Epilepsy Research (2014) 108, 748—754
journal homepage: www.elsevier.com/locate/epilepsyres
Temporal lobe epilepsy surgery modulates the activity of auditory pathway Margarita Minou Báez-Martín a,∗, Lilia María Morales-Chacón a, Iván García-Maeso a, Bárbara Estupi˜ nán-Díaz a, Lourdes Lorigados-Pedre a, María Eugenia García a, Reynaldo Galvizu a, Juan E. Bender a, Ivette Cabrera-Abreu a, Yamila Pérez-Téllez a, Lídice Galán b a b
International Center for Neurological Restoration (CIREN), Ave. 25 #15805% 158-160, Havana 11300, Cuba Cuban Neuroscience Center (CNC), Ave. 25 #15202% 158-160, Havana 11300, Cuba
Received 26 August 2013; received in revised form 6 February 2014; accepted 28 February 2014 Available online 12 March 2014
KEYWORDS Auditory brainstem response; Drug-resistant epilepsy; Magnetic resonance imaging; Middle latency response; Temporal lobectomy
∗
Summary The purpose of this paper is to evaluate the effects of the anterior temporal lobectomy on the functional state of the auditory pathway in a group of drug-resistant epileptic patients, linking the electrophysiological results to the resection magnitude. Twenty-seven patients with temporal lobe epilepsy and a matched control group were studied. Auditory brainstem and middle latency responses (ABR and MLR respectively) were carried out before and after 6, 12 and 24 months surgical treatment. The volume and longitude of temporo-mesial resected structures were estimated on magnetic resonance images taken 6 months after surgery. Before the intervention the patients showed a significant delay of latency in waves III, V, Pa and Nb, with an increase in duration of I—V interval in comparison with healthy subjects (Mann—Whitney Utest, p < 0.05). After resection, additional significant differences in waves I and Na latency were observed. Na and Pa waveforms showed a tendency to increase in amplitude, which became statistically significant 12 months after surgery for right hemisphere lobectomized patients in the midline electrode, and in Pa waveform for all patients in the temporal electrodes ipsilateral to resection (Wilcoxon test, p < 0.05). In general, latency variations of MLR correlated with resection longitude, while changes in amplitude correlated with the volume of the resection in the middle temporal pole and amygdala (Pearson’ correlation test, p < 0.05). As a result, we assume that anterior temporal lobectomy provokes functional modifications into the auditory pathway, probably related to an indirect modulation of its activity by the temporo-mesial removed structures. © 2014 Published by Elsevier B.V.
Corresponding author. Tel.: +53 7 273 6356; fax: +53 7 273 6028. E-mail address: [email protected] (M.M. Báez-Martín).
http://dx.doi.org/10.1016/j.eplepsyres.2014.02.017 0920-1211/© 2014 Published by Elsevier B.V.
Effects of the anterior temporal lobectomy
Introduction Temporal lobe epilepsy is the most common type of focal epilepsy in adults. In most cases it involves the temporomesial structures (Gronich et al., 2002). The complex partial seizures in this entity often become drug-resistant, but it is a surgically remediable syndrome (Engel, 2009), showing a resolution of seizures in as much as 70—85% of patients after resection of the epileptogenic area (Karceski and Morrell, 2006). The anterior temporal lobectomy may cause changes in the visual and auditory pathways considering their close relationships with the temporal horn of the lateral ventricles, and the projections to the occipital calcarine banks and the temporal operculum respectively (Sindou and Guenot, 2003). Some efferent projection fibers of the temporal cortex go to the amygdala and hippocampus (Kiernan, 2012), structures that are also total or partially resected during the anterior temporal lobectomy. The most common sensorial sequel is a superior quadrantanopia contralateral to the side of resection secondary to the damage of the Meyer’ loop of the geniculocalcarine tract (Compston, 2005; Winston et al., 2012). It has been well established using both anatomical (Winston et al., 2012; Yogarajah et al., 2009) and functional procedures (Babb et al., 1982; Baez Martin et al., 2010). However, few reports have considered the possibility of changes in the primary auditory pathway after the resection of temporo-mesial structures (Bougeard and Fischer, 2002; Jacobson et al., 1990; Khalfa et al., 2001). Standardized anterior temporal lobectomy