Effects of Passive Tactile and Auditory Stimuli on Left Visual Marc Hommel, MD; Blandine Peres, MPh; Pierre Pollak, MD; Bernard G\l=e'\rardBesson, MD; Jean-Marc Gaio, MD; Jean Perret, MD
\s=b\ Patients with left-sided visual neglect fail to copy the left part of drawings or the drawings on the left side of a sheet of paper. Our aim was to study the variations in copying drawings induced by passive stimulation in patients with left-sided visual neglect. No stimulation at all, tactile unilateral and bilateral, binaural auditory verbal, and nonverbal stimuli were randomly applied to 14 patients with right\x=req-\ hemisphere strokes. Only nonverbal stimuli decreased the neglect. As nonverbal stimuli mainly activate the right hemisphere, the decrease in neglect suggests right-hemispheric hypoactivity at rest in these patients. The absence of modification of neglect during verbal stimulation suggests a bilateral hemispheric activation and the persistence of interhemispheric imbalance. Our results showed that auditory pathways take part in the network involved with neglect. Passive nonverbal auditory stimuli may be of interest in the rehabilitation of patients with left visual neglect. (Arch Neurol. 1990;47:573-576)
neglect syndrome is composed of rphe a failure to report, respond, or ori¬
ent to a novel or meaningful stimulus presented to the side opposite a brain
lesion. This failure cannot be attrib¬ uted to either sensory or motor defects. The decrease in activity of the lesioned hemisphere may be responsible.1 Hemispatial neglect is a part of the neglect syndrome and consists of neAccepted for publication August 30, 1989. From the Department of Clinical and Biological Neurosciences, Stroke Unit, Centre Hospitalier R\l=e'\gionalUniversitaire de Grenoble (France). Reprint requests to the Clinique Neurologique, Centre Universitaire de Grenoble, BP 217 X, 38043 Grenoble Cedex, France (Dr Hommel).
Neglect
Memin, MD;
gleet in behavioral tasks performed in the hemispace contralateral to the le¬ sion. For example, patients draw only half of a picture of a flower; when asked to bisect a line, they may quarter it in¬
stead or may fail to cross out lines dis¬ tributed over a page.2 It is more fre¬ quent and severe with right-sided lesions.3·4 The degree of neglect may vary. It may be more severe if the in¬ farct size and premorbid brain atrophy is severe,5 and may improve with re¬ covery from a stroke.6 Neglect may be modified by changing the visuospatial to verbal nature of the stimuli,7 by ca¬ loric stimulations,8 by voluntary orientation,9 by gaze deviation10 to¬ ward the left side, by pointing toward the left side with the right hand,11 or by using a dopaminergic agonist.12 Ne¬ glect is a dynamic process and these modifications have been considered the result of an increase in the activity level in the right hemisphere1 and/or changes in right-left hemisphere im¬ balance.13 A change in the brain's ac¬ tivity level induced by sensory stimu¬ lation or neuropsychological tests is accompanied by an increase in cere¬ bral blood flow14 and metabolism.15 A decrease in blood flow has been ob¬ served in the parietal areas in patients with neglect syndrome,16 and in the metabolism of deep brain structures in an experimental model of neglect in the monkey.17 Our aim was to study whether modifications in hemispatial neglect could be induced by unilateral or bilateral passive external stimula¬ tion predicted to change the level in
right- or left-hemispheric activity. PATIENTS AND METHODS
Fourteen right-handed patients (8 men, 6 women) with left-sided visual neglect
Downloaded From: http://archneur.jamanetwork.com/ by a Michigan State University User on 06/08/2015
(mean age, 57 years [range, 29 to 81 years]) presented consecutively to our institution and were included in the study. All of them were right handed18 (Edinburgh score, +100). The mean delay between the onset of the stroke and the neuropsychological eval¬ uation was 15 days (range, 2 to 28 days). Motor and sensory impairment as well as hemianopia were sometimes present. The stroke was an infarction in 12 patients and a
