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Creative innovation with temporal lobe epilepsy and lobectomy
Journal of the Neurological Sciences 324 (2013) 45–48
Contents lists available at SciVerse ScienceDirect
Journal of the Neurological Sciences journal homepage: www.elsevier.com/locate/jns
Creative innovation with temporal lobe epilepsy and lobectomy Georges A. Ghacibeh a, Kenneth M. Heilman b,⁎ a b
Progressive Neurology, 255 W Spring Valley Ave, Suite 205, Maywood, NJ 07607, United States Department of Neurology, PO Box 100236, University of Florida, Gainesville, FL 32610, United States
a r t i c l e
i n f o
Article history: Received 23 July 2012 Received in revised form 21 September 2012 Accepted 26 September 2012 Available online 30 October 2012 Keywords: Epilepsy Temporal lobectomy Creativity Semantic dementia
a b s t r a c t Objectives: Some patients with left temporal degeneration develop visual artistic abilities. These new artistic abilities may be due to disinhibition of the visuo-spatially dominant right hemisphere. Many famous artists have had epilepsy and it is possible that some may have had left temporal seizures (LTS) and this left temporal dysfunction disinhibited their right hemisphere. Alternatively, unilateral epilepsy may alter intrahemispheric connectivity and right anterior temporal lobe seizures (RTS) may have increased these artists' right hemisphere mediated visual artistic creativity. Methods: To test the disinhibition versus enhanced connectivity hypotheses we studied 9 participants with RTS and 9 with left anterior temporal seizures (LTS) who underwent unilateral lobectomy for the treatment of medically refractory epilepsy. Creativity was tested using the Torrance Test of Creative Thinking (TTCT). Results and conclusions: There were no between group differences in either the verbal or figural scores of the TTCT, suggesting that unilateral anterior temporal ablation did not enhance visual artistic ability; however, for the RTS participants' figural creativity scores were significantly higher than verbal scores. Whereas these results fail to support the left temporal lobe disinhibition postulate of enhanced figural creativity, the finding that the patients with RTS had better figural than verbal creativity suggests that their recurrent right hemispheric seizures lead to changes in their right hemispheric networks that facilitated visual creativity. To obtain converging evidence, studies on RTS participants who have not undergone lobectomy will need to be performed. Published by Elsevier B.V.
1. Introduction Creativity has been defined as the ability to understand, develop and express in a systematic fashion, novel orderly relationships [1,2]. Although creative innovation is one of the most important functions of the human brain, the means by which the brain develops creative ideas as well as how diseases of the brain alter creativity are not well understood. Studies of patients with semantic dementia, a form of primary aphasia associated with a progressive frontal temporal lobar degeneration (PPA-FTLD) [3,4], who have relatively isolated left anterior temporal lobe degeneration reveal that some of these patients acquire new visual artistic skills. These observations suggest that loss of function in the left anterior temporal lobe may lead to the “facilitation” of right hemisphere mediated visual artistic skills. The concept that loss of function in one brain area can release or enhance functions mediated by other areas of the brain has not been fully explored or understood; however, one possible explanation is based on the concept that a lesion in a certain brain area might disrupt a cortical inhibitory network leading to facilitation in another brain area, a concept referred to as paradoxical functional facilitation [5]. This functional facilitation, for example, has been used
⁎ Corresponding author. Tel.: +1 352 352-273-5550; fax: +1 352 352-273-5575. E-mail address: [email protected]fl.edu (K.M. Heilman). 0022-510X/$ – see front matter. Published by Elsevier B.V. http://dx.doi.org/10.1016/j.jns.2012.09.029
to explain rightward attentional bias associated with right hemisphere lesions [6]. The same mechanism is thought to play a role in the emergence of visuo-spatial artistic skills in patients with left anterior temporal degeneration. However, there is paucity of converging evidence to support this postulate. Therefore, one way to test this hypothesis is to study patients with dysfunction of the same anatomical area caused by a different disease process. About one third of patients with anterior temporal lobe epilepsy have medically intractable seizures, many of whom are candidates for anterior temporal lobectomy [7]. According to the paradoxical functional facilitation hypothesis [5] since patients with chronic left anterior temporal lobe seizures may have left hemispheric dysfunction and subsequently have an ablation of their left anterior temporal lobes they should have greater visuo-spatial artistic ability than those patients who have long standing right anterior temporal lobe epilepsy and ablation of their anterior left temporal lobe. Similarly, based on this disinhibition hypothesis, we may expect patients who have long standing right anterior temporal epilepsy and a right anterior temporal lobectomy to have an increase in their verbal creativity. Whereas some investigators have reported a decline of musical abilities with right temporal lobectomy [8,9] and trouble with word finding following left temporal lobectomy [10,11], to our knowledge no one has reported an increase in verbal creativity with right temporal lobectomy or an increase of visual artistic creativity with removal of the left temporal lobe.
