FULL-LENGTH ORIGINAL RESEARCH
Better object recognition and naming outcome with MRI-guided stereotactic laser amygdalohippocampotomy for temporal lobe epilepsy *†‡Daniel L. Drane, *†David W. Loring, §Natalie L. Voets, *Michele Price, ¶Jeffrey G. Ojemann, *#Jon T. Willie, **Amit M. Saindane, ‡Vaishali Phatak, *Mirjana Ivanisevic, ††Scott Millis, *†Sandra L. Helmers, ‡¶John W. Miller, *†Kimford J. Meador, and *#Robert E. Gross Epilepsia, 56(1):101–113, 2015 doi: 10.1111/epi.12860
SUMMARY
Dr. Daniel L. Drane is Assistant Professor of Neurology and Pediatrics at Emory University School of Medicine.
Objectives: Patients with temporal lobe epilepsy (TLE) experience significant deficits in category-related object recognition and naming following standard surgical approaches. These deficits may result from a decoupling of core processing modules (e.g., language, visual processing, and semantic memory), due to “collateral damage” to temporal regions outside the hippocampus following open surgical approaches. We predicted that stereotactic laser amygdalohippocampotomy (SLAH) would minimize such deficits because it preserves white matter pathways and neocortical regions that are critical for these cognitive processes. Methods: Tests of naming and recognition of common nouns (Boston Naming Test) and famous persons were compared with nonparametric analyses using exact tests between a group of 19 patients with medically intractable mesial TLE undergoing SLAH (10 dominant, 9 nondominant), and a comparable series of TLE patients undergoing standard surgical approaches (n = 39) using a prospective, nonrandomized, nonblinded, parallel-group design. Results: Performance declines were significantly greater for the patients with dominant TLE who were undergoing open resection versus SLAH for naming famous faces and common nouns (F = 24.3, p < 0.0001, g2 = 0.57, and F = 11.2, p < 0.001, g2 = 0.39, respectively), and for the patients with nondominant TLE undergoing open resection versus SLAH for recognizing famous faces (F = 3.9, p < 0.02, g2 = 0.19). When examined on an individual subject basis, no SLAH patients experienced any performance declines on these measures. In contrast, 32 of the 39 patients undergoing standard surgical approaches declined on one or more measures for both object types (p < 0.001, Fisher’s exact test). Twenty-one of 22 left (dominant) TLE patients declined on one or both naming tasks after open resection, while 11 of 17 right (nondominant) TLE patients declined on face recognition. Significance: Preliminary results suggest (1) naming and recognition functions can be spared in TLE patients undergoing SLAH, and (2) the hippocampus does not appear to be an essential component of neural networks underlying name retrieval or recognition of common objects or famous faces.
Accepted October 3, 2014; Early View publication December 8, 2014. *Department of Neurology, Emory University School of Medicine, Atlanta, Georgia, U.S.A.; †Department of Pediatrics, Emory University School of Medicine, Atlanta, Georgia, U.S.A.; ‡Department of Neurology, University of Washington School of Medicine, Seattle, Washington, U.S.A.; §Nuffield Department of Clinical Neurosciences, FMRIB Centre, University of Oxford, Oxford, United Kingdom; ¶Department of Neurological Surgery, University of Washington School of Medicine, Seattle, Washington, U.S.A.; #Department of Neurosurgery, Emory University School of Medicine, Atlanta, Georgia, U.S.A.; **Department of Radiology, Emory University School of Medicine, Atlanta, Georgia, U.S.A.; and ††Department of Physical Medicine & Rehabilitation, Wayne State University School of Medicine, Detroit, Michigan, U.S.A. Address correspondence to Daniel L. Drane, Departments of Neurology and Pediatrics, Emory University School of Medicine, Woodruff Memorial Research Building, 101 Woodruff Circle, Suite 6111, Mailstop 1930-001-1AN, Atlanta, GA 30322, U.S.A. E-mail: [email protected] Wiley Periodicals, Inc. © 2014 International League Against Epilepsy
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102 D. L. Drane et al. KEY WORDS: Epilepsy surgery, Naming and recognition, Cognitive outcome, Famous faces, Laser interstitial thermal therapy.