spontaneous intracranial hematoma in 2
patients. The clinical and computed tomo¬ graphic findings are summarized in the Ta¬ ble. The patients had no history of stroke, dementia, or other neurologic illness. Visuoconstructive disorders, if present, were
mild and did not prevent them from
drawing. The levels of consciousness and attention were normal. Hearing was exam¬ ined only at the bedside with whispered speech at 3 m, and by the Rinné and Weber tuning-fork tests; all patients denied any difficulty in hearing. No patient was musi¬ cally sophisticated. The test consisted of copying six draw¬ ings: a flower, a cube, a bicycle, a clock, a house, and three men. The instruction was to copy the drawings as accurately as pos¬
sible on the same sheet of paper. The sheet of paper was placed in front of the patient. When the patient finished, he had to lay the pencil down. If he did nothing for 15 sec¬ onds, the examiner gave the instruction again. There was no time limit. All the tests were performed in the same session to avoid spontaneous fluctuations in neglect. The examiner and the patient remained silent throughout the test. Passive stimulations were given to the patient in a random order during the draw¬ ing tests. Twice, no stimulation at all was applied. The patient was exposed only to ambient stimulation and the noise of the single-bed room. This policy was used to test the effects of fatigue or learning on the task. Tactile stimulation consisted of repeti¬ tive taps with the smooth part of a pencil on the cheek, rapid but hard enough to cause an appreciable stimulus without causing
'
Clinical and
any discomfort:
(1) stimulation on the left cheek; (2) stimulation on the right cheek; and (3) simultaneous stimulations on both
Computed Tomographic (CT) Findings Findings
cheeks.
Case/
Age,
y Sex
Hand and
arm
Clinical distal motor and sensory
defect
Left-sided sensory loss; left
3/68/F
Left-sided facial and brachial
4/73/F
Left-sided sensory motor defect,
left-sided lateral
Right-sided parietal
arm
hemianopia paresis
Right-sided frontal, temporal, and parietal infarct Right-sided head of caudate, anterior arm of internal capsule, and lenticular infarct
Right-sided parietal
left-sided lateral
hemianopia Left-sided hypesthesia and facial paresis; left-sided hemianopia
5/53/M 6/42/F
Left-sided sensory motor defect; left-sided lateral hemianopia
7/43/M
Left-sided sensory motor defect; left-sided lateral hemianopia
8/61/M
Left-sided facial lateral
paresis, hemianopia
occipital
Left-sided sensory motor affecting lower face
infarct
Right-sided frontal, temporal, and parietal infarct_ Lenticular capsular hematoma
left-sided
Recent and
right-sided precentrai infarct parietal infarct; old right-sided
corona
9/65/M
lobar hematoma
Right-sided thalamic, internal capsule, and
radiata lacune
capsule and lenticular infarct Old right-sided premotor infarct; recent right-sided frontal, temporal, and
hemiparesis
Right
10/70/M
Left-sided sensory motor defect
11/29/M
Left-sided sensory motor defect
12/72/F
Left-sided facial weakness; lateral hemianopia; and anesthesia
13/81/M
Left-sided sensory motor defect
14/65/M
Left-sided lateral hemianopia; left-sided sensory extinction
genou of internal
parietal infarct_ Right-sided parietotemporal posterior arm of the internal capsule, head of caudate, and lenticular infarct Right-sided frontal and parietal infarct Right-sided frontal, temporal, and
parietal infarct_ Right-sided parietal infarct
Fig 1.—Modifications in neglect during the stimuli. Means of the intensity in neglect during the stimuli: 1, no stimulation on first task; 2, no stimulation on second task; 3, right cheek, tactile stim¬ ulation; 4, left cheek, tactile stimulation; 5, both cheeks, tactile stimulations; 6, headphones alone; 7, auditory verbal stimulations (description of a landscape); 8, auditory verbal stimulations (en¬ couragement); 9, music; and 10, white noise. The 0.99 confidence bounds for comparison of the means in neglect between the first task without stimuli and the other stimuli using Tukey's method are shown (dashed lines).