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G.A. Ghacibeh, K.M. Heilman / Journal of the Neurological Sciences 324 (2013) 45–48
Some great artists such as Leonardo Da Vinci, Michelangelo and Van Gogh, as well as some creative authors, such as Lewis Carroll, Edgar Allan Poe, Fyodor Dostoevsky were thought to have temporal lobe epilepsy. Whereas these creative geniuses did not have temporal lobectomy and the type as well as the laterality of their seizures is unknown, it is possible that temporal lobe epilepsy, altered their brain connectivity of the hemisphere that is ipsilateral to their seizure focus and this change enhanced the specific form of creativity that is heavily dependent on that hemisphere. Thus, the purpose of this study is twofold, and includes testing the disinhibition postulate of creative innovation in patients with temporal lobe epilepsy who underwent surgical resection of their left or right anterior temporal lobe as well as to learn if there are verbal versus visuospatial differences in creativity as a function of seizure laterality. 2. Methods 2.1. Subjects Eighteen patients (9 men and 9 women, age: 40±12) with medically refractory temporal lobe epilepsy, who underwent standard temporal lobectomy at least 6 months prior to testing (median: 24 months, range: 7–166), served as study participants. Nine patients had left temporal lobectomy for left temporal lobe epilepsy (5 men, 4 women) and 9 patients had right temporal lobectomy for right temporal lobe epilepsy (5 women and 4 men). Table 1 summarizes subject characteristics. The study was approved by the Institutional Review Board of the University of Florida and all subjects gave written informed consent. All subjects were right-handed by self report. All participants were still on their usual doses of anti-epileptic medications at the time of testing and were free of seizures. 2.2. Testing All 18 participants were assessed with the verbal and figural subtests of the Torrance Test of Creative Thinking (TTCT), form A [12–14]. Following the instructions provided by the publisher of the TTCT, all testing was completed in a single session. The figural subtest of the TTCT consists of 3 activities. During all three figural activities, subjects are given different types of incomplete figures and are asked to complete them by turning them into significant pictures, as well as giving
them titles. Although all three figural activities have similarities, the types of incomplete figures are different and tap into different aspects of creative functioning [14]. The verbal subtest consists of six activities. During the first three activities, subjects are given a drawing and are asked to come up with a list of answers describing the action taking place in the drawing, its causes and consequences. In the fourth activity, subjects are shown a drawing of a toy and are asked to come up with ideas that would improve it. In the fifth activity, subjects are asked to think of unusual uses of a specific object, such as a brick or a cardboard. The last activity consists of a hypothetical scenario where subjects are asked to suppose that a certain unlikely scenario happened (example: clouds had strings attached to them which head down to earth) and are asked to come up a list of ideas about the consequences of such a situation. All test sheets were de-identified, coded and mailed to the publisher, Scholastic Testing Service, Inc., for scoring. Scoring was performed following the scoring manuals. The figural tasks are scored on fluency, originality, abstractness of titles, elaboration and resistance to premature closure. Raw scores are generated for each of the 5 dimensions then an average score is calculated and normalized for age. In addition, a 13 point check list for creative strength is also calculated for each of the 5 dimensions, and the results are computed with the average score to generate a Figural Creativity Index (FCI) [14]. The verbal tasks are scored on fluency, originality and flexibility. Raw scores are generated for each of the 3 dimensions and averaged for each subject, then normalized for age to generate a verbal average score which will be referred to as the Verbal Creativity Index (VCI). 2.3. Statistical analysis To ensure that both the right and left temporal lobectomy groups did not differ, age and time since surgery were compared using independent t-tests. To assess for significant differences in creativity between the two groups, a two-way repeated measures analysis of variance (ANOVA) was used with the side of surgery (right versus left) being the between group factor and type of creativity (verbal versus figural) as being the within group factor. When appropriate, post-hoc analysis for pair wise comparisons was performed using paired t-tests. An alpha value level of 5% or less was considered statistically significant. 2.4. Results
Table 1 Patient characteristics and creativity scores. Patient
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18
Age
37 46 45 31 46 22 52 59 36 45 53 46 53 20 25 36 25 45
Sex
Female Female Female Female Male Male Male Male Male Female Female Female Female Female Male Male Male Male
TFS
63 24 89 97 8 14 24 166 6 125 79 21 13 7 7 28 24 21
Side
Left Left Left Left Left Left Left Left Left Right Right Right Right Right Right Right Right Right
AEDs
PHN, LEV LTG, ZNS CBZ, LEV LEV, CBZ OXC OXC, VPA OXC PHN, CBZ LTG, TOP VPA, PRM, LEV OXC OXC, TOP TOP, LEV, PRM, ALP CBZ, LEV, ZNS VPA, LEV CBZ, VPA LEV, LTG CBZ, TOP
Creativity scores Figural
Verbal
99 78 95 75 88 78 73 95 65 117 51 133 76 65 113 102 93 88
70 75 76 59 83 111 72 76 68 77 48 146 62 70 71 79 65 66
TFS: time from surgery in months; AEDs: anti-epileptic drugs; PHN: phenytoin; LEV: levetiracetam; LTG: lamotrigine; ZNS: zonisamide; CBZ: carbamazepine; OXC: oxcarbazepine; VPA: valproic acid; TOP: topiramate; PRM: primidone; ALP: alprazolam.