Magnetic resonance imaging (MRI)–guided stereotactic laser amygdalohippocampotomy (SLAH) is a novel, minimally invasive approach to epilepsy surgery. SLAH holds promise for reducing procedure duration and hospital stay,1 has cosmetic advantages, involves less pain and discomfort, and may minimize postsurgical cognitive decline associated with standard resections. Initial experience with SLAH for mesial temporal lobe epilepsy (TLE) demonstrates that it can eliminate seizures in well-selected patients,2,3 but cognitive outcomes have not yet been reported. Decreased naming ability, often more pronounced for proper nouns (e.g., famous faces, landmarks), commonly occurs after language-dominant (typically left-sided) anteromedial TL resection.4–7 Furthermore, we have demonstrated meaningful declines in recognition of famous faces and select object categories (e.g., landmarks and animals but not common object recognition) following right anteromedial TL resection.5,7,8 Because assessment of these functions is not a routine component of preoperative evaluation at most epilepsy centers, these declines in famous face and object recognition have not been widely appreciated. Nevertheless, naming and recognition deficits can cause social, vocational, and academic difficulty. Duffau et al.9 demonstrated that even a subtle decline in naming response speed in patients undergoing tumor surgery involving the anterior TL region predicted a poor outcome in terms of returning to work. Fortunately, the effects of face and object recognition deficits on daily life in some patient groups are becoming increasingly recognized.10 Naming and recognition deficits may reflect temporal stem white matter (WM) damage sustained during access to, rather than direct resection of, mesial TL structures.7 Indeed, naming and recognition deficits characteristic of semantic dementia result from pathology of bilateral temporal poles and lateral inferior temporal gyri, initially sparing mesial TL.11 Nevertheless, many researchers, particularly in the setting of epilepsy, consider the hippocampus critical for naming and recognition based on (1) its activation during functional neuroimaging studies of object and face naming,12 (2) volumetric studies associating smaller hippocampal volume with poorer naming,13 and (3) observations that naming deficits always occurred when the hippocampus was included in the resection despite patients undergoing cortical stimulation mapping.14 However, open resections including the hippocampus typically affect broader anteromedial TL regions and white matter, making it difficult to attribute such declines solely to this structure. Research involving patients with congenital prosopagnosia who are unable to recognize familiar persons provides a Epilepsia, 56(1):101–113, 2015 doi: 10.1111/epi.12860
working hypothesis for declines in famous face recognition following right TLE surgery. Patients with congenital prosopagnosia experience defects in their bilateral inferior visual processing stream (including the inferior lateral fasciculus [ILF] and inferior frontooccipital fasciculus [IFOF]), with dysfunction of these pathways in the right hemisphere correlating with poor face recognition performance.15 Most open anteromedial TL resections affect one or both of these WM pathways, with the IFOF comprising the posterior two thirds of the WM running through the temporal stem.16 In addition, some open resections also encroach upon the fusiform gyrus, which has been implicated in the processing of faces.17 Therefore, we examined the relationship between hippocampal resection and outcome for naming and recognition as a function of whether collateral tissue was spared. Our primary hypotheses were the following: (1) a greater frequency of dominant TL patients undergoing open anteromedial resection will experience significant naming declines on either famous faces or common objects than will dominant TL patients undergoing SLAH; (2) a greater frequency of nondominant TL patients undergoing open anteromedial resection will experience significant recognition declines for famous faces than will nondominant TL patients undergoing SLAH; and (3) no patients undergoing anteromedial resection or SLAH will experience recognition declines for common objects (as prior work has related decline in this area to posterior TL lesions).18
Methods Subjects We present pre- and postsurgical data for 39 patients undergoing traditional open anteromedial TL resections at either Emory University or the University of Washington, and 19 patients undergoing SLAH at Emory only. Institutional review board approval for this study was obtained at both universities, and all patients provided informed consent. Patients were at least 18 years of age and native English speakers. All patients were left-hemisphere dominant for language, with the exception of two SLAH patients. One left SLAH patient was exclusively right-language dominant by Wada testing, and one right SLAH had bilateral language dominance by Wada testing (left > right). Both patients were included in the nondominant resection group (see Table 1 for demographic data). Two additional patients underwent SLAH at Emory University during the same period. One was excluded due to age (
Better object recognition and naming outcome with MRI-guided stereotactic laser amygdalohippocampotomy for temporal lobe epilepsy *†‡Daniel L. Drane, *†David W. Loring, §Natalie L. Voets, *Michele Price, ¶Jeffrey G. Ojemann, *#Jon T. Willie, **Amit M. Saindane, ‡Vaishali Phatak, *Mirjana Ivanisevic, ††Scott Millis, *†Sandra L. Helmers, ‡¶John W. Miller, *†Kimford J. Meador, and *#Robert E. Gross Epilepsia, 56(1):101–113, 2015 doi: 10.1111/epi.12860
SUMMARY
Dr. Daniel L. Drane is Assistant Professor of Neurology and Pediatrics at Emory University School of Medicine.
