Neuromodulation: Technology at the Neural Interface Received: January 12, 2013
Revised: October 18, 2013
Accepted: October 21, 2013
(onlinelibrary.wiley.com) DOI: 10.1111/ner.12140
LETTER TO THE EDITOR
Transcranial Direct Current Stimulation in de novo Artistic Ability After Stroke To the Editor: The emergence of de novo artistic ability after brain injury has been well documented in cases following neurological disorders such as stroke (1,2), frontotemporal dementia (3–5), subarachnoid hemorrhage (6), and Parkinson’s disease (7). Although the mechanisms behind this remarkable phenomenon remain unknown, several theories have attempted to explain the artistic drive in patients with previous nonexistent artistic output. One theory behind the development of such skills propose that savant-like skills are innate in everyone, but are not readily accessible due to topdown inhibition of the conscious awareness (8,9). Brain lesions provide an ideal scenario to study the atypical hemispheric imbalance necessary to access this “lower” level information. In stroke, reorganization of neural networks amplifies input signals to compensate for the loss of sensory afferents and may expose previously existing, but functionally inactive pathways (10). Although noninvasive brain stimulation techniques such as repetitive transcranial magnetic stimulation can facilitate savant-like skills in healthy subjects (8), there is limited information on the effects of brain stimulation, namely transcranial direct current stimulation (tDCS), on enhanced skills of individuals with neuroanatomical changes due to brain injury. The aim of this study was to use tDCS to modulate cortical activity and assess changes in artistic ability in a patient with a reorganized cerebral network due to stroke. We hypothesized that anodal stimulation of the right fronto-temporal region would temporarily facilitate these savant-like skills and result in stylistic changes in drawings.
METHODS
www.neuromodulationjournal.com
tDCS The protocol consisted of a three-visit, cross-over design with a one-week washout between visits. A 1 × 1 low-intensity DC stimulator was used to deliver 2 mA of constant current for 30 min through two oppositely charged electrodes. A 5 × 7 cm electrode was placed over area of interest, the right fronto-temporal region (F8), which was localized through the 10–20 EEG system. This area has been associated with spontaneous emergence of artistic talent (3,11,12). The unaffected hemisphere was chosen as the main target for modulation, as anatomical changes poststroke lead to reorganization of neural networks (13) and make stimulation less predictable due to displacement of the electric current (14). A large, contralateral reference electrode (10 × 10 cm) was placed on the left hemisphere over the fronto-temporal-parietal region. It has been shown that the effect on cortical activity of this size of electrode is not significant due to the diffuse current density (15,16). During the first visit, the subject received cathodal stimulation over F8. During the second visit, the subject received anodal stimulation over F8. During the third visit the subject received sham stimulation. Each visit consisted of 30 min of tDCS stimulation. The subject received sham tDCS for the first 10 min of stimulation (baseline). During this time, he was asked to draw three different pictures (a house, a horse, and a picture of his choice) with a time limit of 2.5 min per picture. The choice of these pictures was arbitrary (8). During the following 20 min of stimulation, the subject received anodal, cathodal, or sham stimulation over F8. Ten minutes before the session was over, he was asked to draw the three pictures again. The time limit was the same (Fig. 3). The local ethics committee approved the study, and the participant gave written informed consent prior to entering the study.
Address correspondence to: Felipe Fregni, MD, PhD, MPH, Laboratory of Neuromodulation, Spaulding Rehabilitation Hospital, 125 Nashua Street #726, Boston, MA 02114, USA. Email: [email protected] For more information on author guidelines, an explanation of our peer review process, and conflict of interest informed consent policies, please go to http:// www.wiley.com/bw/submit.asp?ref=1094-7159&site=1 1 Equally contributing authors. Conflict of Interest: The authors have no conflicts to declare.
© 2013 International Neuromodulation Society
Neuromodulation 2014; 17: 497–501
497
Case Presentation We had the opportunity to observe a 67-year-old, right-handed man, who reported an inexplicable urge to draw one week after a left middle cerebral artery stroke four years prior to the study. In 2009, he had an acute ischemic stroke, which affected the left cortical and subcortical regions of the postcentral gyrus, parietal lobe, insula, and the posterior limb of the internal capsule (Fig. 1). Sequels of the stroke included right-sided hemiparesis and mild Broca’s aphasia. The patient was in a conventional rehabilitation program during the first year after the stroke. During this year, he had an important improvement of the aphasia and motor deficit as shown by the Medical Research Council Scale for Muscle Strength. He improved his score from 1 to 4 in his right arm and from 2 to 4 in right leg. He reached a plateau of neurological deficits that remained steady until the time of the study. The rest of the neurological examination was normal and he showed no symptoms of
dementia. Both family history and past medical history were unremarkable. The patient is a former construction worker, with formal education up to the age of 10, and no previous exposure to art. After the stroke, he referred perfecting his drawing and painting techniques throughout the years using exclusively his left hand (Fig. 2).