The subject characteristics and scores can be found in Table 1. There were no group differences in age and time since surgery. The ANOVA revealed no significant effect of side of surgery on overall creativity (p> 0.05) and no interaction between the side of surgery (right versus left) and the type of creativity (verbal versus figural). However, there was a significant major effect of creativity type (pb 0.05), figural being superior to verbal. Since we found that figural creativity was significantly better than verbal creativity, we wanted to learn if within each group performance on the verbal and figural creativity tasks was different. Paired t-tests were, therefore, performed independently for the RATL and LATL groups, comparing figural to verbal creativity indices. This analysis revealed no difference between the verbal and figural indices in the LATL group (p > 0.05); however, in the RATL group there was a significantly higher figural than verbal scores (p b 0.05). 3. Discussion The participants with LATL, when compared to those with RATL, did not have enhanced figural creativity. This finding fails to support the disinhibition postulate of enhanced figural creativity associated with PPA-FTLD. Similarly, the finding that patients with RATL did not have greater verbal creativity than those participants with LATL
G.A. Ghacibeh, K.M. Heilman / Journal of the Neurological Sciences 324 (2013) 45–48
provides further support against the disinhibition postulate. There are, however, several possible explanations for the failure to support paradoxical facilitation. First, although patients with PPA-FTLD with increased creativity were reported to have isolated left anterior temporal lobe atrophy, clinically, they had very poor social skills, suggesting that the disease process extended beyond the temporal lobe, most likely into the frontal lobe. Second, these patients with PPA-FTLD had lost much of their ability to use verbal communication and since their right hemisphere was relatively intact it is possible that they developed pictorial skills as a form of compensation. Since most patients with PPA-FTLD who developed increased creativity were not artists before this disease started, we cannot know if the left anterior temporal lobe degeneration enhanced their artistic-pictorial creativity or helped to initiate pictorial productions as a form of compensation. Support for this compensatory postulate comes from the study of an artist who developed the PPA form of FTLD [15]. The paintings created by this artist before the onset of her dementia compared to those after dementia onset, revealed that her artistic ability did not improve. Instead, the novelty of her work decreased, suggesting that FTLD did not improve artistic skills in this patient who already possessed these skills. In contrast, the disorder induced a decrease in novelty, a key component of creativity. Another report [16], of a patient with PPA-FTLD who was an artist before the onset of his disease and continued to produce artistic work after the onset of his dementia, revealed an improvement of technique that might be related to sparing and disinhibition of the right posterior neocortex, but a reduction of closure (completeness of the painting), possibly induced by impersistence and a decrease in evocative impact which might be explained by frontal and anterior temporal lobe-limbic dysfunction. The third explanation of the inconsistency between our results and the reports that some patients with PPA-FTLD who developed artistic creativity is based on the fundamental differences between the two diseases. Unlike the patients with PPA-FTLD who have progressive neuronal degeneration, patients with chronic epilepsy have frequent recurrent seizures that may alter certain neuronal networks and lead to differences in the way certain brain areas react to acute injuries. A potentially important finding of this study is that patients with RATL performed better at creative figural productions than they did on the verbal task. It is not known if this relative superiority of figural creativity is due to chronic right temporal lobe epilepsy or to the surgery itself. As mentioned, it is possible that chronic epilepsy with recurrent seizures can lead to alterations of neuronal networks in several brain areas. This postulate has been supported by functional and anatomical MRI studies of patients with temporal lobe epilepsy that revealed changes in the pattern of activation of certain functional areas and even atrophy of brain regions outside the primary epileptic focus [17–20]. Therefore, it is possible that recurrent seizures arising in the right temporal lobe might lead to permanent changes in other brain regions, resulting in increased visual–figural creativity. The relationship between their epilepsy and creative innovation is far from being understood, but, these results certainly raises an important question regarding the potential impact of recurrent seizures on brain plasticity and creativity. In contrast to the enhanced visual–figural creativity associated with right anterior temporal epilepsy, there was no evidence that patients with LATL performed better at the verbal than pictorial-drawing tasks. As mentioned patients with left anterior temporal lobe epilepsy and treatment with lobectomy, like patients with degenerative disease of this same region, have problems with word finding [10,11] and this disability may have adversely influenced their verbal creativity. The reason that focal seizures may enhance brain creativity is unknown. Based on ablation and functional imaging studies it is now known that the brain is organized in modular fashion. Therefore, creative people might have the ability to activate more highly distributed networks. Support for this theory comes from electroencephalographic (EEG) studies of normal subjects who demonstrated an increase of anatomically distributed coherence of EEG oscillations