Objectives: Patients with temporal lobe epilepsy (TLE) experience significant deficits in category-related object recognition and naming following standard surgical approaches. These deficits may result from a decoupling of core processing modules (e.g., language, visual processing, and semantic memory), due to “collateral damage” to temporal regions outside the hippocampus following open surgical approaches. We predicted that stereotactic laser amygdalohippocampotomy (SLAH) would minimize such deficits because it preserves white matter pathways and neocortical regions that are critical for these cognitive processes. Methods: Tests of naming and recognition of common nouns (Boston Naming Test) and famous persons were compared with nonparametric analyses using exact tests between a group of 19 patients with medically intractable mesial TLE undergoing SLAH (10 dominant, 9 nondominant), and a comparable series of TLE patients undergoing standard surgical approaches (n = 39) using a prospective, nonrandomized, nonblinded, parallel-group design. Results: Performance declines were significantly greater for the patients with dominant TLE who were undergoing open resection versus SLAH for naming famous faces and common nouns (F = 24.3, p < 0.0001, g2 = 0.57, and F = 11.2, p < 0.001, g2 = 0.39, respectively), and for the patients with nondominant TLE undergoing open resection versus SLAH for recognizing famous faces (F = 3.9, p < 0.02, g2 = 0.19). When examined on an individual subject basis, no SLAH patients experienced any performance declines on these measures. In contrast, 32 of the 39 patients undergoing standard surgical approaches declined on one or more measures for both object types (p < 0.001, Fisher’s exact test). Twenty-one of 22 left (dominant) TLE patients declined on one or both naming tasks after open resection, while 11 of 17 right (nondominant) TLE patients declined on face recognition. Significance: Preliminary results suggest (1) naming and recognition functions can be spared in TLE patients undergoing SLAH, and (2) the hippocampus does not appear to be an essential component of neural networks underlying name retrieval or recognition of common objects or famous faces.
Accepted October 3, 2014; Early View publication December 8, 2014. *Department of Neurology, Emory University School of Medicine, Atlanta, Georgia, U.S.A.; †Department of Pediatrics, Emory University School of Medicine, Atlanta, Georgia, U.S.A.; ‡Department of Neurology, University of Washington School of Medicine, Seattle, Washington, U.S.A.; §Nuffield Department of Clinical Neurosciences, FMRIB Centre, University of Oxford, Oxford, United Kingdom; ¶Department of Neurological Surgery, University of Washington School of Medicine, Seattle, Washington, U.S.A.; #Department of Neurosurgery, Emory University School of Medicine, Atlanta, Georgia, U.S.A.; **Department of Radiology, Emory University School of Medicine, Atlanta, Georgia, U.S.A.; and ††Department of Physical Medicine & Rehabilitation, Wayne State University School of Medicine, Detroit, Michigan, U.S.A. Address correspondence to Daniel L. Drane, Departments of Neurology and Pediatrics, Emory University School of Medicine, Woodruff Memorial Research Building, 101 Woodruff Circle, Suite 6111, Mailstop 1930-001-1AN, Atlanta, GA 30322, U.S.A. E-mail: [email protected] Wiley Periodicals, Inc. © 2014 International League Against Epilepsy
101
102 D. L. Drane et al. KEY WORDS: Epilepsy surgery, Naming and recognition, Cognitive outcome, Famous faces, Laser interstitial thermal therapy.
