cambridge, MA: MIT Press, 2000, pp. 115-23. PIZZAMIGLIO L, ANTONUCCI G, JUDICA A, MONTENERO P, RAZZANO C and ZOCCOLOTTI P. Cognitive rehabilitation of the hemineglect disorders in chronic patients with unilateral right brain damage. Journal of Clinical and Experimental Neuropsychology, 14: 901-923, 1992. ROSSETTI Y, RODE G, PISELLA L, FARNÈ A, LI L, BOISSON D and PERENIN MT. Prism adaptation to a rightward optical deviation rehabilitates left hemispatial neglect. Nature, 395: 166-169, 1998. LÀVADAS E, MENGHINI G and UMILTÀ C. A rehabilitation study of hemispatial neglect. Cognitive Neuropsychology, 11: 75-95, 1994. FARNÈ A, ROSSETTI Y, TONIOLO S and LÀDAVAS E. Ameliorating neglect with prism adaptation: visuo-manual and visuo-verbal measures. Neuropsychologia, 40: 718-729, 2002. CHEDRU F, LEBLANC M and LHERMITTE F. Visual searching in normal and brain damaged subjects: Contribution to the study of unilateral inattention. Cortex, 9: 94-111, 1973. FRASSINETTI F, ANGELI V, MENEGHELLO F and LÀDAVAS E. Longterm amelioration of visuospatial neglect be prism adaptation. Brain, 125: 608-623, 2002. Valentina Angeli, Centro di Neuroscienze Cognitive, Via Comunale Sorrivoli 585 – 47023 Cesena (FC), Italy. E-mail: [email protected]