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while engaged in creative thought-innovation [21,22]. Donald Hebb suggested that neurons that fire together wire together [23], and during a temporal lobe seizure, there is EEG coherence between temporal lobe structures and other areas of the neocortex as well as high coherence values between neocortical structures [24]. Thus, seizure-induced coherence might enhance connectivity and with right temporal seizures, the enhanced right hemisphere connectivity might have lead to enhanced right hemisphere mediated visual artistic creativity. Our study had a small number of subjects in each group and thus it may be of value to learn if our results can be replicated in future studies with more subjects in each group. In addition future research should contrast those participants with right temporal lobe epilepsy, who have not undergone an anterior temporal lobectomy, with those who have had this surgery, to help distinguish the impact of chronic epilepsy from that of the surgery on figural creative innovation. Disclosure The data presented in this manuscript was previously presented, in part, as a poster, at the 61st Annual Meeting of the American Epilepsy Society in Philadelphia, December 2007 and published as an abstract in Epilepsia suppl. (Abst. 2.253), 2007. Conflict of interest There is no conflict of interest. Acknowledgments The authors would like to thank Akhil Patel, Sandeep Konka and Kathrine Winter for their help in testing the participants and John Williamson PhD for being our statistical consultant. References [1] Bronowski J. Science and human values. New York: Harpwer and Row; 1972. [2] Heilman KM, Nadeau SE, Beversdorf DO. Creative innovation: possible brain mechanisms. Neurocase 2003;9:369-79. [3] Miller BL, Boone K, Cummings JL, Read SL, Mishkin F. Functional correlates of musical and visual ability in frontotemporal dementia. Br J Psychiatry 2000;176:458-63. [4] Miller BL, Cummings J, Mishkin F, Boone K, Prince F, Ponton M, et al. Emergence of artistic talent in frontotemporal dementia. Neurology 1998;51:978-82. [5] Kapur N. Paradoxical functional facilitation in brain-behaviour research. A critical review. Brain 1996;119:1775-90 (Pt 5). [6] Kinsbourne M. A model for the mechanism of unilateral neglect of space. Trans Am Neurol Assoc 1970;95:143-6. [7] Engel J, Wiebe S, French J, Sperling M, Williamson P, Spencer D, et al. Practice parameter: temporal lobe and localized neocortical resections for epilepsy. Report of the Quality Standards Subcommittee of the American Academy of Neurology, in Association with the American Epilepsy Society and the American Association of Neurological Surgeons. Epilepsia 2003;44:741-51. [8] Kester DB, Saykin AJ, Sperling MR, O'Connor MJ, Robinson LJ, Gur RC. Acute effect of anterior temporal lobectomy on musical processing. Neuropsychologia 1991;29: 703-8. [9] Zatorre RJ. Discrimination and recognition of tonal melodies after unilateral cerebral excisions. Neuropsychologia 1985;23:31-41. [10] Davies KG, Risse GL, Gates JR. Naming ability after tailored left temporal resection with extraoperative language mapping: increased risk of decline with later epilepsy onset age. Epilepsy Behav 2005;7:273-8. [11] Heilman KM, Wilder BJ, Malzone WF. Anomic aphasia following anterior temporal lobectomy. Trans Am Neurol Assoc 1972;97:291-3. [12] Torrance EP. Torrance tests of creative thinking: manual for scoring and interpreting results, verbal, forms A&B. Bensenville, IL: Scholastic Testing Service, Inc.; 1990. [13] Torrance EP. Torrance tests of creative thinking: norms-technical manual, figural forms A&B. Bensenville, IL: Scholastic Testing Services, Inc.; 1998. [14] Torrance EP, Ball OE, Safter HT. Torrance tests of creative thinking: streamlined scoring guide, figural A&B. Bensenville, IL: Scholastic Testing Service, Inc.; 1992. [15] Finney GR, Heilman KM. Artwork before and after onset of progressive nonfluent aphasia. Cogn Behav Neurol 2007;20:7–10. [16] Drago V, Foster PS, Trifiletti D, FitzGerald DB, Kluger BM, Crucian GP, et al. What's inside the art? The influence of frontotemporal dementia in art production. Neurology 2006;67:1285-7.
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[17] Bernhardt BC, Worsley KJ, Kim H, Evans AC, Bernasconi A, Bernasconi N. Longitudinal and cross-sectional analysis of atrophy in pharmacoresistant temporal lobe epilepsy. Neurology 2009;72:1747-54. [18] Dupont P, Zaknun JJ, Maes A, Tepmongkol S, Vasquez S, Bal CS, et al. Dynamic perfusion patterns in temporal lobe epilepsy. Eur J Nucl Med Mol Imaging 2009;36: 823-30. [19] Keller SS, Baker G, Downes JJ, Roberts N. Quantitative MRI of the prefrontal cortex and executive function in patients with temporal lobe epilepsy. Epilepsy Behav 2009;15:186-95. [20] Riederer F, Lanzenberger R, Kaya M, Prayer D, Serles W, Baumgartner C. Network atrophy in temporal lobe epilepsy: a voxel-based morphometry study. Neurology 2008;71:419-25.