Magnetic resonance imaging (MRI)–guided stereotactic laser amygdalohippocampotomy (SLAH) is a novel, minimally invasive approach to epilepsy surgery. SLAH holds promise for reducing procedure duration and hospital stay,1 has cosmetic advantages, involves less pain and discomfort, and may minimize postsurgical cognitive decline associated with standard resections. Initial experience with SLAH for mesial temporal lobe epilepsy (TLE) demonstrates that it can eliminate seizures in well-selected patients,2,3 but cognitive outcomes have not yet been reported. Decreased naming ability, often more pronounced for proper nouns (e.g., famous faces, landmarks), commonly occurs after language-dominant (typically left-sided) anteromedial TL resection.4–7 Furthermore, we have demonstrated meaningful declines in recognition of famous faces and select object categories (e.g., landmarks and animals but not common object recognition) following right anteromedial TL resection.5,7,8 Because assessment of these functions is not a routine component of preoperative evaluation at most epilepsy centers, these declines in famous face and object recognition have not been widely appreciated. Nevertheless, naming and recognition deficits can cause social, vocational, and academic difficulty. Duffau et al.9 demonstrated that even a subtle decline in naming response speed in patients undergoing tumor surgery involving the anterior TL region predicted a poor outcome in terms of returning to work. Fortunately, the effects of face and object recognition deficits on daily life in some patient groups are becoming increasingly recognized.10 Naming and recognition deficits may reflect temporal stem white matter (WM) damage sustained during access to, rather than direct resection of, mesial TL structures.7 Indeed, naming and recognition deficits characteristic of semantic dementia result from pathology of bilateral temporal poles and lateral inferior temporal gyri, initially sparing mesial TL.11 Nevertheless, many researchers, particularly in the setting of epilepsy, consider the hippocampus critical for naming and recognition based on (1) its activation during functional neuroimaging studies of object and face naming,12 (2) volumetric studies associating smaller hippocampal volume with poorer naming,13 and (3) observations that naming deficits always occurred when the hippocampus was included in the resection despite patients undergoing cortical stimulation mapping.14 However, open resections including the hippocampus typically affect broader anteromedial TL regions and white matter, making it difficult to attribute such declines solely to this structure. Research involving patients with congenital prosopagnosia who are unable to recognize familiar persons provides a Epilepsia, 56(1):101–113, 2015 doi: 10.1111/epi.12860
working hypothesis for declines in famous face recognition following right TLE surgery. Patients with congenital prosopagnosia experience defects in their bilateral inferior visual processing stream (including the inferior lateral fasciculus [ILF] and inferior frontooccipital fasciculus [IFOF]), with dysfunction of these pathways in the right hemisphere correlating with poor face recognition performance.15 Most open anteromedial TL resections affect one or both of these WM pathways, with the IFOF comprising the posterior two thirds of the WM running through the temporal stem.16 In addition, some open resections also encroach upon the fusiform gyrus, which has been implicated in the processing of faces.17 Therefore, we examined the relationship between hippocampal resection and outcome for naming and recognition as a function of whether collateral tissue was spared. Our primary hypotheses were the following: (1) a greater frequency of dominant TL patients undergoing open anteromedial resection will experience significant naming declines on either famous faces or common objects than will dominant TL patients undergoing SLAH; (2) a greater frequency of nondominant TL patients undergoing open anteromedial resection will experience significant recognition declines for famous faces than will nondominant TL patients undergoing SLAH; and (3) no patients undergoing anteromedial resection or SLAH will experience recognition declines for common objects (as prior work has related decline in this area to posterior TL lesions).18
Methods Subjects We present pre- and postsurgical data for 39 patients undergoing traditional open anteromedial TL resections at either Emory University or the University of Washington, and 19 patients undergoing SLAH at Emory only. Institutional review board approval for this study was obtained at both universities, and all patients provided informed consent. Patients were at least 18 years of age and native English speakers. All patients were left-hemisphere dominant for language, with the exception of two SLAH patients. One left SLAH patient was exclusively right-language dominant by Wada testing, and one right SLAH had bilateral language dominance by Wada testing (left > right). Both patients were included in the nondominant resection group (see Table 1 for demographic data). Two additional patients underwent SLAH at Emory University during the same period. One was excluded due to age (