SIMIS ET AL.
Figure 1. Location of brain lesions after a left middle cerebral artery stroke. a. T2-weighted MRI b. Diffusion tensor imaging (DTI) showing discontinuation of the corpus callosum fibers in the stroke area (arrow).
Session 1
Sham tDCS 10 min
Cathodal tDCS over F8 10 min
↑ Session 2
↑
Sham tDCS 10 min
Anodal tDCS over F8 10 min
↑ Session 3
10 min
↑
Sham tDCS 10 min
10 min
Sham tDCS 10 min
10 min
↑
↑
Drawings Set 1
Drawings Set 2
Figure 3. Experimental protocol. This was a cross-over study, in which the patient received 10 min of sham tDCS and was asked to draw a set of pictures. During the last 20 min of active stimulation, he received either anodal, cathodal, or sham tDCS over F8. He was asked to draw a second set of pictures during the last 10 min of active stimulation. tDCS, transcranial direct current stimulation.
Figure 2. Pictures drawn by the patient over the time span of several weeks.
498 www.neuromodulationjournal.com
Evaluation of Drawings Eleven postdoctoral research fellows blinded to stimulation assignment evaluated the drawings. All the pictures were coded and presented in randomized order to prevent bias. The evaluators were instructed to rate the pictures on a scale of 1 (lowest score) to 10 (highest score) for the following categories: creativity (use of the imagination or original ideas), perspective (representation of solid object on a two-dimensional surface), aesthetics (concerned with beauty or the appreciation of beauty), reality (actually existing as a
© 2013 International Neuromodulation Society
Neuromodulation 2014; 17: 497–501
LETTER TO THE EDITOR Sham
Cathodal
Anodal
Figure 4. Pictures drawn by the patient during the first 10 min of sham stimulation—baseline (left) and during the last 10 min of either cathodal (middle) or anodal stimulation over F8 (right).
thing, not imagined or supposed), and accuracy (meticulously careful and free from errors) based on their first impression. As there are no standardized categories to measure art, we chose these categories based on previous case reports of creative output after brain injury (2,11,17,18).
Statistical Analysis A Kruskal–Wallis test was conducted on the difference in drawing ratings from the first and last 10 min of stimulation for each one of the conditions. A p value
Revised: October 18, 2013
Accepted: October 21, 2013
(onlinelibrary.wiley.com) DOI: 10.1111/ner.12140
LETTER TO THE EDITOR
Transcranial Direct Current Stimulation in de novo Artistic Ability After Stroke To the Editor: The emergence of de novo artistic ability after brain injury has been well documented in cases following neurological disorders such as stroke (1,2), frontotemporal dementia (3–5), subarachnoid hemorrhage (6), and Parkinson’s disease (7). Although the mechanisms behind this remarkable phenomenon remain unknown, several theories have attempted to explain the artistic drive in patients with previous nonexistent artistic output. One theory behind the development of such skills propose that savant-like skills are innate in everyone, but are not readily accessible due to topdown inhibition of the conscious awareness (8,9). Brain lesions provide an ideal scenario to study the atypical hemispheric imbalance necessary to access this “lower” level information. In stroke, reorganization of neural networks amplifies input signals to compensate for the loss of sensory afferents and may expose previously existing, but functionally inactive pathways (10). Although noninvasive brain stimulation techniques such as repetitive transcranial magnetic stimulation can facilitate savant-like skills in healthy subjects (8), there is limited information on the effects of brain stimulation, namely transcranial direct current stimulation (tDCS), on enhanced skills of individuals with neuroanatomical changes due to brain injury. The aim of this study was to use tDCS to modulate cortical activity and assess changes in artistic ability in a patient with a reorganized cerebral network due to stroke. We hypothesized that anodal stimulation of the right fronto-temporal region would temporarily facilitate these savant-like skills and result in stylistic changes in drawings.