[21] Jausovec N, Jausovec K. EEG activity during the performance of complex mental problems. Int J Psychophysiol 2000;36:73-88. [22] Petsche H. Approaches to verbal, visual and musical creativity by EEG coherence analysis. Int J Psychophysiol 1996;24:145-59. [23] Hebb D. The organization of behavior. New York: John Wiley and Sons; 1949. [24] Bartolomei F, Wendling F, Vignal JP, Kochen S, Bellanger JJ, Badier JM, et al. Seizures of temporal lobe epilepsy: identification of subtypes by coherence analysis using stereo-electro-encephalography. Clin Neurophysiol 1999;110:1741-54.
Contents lists available at SciVerse ScienceDirect
Journal of the Neurological Sciences journal homepage: www.elsevier.com/locate/jns
Creative innovation with temporal lobe epilepsy and lobectomy Georges A. Ghacibeh a, Kenneth M. Heilman b,⁎ a b
Progressive Neurology, 255 W Spring Valley Ave, Suite 205, Maywood, NJ 07607, United States Department of Neurology, PO Box 100236, University of Florida, Gainesville, FL 32610, United States
a r t i c l e
i n f o
Article history: Received 23 July 2012 Received in revised form 21 September 2012 Accepted 26 September 2012 Available online 30 October 2012 Keywords: Epilepsy Temporal lobectomy Creativity Semantic dementia
a b s t r a c t Objectives: Some patients with left temporal degeneration develop visual artistic abilities. These new artistic abilities may be due to disinhibition of the visuo-spatially dominant right hemisphere. Many famous artists have had epilepsy and it is possible that some may have had left temporal seizures (LTS) and this left temporal dysfunction disinhibited their right hemisphere. Alternatively, unilateral epilepsy may alter intrahemispheric connectivity and right anterior temporal lobe seizures (RTS) may have increased these artists' right hemisphere mediated visual artistic creativity. Methods: To test the disinhibition versus enhanced connectivity hypotheses we studied 9 participants with RTS and 9 with left anterior temporal seizures (LTS) who underwent unilateral lobectomy for the treatment of medically refractory epilepsy. Creativity was tested using the Torrance Test of Creative Thinking (TTCT). Results and conclusions: There were no between group differences in either the verbal or figural scores of the TTCT, suggesting that unilateral anterior temporal ablation did not enhance visual artistic ability; however, for the RTS participants' figural creativity scores were significantly higher than verbal scores. Whereas these results fail to support the left temporal lobe disinhibition postulate of enhanced figural creativity, the finding that the patients with RTS had better figural than verbal creativity suggests that their recurrent right hemispheric seizures lead to changes in their right hemispheric networks that facilitated visual creativity. To obtain converging evidence, studies on RTS participants who have not undergone lobectomy will need to be performed. Published by Elsevier B.V.
1. Introduction Creativity has been defined as the ability to understand, develop and express in a systematic fashion, novel orderly relationships [1,2]. Although creative innovation is one of the most important functions of the human brain, the means by which the brain develops creative ideas as well as how diseases of the brain alter creativity are not well understood. Studies of patients with semantic dementia, a form of primary aphasia associated with a progressive frontal temporal lobar degeneration (PPA-FTLD) [3,4], who have relatively isolated left anterior temporal lobe degeneration reveal that some of these patients acquire new visual artistic skills. These observations suggest that loss of function in the left anterior temporal lobe may lead to the “facilitation” of right hemisphere mediated visual artistic skills. The concept that loss of function in one brain area can release or enhance functions mediated by other areas of the brain has not been fully explored or understood; however, one possible explanation is based on the concept that a lesion in a certain brain area might disrupt a cortical inhibitory network leading to facilitation in another brain area, a concept referred to as paradoxical functional facilitation [5]. This functional facilitation, for example, has been used
⁎ Corresponding author. Tel.: +1 352 352-273-5550; fax: +1 352 352-273-5575. E-mail address: [email protected]fl.edu (K.M. Heilman). 0022-510X/$ – see front matter. Published by Elsevier B.V. http://dx.doi.org/10.1016/j.jns.2012.09.029
to explain rightward attentional bias associated with right hemisphere lesions [6]. The same mechanism is thought to play a role in the emergence of visuo-spatial artistic skills in patients with left anterior temporal degeneration. However, there is paucity of converging evidence to support this postulate. Therefore, one way to test this hypothesis is to study patients with dysfunction of the same anatomical area caused by a different disease process. About one third of patients with anterior temporal lobe epilepsy have medically intractable seizures, many of whom are candidates for anterior temporal lobectomy [7]. According to the paradoxical functional facilitation hypothesis [5] since patients with chronic left anterior temporal lobe seizures may have left hemispheric dysfunction and subsequently have an ablation of their left anterior temporal lobes they should have greater visuo-spatial artistic ability than those patients who have long standing right anterior temporal lobe epilepsy and ablation of their anterior left temporal lobe. Similarly, based on this disinhibition hypothesis, we may expect patients who have long standing right anterior temporal epilepsy and a right anterior temporal lobectomy to have an increase in their verbal creativity. Whereas some investigators have reported a decline of musical abilities with right temporal lobectomy [8,9] and trouble with word finding following left temporal lobectomy [10,11], to our knowledge no one has reported an increase in verbal creativity with right temporal lobectomy or an increase of visual artistic creativity with removal of the left temporal lobe.