4en
i
P< .01
\ \ \ \ \ si
\ \
\
\ \
4 \
\ \ \
s s
J3LS \ \ \ \ \ \ 5
6
Stimulations
7
*
was given in both with a tape recorder and headphones. In all the auditory stimulation, sound amplitude was increased gradually. The patient was asked if he heard well; the in¬ tensity of the sound never caused any dis¬ comfort: (1) headphones without any audi¬ tory stimulation; (2) text bearing no rela¬ tionship with the test situation (description of a landscape); this text was read with a female voice; (3) text with encouragement in relation to the test situation given with the same female voice as the preceding stimulation; (4) musical stimulation with classical music (Bach and Vivaldi concer¬ tos); and (5) auditory stimulation with a continuous and constant white noise. The drawings were analyzed indepen¬ dently by two of us (P.P. and M.H.) unaware of the patient and of the stimulation used. The criteria used were the absence in copy¬ ing of the left-most drawings distributed over the sheet of paper and the tendency to leave the left half of each drawing unfin¬ ished. The degree of neglect on each draw¬ ing was rated as follows: 3, no copy at all; 2, copy with severe neglect; 1, copy with mod¬ erate neglect; and 0, no neglect. The two of us took part in the elaboration of the scale; we trained ourselves in the use of this scale by openly analyzing the drawings of five patients not included in this study. This or¬ dinal scale was transformed into quantita¬ tive data according to the Ridits method." For each of us the Ridits scores of each sheet of paper were summed. The means of the Ridits scores between both observers were considered as the result of the unilat¬ eral neglect during the stimulation: 5.46, maximum neglect; 0.67, no neglect. STATISTICAL ANALYSES Interobserver agreement was assessed with the kappa statistic.20 If a patient did not lend himself to all the stimulations, the missing data were estimated.21 The normal distribution of the neglect scores was ex¬ amined with the Wilk-Shapiro/Rankit plots. The results were analyzed with the two-way randomized block design analysis of variance. This was performed both by deleting the cases with missing data and by adding the cases with estimated missing data. To recognize which stimulation mod¬ ified the neglect, Tukey's method for com¬ parison of means was employed. ears
infarct; cortical
atrophy_
2/77/F
paresis;
Auditory stimulation
CT
RESULTS
*
[5L_
u 10
Downloaded From: http://archneur.jamanetwork.com/ by a Michigan State University User on 06/08/2015
In 9 patients all of the modalities of stimulation were used. In the 5 re¬ maining patients, who were too tired to get through all the procedures, there were 13 missing values. The two of us were substantially concordant in the rating of the drawings (kappa, 0.75). The results of the statistical analyses did not differ, whether or not the cases with missing values were dropped out. Overall, the stimulations modified the
neglect (F
=
4.45;
\s=b\ Patients with left-sided visual neglect fail to copy the left part of drawings or the drawings on the left side of a sheet of paper. Our aim was to study the variations in copying drawings induced by passive stimulation in patients with left-sided visual neglect. No stimulation at all, tactile unilateral and bilateral, binaural auditory verbal, and nonverbal stimuli were randomly applied to 14 patients with right\x=req-\ hemisphere strokes. Only nonverbal stimuli decreased the neglect. As nonverbal stimuli mainly activate the right hemisphere, the decrease in neglect suggests right-hemispheric hypoactivity at rest in these patients. The absence of modification of neglect during verbal stimulation suggests a bilateral hemispheric activation and the persistence of interhemispheric imbalance. Our results showed that auditory pathways take part in the network involved with neglect. Passive nonverbal auditory stimuli may be of interest in the rehabilitation of patients with left visual neglect. (Arch Neurol. 1990;47:573-576)
neglect syndrome is composed of rphe a failure to report, respond, or ori¬
ent to a novel or meaningful stimulus presented to the side opposite a brain
lesion. This failure cannot be attrib¬ uted to either sensory or motor defects. The decrease in activity of the lesioned hemisphere may be responsible.1 Hemispatial neglect is a part of the neglect syndrome and consists of neAccepted for publication August 30, 1989. From the Department of Clinical and Biological Neurosciences, Stroke Unit, Centre Hospitalier R\l=e'\gionalUniversitaire de Grenoble (France). Reprint requests to the Clinique Neurologique, Centre Universitaire de Grenoble, BP 217 X, 38043 Grenoble Cedex, France (Dr Hommel).