METHODS
www.neuromodulationjournal.com
tDCS The protocol consisted of a three-visit, cross-over design with a one-week washout between visits. A 1 × 1 low-intensity DC stimulator was used to deliver 2 mA of constant current for 30 min through two oppositely charged electrodes. A 5 × 7 cm electrode was placed over area of interest, the right fronto-temporal region (F8), which was localized through the 10–20 EEG system. This area has been associated with spontaneous emergence of artistic talent (3,11,12). The unaffected hemisphere was chosen as the main target for modulation, as anatomical changes poststroke lead to reorganization of neural networks (13) and make stimulation less predictable due to displacement of the electric current (14). A large, contralateral reference electrode (10 × 10 cm) was placed on the left hemisphere over the fronto-temporal-parietal region. It has been shown that the effect on cortical activity of this size of electrode is not significant due to the diffuse current density (15,16). During the first visit, the subject received cathodal stimulation over F8. During the second visit, the subject received anodal stimulation over F8. During the third visit the subject received sham stimulation. Each visit consisted of 30 min of tDCS stimulation. The subject received sham tDCS for the first 10 min of stimulation (baseline). During this time, he was asked to draw three different pictures (a house, a horse, and a picture of his choice) with a time limit of 2.5 min per picture. The choice of these pictures was arbitrary (8). During the following 20 min of stimulation, the subject received anodal, cathodal, or sham stimulation over F8. Ten minutes before the session was over, he was asked to draw the three pictures again. The time limit was the same (Fig. 3). The local ethics committee approved the study, and the participant gave written informed consent prior to entering the study.
Address correspondence to: Felipe Fregni, MD, PhD, MPH, Laboratory of Neuromodulation, Spaulding Rehabilitation Hospital, 125 Nashua Street #726, Boston, MA 02114, USA. Email: [email protected] For more information on author guidelines, an explanation of our peer review process, and conflict of interest informed consent policies, please go to http:// www.wiley.com/bw/submit.asp?ref=1094-7159&site=1 1 Equally contributing authors. Conflict of Interest: The authors have no conflicts to declare.
© 2013 International Neuromodulation Society
Neuromodulation 2014; 17: 497–501
497
Case Presentation We had the opportunity to observe a 67-year-old, right-handed man, who reported an inexplicable urge to draw one week after a left middle cerebral artery stroke four years prior to the study. In 2009, he had an acute ischemic stroke, which affected the left cortical and subcortical regions of the postcentral gyrus, parietal lobe, insula, and the posterior limb of the internal capsule (Fig. 1). Sequels of the stroke included right-sided hemiparesis and mild Broca’s aphasia. The patient was in a conventional rehabilitation program during the first year after the stroke. During this year, he had an important improvement of the aphasia and motor deficit as shown by the Medical Research Council Scale for Muscle Strength. He improved his score from 1 to 4 in his right arm and from 2 to 4 in right leg. He reached a plateau of neurological deficits that remained steady until the time of the study. The rest of the neurological examination was normal and he showed no symptoms of
dementia. Both family history and past medical history were unremarkable. The patient is a former construction worker, with formal education up to the age of 10, and no previous exposure to art. After the stroke, he referred perfecting his drawing and painting techniques throughout the years using exclusively his left hand (Fig. 2).
SIMIS ET AL.
Figure 1. Location of brain lesions after a left middle cerebral artery stroke. a. T2-weighted MRI b. Diffusion tensor imaging (DTI) showing discontinuation of the corpus callosum fibers in the stroke area (arrow).
Session 1
Sham tDCS 10 min
Cathodal tDCS over F8 10 min
↑ Session 2
↑
Sham tDCS 10 min
Anodal tDCS over F8 10 min
↑ Session 3
10 min
↑
Sham tDCS 10 min
10 min
Sham tDCS 10 min
10 min
↑
↑
Drawings Set 1
Drawings Set 2
Figure 3. Experimental protocol. This was a cross-over study, in which the patient received 10 min of sham tDCS and was asked to draw a set of pictures. During the last 20 min of active stimulation, he received either anodal, cathodal, or sham tDCS over F8. He was asked to draw a second set of pictures during the last 10 min of active stimulation. tDCS, transcranial direct current stimulation.
Figure 2. Pictures drawn by the patient over the time span of several weeks.
498 www.neuromodulationjournal.com
Evaluation of Drawings Eleven postdoctoral research fellows blinded to stimulation assignment evaluated the drawings. All the pictures were coded and presented in randomized order to prevent bias. The evaluators were instructed to rate the pictures on a scale of 1 (lowest score) to 10 (highest score) for the following categories: creativity (use of the imagination or original ideas), perspective (representation of solid object on a two-dimensional surface), aesthetics (concerned with beauty or the appreciation of beauty), reality (actually existing as a
© 2013 International Neuromodulation Society
Neuromodulation 2014; 17: 497–501
LETTER TO THE EDITOR Sham
Cathodal
Anodal
Figure 4. Pictures drawn by the patient during the first 10 min of sham stimulation—baseline (left) and during the last 10 min of either cathodal (middle) or anodal stimulation over F8 (right).
thing, not imagined or supposed), and accuracy (meticulously careful and free from errors) based on their first impression. As there are no standardized categories to measure art, we chose these categories based on previous case reports of creative output after brain injury (2,11,17,18).
Statistical Analysis A Kruskal–Wallis test was conducted on the difference in drawing ratings from the first and last 10 min of stimulation for each one of the conditions. A p value