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G.A. Ghacibeh, K.M. Heilman / Journal of the Neurological Sciences 324 (2013) 45–48
Some great artists such as Leonardo Da Vinci, Michelangelo and Van Gogh, as well as some creative authors, such as Lewis Carroll, Edgar Allan Poe, Fyodor Dostoevsky were thought to have temporal lobe epilepsy. Whereas these creative geniuses did not have temporal lobectomy and the type as well as the laterality of their seizures is unknown, it is possible that temporal lobe epilepsy, altered their brain connectivity of the hemisphere that is ipsilateral to their seizure focus and this change enhanced the specific form of creativity that is heavily dependent on that hemisphere. Thus, the purpose of this study is twofold, and includes testing the disinhibition postulate of creative innovation in patients with temporal lobe epilepsy who underwent surgical resection of their left or right anterior temporal lobe as well as to learn if there are verbal versus visuospatial differences in creativity as a function of seizure laterality. 2. Methods 2.1. Subjects Eighteen patients (9 men and 9 women, age: 40±12) with medically refractory temporal lobe epilepsy, who underwent standard temporal lobectomy at least 6 months prior to testing (median: 24 months, range: 7–166), served as study participants. Nine patients had left temporal lobectomy for left temporal lobe epilepsy (5 men, 4 women) and 9 patients had right temporal lobectomy for right temporal lobe epilepsy (5 women and 4 men). Table 1 summarizes subject characteristics. The study was approved by the Institutional Review Board of the University of Florida and all subjects gave written informed consent. All subjects were right-handed by self report. All participants were still on their usual doses of anti-epileptic medications at the time of testing and were free of seizures. 2.2. Testing All 18 participants were assessed with the verbal and figural subtests of the Torrance Test of Creative Thinking (TTCT), form A [12–14]. Following the instructions provided by the publisher of the TTCT, all testing was completed in a single session. The figural subtest of the TTCT consists of 3 activities. During all three figural activities, subjects are given different types of incomplete figures and are asked to complete them by turning them into significant pictures, as well as giving
them titles. Although all three figural activities have similarities, the types of incomplete figures are different and tap into different aspects of creative functioning [14]. The verbal subtest consists of six activities. During the first three activities, subjects are given a drawing and are asked to come up with a list of answers describing the action taking place in the drawing, its causes and consequences. In the fourth activity, subjects are shown a drawing of a toy and are asked to come up with ideas that would improve it. In the fifth activity, subjects are asked to think of unusual uses of a specific object, such as a brick or a cardboard. The last activity consists of a hypothetical scenario where subjects are asked to suppose that a certain unlikely scenario happened (example: clouds had strings attached to them which head down to earth) and are asked to come up a list of ideas about the consequences of such a situation. All test sheets were de-identified, coded and mailed to the publisher, Scholastic Testing Service, Inc., for scoring. Scoring was performed following the scoring manuals. The figural tasks are scored on fluency, originality, abstractness of titles, elaboration and resistance to premature closure. Raw scores are generated for each of the 5 dimensions then an average score is calculated and normalized for age. In addition, a 13 point check list for creative strength is also calculated for each of the 5 dimensions, and the results are computed with the average score to generate a Figural Creativity Index (FCI) [14]. The verbal tasks are scored on fluency, originality and flexibility. Raw scores are generated for each of the 3 dimensions and averaged for each subject, then normalized for age to generate a verbal average score which will be referred to as the Verbal Creativity Index (VCI). 2.3. Statistical analysis To ensure that both the right and left temporal lobectomy groups did not differ, age and time since surgery were compared using independent t-tests. To assess for significant differences in creativity between the two groups, a two-way repeated measures analysis of variance (ANOVA) was used with the side of surgery (right versus left) being the between group factor and type of creativity (verbal versus figural) as being the within group factor. When appropriate, post-hoc analysis for pair wise comparisons was performed using paired t-tests. An alpha value level of 5% or less was considered statistically significant. 2.4. Results
Table 1 Patient characteristics and creativity scores. Patient
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18
Age
37 46 45 31 46 22 52 59 36 45 53 46 53 20 25 36 25 45
Sex
Female Female Female Female Male Male Male Male Male Female Female Female Female Female Male Male Male Male
TFS
63 24 89 97 8 14 24 166 6 125 79 21 13 7 7 28 24 21
Side
Left Left Left Left Left Left Left Left Left Right Right Right Right Right Right Right Right Right
AEDs
PHN, LEV LTG, ZNS CBZ, LEV LEV, CBZ OXC OXC, VPA OXC PHN, CBZ LTG, TOP VPA, PRM, LEV OXC OXC, TOP TOP, LEV, PRM, ALP CBZ, LEV, ZNS VPA, LEV CBZ, VPA LEV, LTG CBZ, TOP
Creativity scores Figural
Verbal
99 78 95 75 88 78 73 95 65 117 51 133 76 65 113 102 93 88
70 75 76 59 83 111 72 76 68 77 48 146 62 70 71 79 65 66
TFS: time from surgery in months; AEDs: anti-epileptic drugs; PHN: phenytoin; LEV: levetiracetam; LTG: lamotrigine; ZNS: zonisamide; CBZ: carbamazepine; OXC: oxcarbazepine; VPA: valproic acid; TOP: topiramate; PRM: primidone; ALP: alprazolam.