Neglect
Memin, MD;
gleet in behavioral tasks performed in the hemispace contralateral to the le¬ sion. For example, patients draw only half of a picture of a flower; when asked to bisect a line, they may quarter it in¬
stead or may fail to cross out lines dis¬ tributed over a page.2 It is more fre¬ quent and severe with right-sided lesions.3·4 The degree of neglect may vary. It may be more severe if the in¬ farct size and premorbid brain atrophy is severe,5 and may improve with re¬ covery from a stroke.6 Neglect may be modified by changing the visuospatial to verbal nature of the stimuli,7 by ca¬ loric stimulations,8 by voluntary orientation,9 by gaze deviation10 to¬ ward the left side, by pointing toward the left side with the right hand,11 or by using a dopaminergic agonist.12 Ne¬ glect is a dynamic process and these modifications have been considered the result of an increase in the activity level in the right hemisphere1 and/or changes in right-left hemisphere im¬ balance.13 A change in the brain's ac¬ tivity level induced by sensory stimu¬ lation or neuropsychological tests is accompanied by an increase in cere¬ bral blood flow14 and metabolism.15 A decrease in blood flow has been ob¬ served in the parietal areas in patients with neglect syndrome,16 and in the metabolism of deep brain structures in an experimental model of neglect in the monkey.17 Our aim was to study whether modifications in hemispatial neglect could be induced by unilateral or bilateral passive external stimula¬ tion predicted to change the level in
right- or left-hemispheric activity. PATIENTS AND METHODS
Fourteen right-handed patients (8 men, 6 women) with left-sided visual neglect
Downloaded From: http://archneur.jamanetwork.com/ by a Michigan State University User on 06/08/2015
(mean age, 57 years [range, 29 to 81 years]) presented consecutively to our institution and were included in the study. All of them were right handed18 (Edinburgh score, +100). The mean delay between the onset of the stroke and the neuropsychological eval¬ uation was 15 days (range, 2 to 28 days). Motor and sensory impairment as well as hemianopia were sometimes present. The stroke was an infarction in 12 patients and a
spontaneous intracranial hematoma in 2
patients. The clinical and computed tomo¬ graphic findings are summarized in the Ta¬ ble. The patients had no history of stroke, dementia, or other neurologic illness. Visuoconstructive disorders, if present, were
mild and did not prevent them from
drawing. The levels of consciousness and attention were normal. Hearing was exam¬ ined only at the bedside with whispered speech at 3 m, and by the Rinné and Weber tuning-fork tests; all patients denied any difficulty in hearing. No patient was musi¬ cally sophisticated. The test consisted of copying six draw¬ ings: a flower, a cube, a bicycle, a clock, a house, and three men. The instruction was to copy the drawings as accurately as pos¬
sible on the same sheet of paper. The sheet of paper was placed in front of the patient. When the patient finished, he had to lay the pencil down. If he did nothing for 15 sec¬ onds, the examiner gave the instruction again. There was no time limit. All the tests were performed in the same session to avoid spontaneous fluctuations in neglect. The examiner and the patient remained silent throughout the test. Passive stimulations were given to the patient in a random order during the draw¬ ing tests. Twice, no stimulation at all was applied. The patient was exposed only to ambient stimulation and the noise of the single-bed room. This policy was used to test the effects of fatigue or learning on the task. Tactile stimulation consisted of repeti¬ tive taps with the smooth part of a pencil on the cheek, rapid but hard enough to cause an appreciable stimulus without causing
'
Clinical and
any discomfort:
(1) stimulation on the left cheek; (2) stimulation on the right cheek; and (3) simultaneous stimulations on both
Computed Tomographic (CT) Findings Findings
cheeks.