The subject characteristics and scores can be found in Table 1. There were no group differences in age and time since surgery. The ANOVA revealed no significant effect of side of surgery on overall creativity (p> 0.05) and no interaction between the side of surgery (right versus left) and the type of creativity (verbal versus figural). However, there was a significant major effect of creativity type (pb 0.05), figural being superior to verbal. Since we found that figural creativity was significantly better than verbal creativity, we wanted to learn if within each group performance on the verbal and figural creativity tasks was different. Paired t-tests were, therefore, performed independently for the RATL and LATL groups, comparing figural to verbal creativity indices. This analysis revealed no difference between the verbal and figural indices in the LATL group (p > 0.05); however, in the RATL group there was a significantly higher figural than verbal scores (p b 0.05). 3. Discussion The participants with LATL, when compared to those with RATL, did not have enhanced figural creativity. This finding fails to support the disinhibition postulate of enhanced figural creativity associated with PPA-FTLD. Similarly, the finding that patients with RATL did not have greater verbal creativity than those participants with LATL
G.A. Ghacibeh, K.M. Heilman / Journal of the Neurological Sciences 324 (2013) 45–48
provides further support against the disinhibition postulate. There are, however, several possible explanations for the failure to support paradoxical facilitation. First, although patients with PPA-FTLD with increased creativity were reported to have isolated left anterior temporal lobe atrophy, clinically, they had very poor social skills, suggesting that the disease process extended beyond the temporal lobe, most likely into the frontal lobe. Second, these patients with PPA-FTLD had lost much of their ability to use verbal communication and since their right hemisphere was relatively intact it is possible that they developed pictorial skills as a form of compensation. Since most patients with PPA-FTLD who developed increased creativity were not artists before this disease started, we cannot know if the left anterior temporal lobe degeneration enhanced their artistic-pictorial creativity or helped to initiate pictorial productions as a form of compensation. Support for this compensatory postulate comes from the study of an artist who developed the PPA form of FTLD [15]. The paintings created by this artist before the onset of her dementia compared to those after dementia onset, revealed that her artistic ability did not improve. Instead, the novelty of her work decreased, suggesting that FTLD did not improve artistic skills in this patient who already possessed these skills. In contrast, the disorder induced a decrease in novelty, a key component of creativity. Another report [16], of a patient with PPA-FTLD who was an artist before the onset of his disease and continued to produce artistic work after the onset of his dementia, revealed an improvement of technique that might be related to sparing and disinhibition of the right posterior neocortex, but a reduction of closure (completeness of the painting), possibly induced by impersistence and a decrease in evocative impact which might be explained by frontal and anterior temporal lobe-limbic dysfunction. The third explanation of the inconsistency between our results and the reports that some patients with PPA-FTLD who developed artistic creativity is based on the fundamental differences between the two diseases. Unlike the patients with PPA-FTLD who have progressive neuronal degeneration, patients with chronic epilepsy have frequent recurrent seizures that may alter certain neuronal networks and lead to differences in the way certain brain areas react to acute injuries. A potentially important finding of this study is that patients with RATL performed better at creative figural productions than they did on the verbal task. It is not known if this relative superiority of figural creativity is due to chronic right temporal lobe epilepsy or to the surgery itself. As mentioned, it is possible that chronic epilepsy with recurrent seizures can lead to alterations of neuronal networks in several brain areas. This postulate has been supported by functional and anatomical MRI studies of patients with temporal lobe epilepsy that revealed changes in the pattern of activation of certain functional areas and even atrophy of brain regions outside the primary epileptic focus [17–20]. Therefore, it is possible that recurrent seizures arising in the right temporal lobe might lead to permanent changes in other brain regions, resulting in increased visual–figural creativity. The relationship between their epilepsy and creative innovation is far from being understood, but, these results certainly raises an important question regarding the potential impact of recurrent seizures on brain plasticity and creativity. In contrast to the enhanced visual–figural creativity associated with right anterior temporal epilepsy, there was no evidence that patients with LATL performed better at the verbal than pictorial-drawing tasks. As mentioned patients with left anterior temporal lobe epilepsy and treatment with lobectomy, like patients with degenerative disease of this same region, have problems with word finding [10,11] and this disability may have adversely influenced their verbal creativity. The reason that focal seizures may enhance brain creativity is unknown. Based on ablation and functional imaging studies it is now known that the brain is organized in modular fashion. Therefore, creative people might have the ability to activate more highly distributed networks. Support for this theory comes from electroencephalographic (EEG) studies of normal subjects who demonstrated an increase of anatomically distributed coherence of EEG oscillations
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while engaged in creative thought-innovation [21,22]. Donald Hebb suggested that neurons that fire together wire together [23], and during a temporal lobe seizure, there is EEG coherence between temporal lobe structures and other areas of the neocortex as well as high coherence values between neocortical structures [24]. Thus, seizure-induced coherence might enhance connectivity and with right temporal seizures, the enhanced right hemisphere connectivity might have lead to enhanced right hemisphere mediated visual artistic creativity. Our study had a small number of subjects in each group and thus it may be of value to learn if our results can be replicated in future studies with more subjects in each group. In addition future research should contrast those participants with right temporal lobe epilepsy, who have not undergone an anterior temporal lobectomy, with those who have had this surgery, to help distinguish the impact of chronic epilepsy from that of the surgery on figural creative innovation. Disclosure The data presented in this manuscript was previously presented, in part, as a poster, at the 61st Annual Meeting of the American Epilepsy Society in Philadelphia, December 2007 and published as an abstract in Epilepsia suppl. (Abst. 2.253), 2007. Conflict of interest There is no conflict of interest. Acknowledgments The authors would like to thank Akhil Patel, Sandeep Konka and Kathrine Winter for their help in testing the participants and John Williamson PhD for being our statistical consultant. References [1] Bronowski J. Science and human values. New York: Harpwer and Row; 1972. [2] Heilman KM, Nadeau SE, Beversdorf DO. Creative innovation: possible brain mechanisms. Neurocase 2003;9:369-79. [3] Miller BL, Boone K, Cummings JL, Read SL, Mishkin F. Functional correlates of musical and visual ability in frontotemporal dementia. Br J Psychiatry 2000;176:458-63. [4] Miller BL, Cummings J, Mishkin F, Boone K, Prince F, Ponton M, et al. Emergence of artistic talent in frontotemporal dementia. Neurology 1998;51:978-82. [5] Kapur N. Paradoxical functional facilitation in brain-behaviour research. A critical review. Brain 1996;119:1775-90 (Pt 5). [6] Kinsbourne M. A model for the mechanism of unilateral neglect of space. Trans Am Neurol Assoc 1970;95:143-6. [7] Engel J, Wiebe S, French J, Sperling M, Williamson P, Spencer D, et al. Practice parameter: temporal lobe and localized neocortical resections for epilepsy. Report of the Quality Standards Subcommittee of the American Academy of Neurology, in Association with the American Epilepsy Society and the American Association of Neurological Surgeons. Epilepsia 2003;44:741-51. [8] Kester DB, Saykin AJ, Sperling MR, O'Connor MJ, Robinson LJ, Gur RC. Acute effect of anterior temporal lobectomy on musical processing. Neuropsychologia 1991;29: 703-8. [9] Zatorre RJ. Discrimination and recognition of tonal melodies after unilateral cerebral excisions. Neuropsychologia 1985;23:31-41. [10] Davies KG, Risse GL, Gates JR. Naming ability after tailored left temporal resection with extraoperative language mapping: increased risk of decline with later epilepsy onset age. Epilepsy Behav 2005;7:273-8. [11] Heilman KM, Wilder BJ, Malzone WF. Anomic aphasia following anterior temporal lobectomy. Trans Am Neurol Assoc 1972;97:291-3. [12] Torrance EP. Torrance tests of creative thinking: manual for scoring and interpreting results, verbal, forms A&B. Bensenville, IL: Scholastic Testing Service, Inc.; 1990. [13] Torrance EP. Torrance tests of creative thinking: norms-technical manual, figural forms A&B. Bensenville, IL: Scholastic Testing Services, Inc.; 1998. [14] Torrance EP, Ball OE, Safter HT. Torrance tests of creative thinking: streamlined scoring guide, figural A&B. Bensenville, IL: Scholastic Testing Service, Inc.; 1992. [15] Finney GR, Heilman KM. Artwork before and after onset of progressive nonfluent aphasia. Cogn Behav Neurol 2007;20:7–10. [16] Drago V, Foster PS, Trifiletti D, FitzGerald DB, Kluger BM, Crucian GP, et al. What's inside the art? The influence of frontotemporal dementia in art production. Neurology 2006;67:1285-7.
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