Case/
Age,
y Sex
Hand and
arm
Clinical distal motor and sensory
defect
Left-sided sensory loss; left
3/68/F
Left-sided facial and brachial
4/73/F
Left-sided sensory motor defect,
left-sided lateral
Right-sided parietal
arm
hemianopia paresis
Right-sided frontal, temporal, and parietal infarct Right-sided head of caudate, anterior arm of internal capsule, and lenticular infarct
Right-sided parietal
left-sided lateral
hemianopia Left-sided hypesthesia and facial paresis; left-sided hemianopia
5/53/M 6/42/F
Left-sided sensory motor defect; left-sided lateral hemianopia
7/43/M
Left-sided sensory motor defect; left-sided lateral hemianopia
8/61/M
Left-sided facial lateral
paresis, hemianopia
occipital
Left-sided sensory motor affecting lower face
infarct
Right-sided frontal, temporal, and parietal infarct_ Lenticular capsular hematoma
left-sided
Recent and
right-sided precentrai infarct parietal infarct; old right-sided
corona
9/65/M
lobar hematoma
Right-sided thalamic, internal capsule, and
radiata lacune
capsule and lenticular infarct Old right-sided premotor infarct; recent right-sided frontal, temporal, and
hemiparesis
Right
10/70/M
Left-sided sensory motor defect
11/29/M
Left-sided sensory motor defect
12/72/F
Left-sided facial weakness; lateral hemianopia; and anesthesia
13/81/M
Left-sided sensory motor defect
14/65/M
Left-sided lateral hemianopia; left-sided sensory extinction
genou of internal
parietal infarct_ Right-sided parietotemporal posterior arm of the internal capsule, head of caudate, and lenticular infarct Right-sided frontal and parietal infarct Right-sided frontal, temporal, and
parietal infarct_ Right-sided parietal infarct
Fig 1.—Modifications in neglect during the stimuli. Means of the intensity in neglect during the stimuli: 1, no stimulation on first task; 2, no stimulation on second task; 3, right cheek, tactile stim¬ ulation; 4, left cheek, tactile stimulation; 5, both cheeks, tactile stimulations; 6, headphones alone; 7, auditory verbal stimulations (description of a landscape); 8, auditory verbal stimulations (en¬ couragement); 9, music; and 10, white noise. The 0.99 confidence bounds for comparison of the means in neglect between the first task without stimuli and the other stimuli using Tukey's method are shown (dashed lines).
4en
i
P< .01
\ \ \ \ \ si
\ \
\
\ \
4 \
\ \ \
s s
J3LS \ \ \ \ \ \ 5
6
Stimulations
7
*
was given in both with a tape recorder and headphones. In all the auditory stimulation, sound amplitude was increased gradually. The patient was asked if he heard well; the in¬ tensity of the sound never caused any dis¬ comfort: (1) headphones without any audi¬ tory stimulation; (2) text bearing no rela¬ tionship with the test situation (description of a landscape); this text was read with a female voice; (3) text with encouragement in relation to the test situation given with the same female voice as the preceding stimulation; (4) musical stimulation with classical music (Bach and Vivaldi concer¬ tos); and (5) auditory stimulation with a continuous and constant white noise. The drawings were analyzed indepen¬ dently by two of us (P.P. and M.H.) unaware of the patient and of the stimulation used. The criteria used were the absence in copy¬ ing of the left-most drawings distributed over the sheet of paper and the tendency to leave the left half of each drawing unfin¬ ished. The degree of neglect on each draw¬ ing was rated as follows: 3, no copy at all; 2, copy with severe neglect; 1, copy with mod¬ erate neglect; and 0, no neglect. The two of us took part in the elaboration of the scale; we trained ourselves in the use of this scale by openly analyzing the drawings of five patients not included in this study. This or¬ dinal scale was transformed into quantita¬ tive data according to the Ridits method." For each of us the Ridits scores of each sheet of paper were summed. The means of the Ridits scores between both observers were considered as the result of the unilat¬ eral neglect during the stimulation: 5.46, maximum neglect; 0.67, no neglect. STATISTICAL ANALYSES Interobserver agreement was assessed with the kappa statistic.20 If a patient did not lend himself to all the stimulations, the missing data were estimated.21 The normal distribution of the neglect scores was ex¬ amined with the Wilk-Shapiro/Rankit plots. The results were analyzed with the two-way randomized block design analysis of variance. This was performed both by deleting the cases with missing data and by adding the cases with estimated missing data. To recognize which stimulation mod¬ ified the neglect, Tukey's method for com¬ parison of means was employed. ears
infarct; cortical
atrophy_
2/77/F
paresis;
Auditory stimulation
CT
RESULTS
*
[5L_
u 10
Downloaded From: http://archneur.jamanetwork.com/ by a Michigan State University User on 06/08/2015
In 9 patients all of the modalities of stimulation were used. In the 5 re¬ maining patients, who were too tired to get through all the procedures, there were 13 missing values. The two of us were substantially concordant in the rating of the drawings (kappa, 0.75). The results of the statistical analyses did not differ, whether or not the cases with missing values were dropped out. Overall, the stimulations modified the
neglect (F
=
4.45;