removed 4—7 cm of the anterior temporal lobe, including mesial temporal structures (Engel, 2009) and sparing the superior temporal gyrus involved in auditory processing. After this procedure, hearing may be impaired and dichotic listening scores reduced on the ear contralateral to the operated temporal lobe (Bougeard and Fischer, 2002). Contrary to these results, the improvement of the automatic central auditory change-detection after a successful resection of the temporal pole has been demonstrated using the mismatch negativity magnetic equivalent (Lin et al., 2007). Auditory brainstem and middle latency responses (ABR and MLR respectively) have been widely used to evaluate the functional state of the auditory pathway. They represent the electrical activity associated with the sequential activation of the auditory pathway from the cochlear nerve to the primary auditory cortex (Legatt, 2005). The midline Na component of MLR appears to originate subcortically in either the inferior colliculi or medial geniculate body of the thalamus, while the Pa component is related to the activity of the auditory radiations and primary auditory cortex in the Heschl gyrus (Baez-Martin and Cabrera-Abreu, 2003). Other studies in patients with temporal and extratemporal epilepsy suggest that MLR may be generated subcortically but modulated by temporal lobe structures (Weate et al., 1996) some of them could be damaged during the temporal lobectomy. This paper proposes the use of ABR and MLR to evaluate the effect of the anterior temporal lobectomy in the functional state of the auditory pathway of drug-resistant
749 epileptic patients, measuring the relationship of the electrophysiological results with the magnitude of resection.
Subjects and methods Subjects Twenty-seven temporal lobe epileptic patients were evaluated at the Telemetric Unit of the International Center for Neurological Restoration in a prospective study. Presurgical evaluation was performed including the localization of ictal zone combining EEG-video, ictal and interictal SPECT, qualitative and quantitavive MRI (voxel-based morphometry) (Ashburner and Friston, 2000) and neuropsychological tests. Clinical and demographical data of patients and controls are shown in Table 1. The most frequently used drugs for treatment were valproate, carbamazepine and clonazepam. Treatment was not changed after the surgical procedure. All patients underwent standard anterior temporal lobectomy guided by electrocorticography. Tissue samples obtained during surgery were processed for histology. Hippocampal sclerosis was defined and focal cortical dysplasia in temporal neocortex classified according to Palmini’ criteria (Palmini et al., 2004) (Table 1). Sixteen age- and gender-matched healthy subjects (free of neurological and audiological diseases) were also neurophysiologically studied. Hearing threshold level was evaluated both in patients and healthy subjects. All of them were right-handed and gave their signed consent to participate in the study.
Electrophysiological tests To record the auditory evoked responses, surface electrodes (Ag/ClAg) were attached to the scalp according to the international 10-20 system (Table 2). The electrode impedance was kept below 5 k. Records were made by an experienced technician under the supervision of a neurophysiologist, who controlled that subjects stayed awake during the recording of the MLR. They were invited to lie on bed in a climate-controlled room during the tests. Patients were evaluated before surgical resection, as well as six, twelve and twenty-four months after surgery. Recording conditions and equipment Recording conditions are summarized in Table 2. The stimuli were 0.1 ms. alternating clicks delivered through a headphone (DR-531B-7, Elegas Acous Co. Ltd, Japan). The records were obtained using the evoked potentials measuring systems Neuropack four-mini and Neuropack M1 (Nihon Kohden, Japan). Evaluation of records Records were evaluated off-line in a visual inspection mode by two clinical neurophysiologists. Measured variables were absolute latency, interpeak intervals and amplitude of I, III, V, Na, Pa and Nb waveforms. Latencies 2.5 SD longer than the average value from normal subjects, and amplitudes lower
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M.M. Báez-Martín et al.
4 3 5 5
1 2
—
4 3
NO 2A 1B 1A
Parameters
ABR
MLR
Analysis time (ms) Filters (Hz) Stimulus frequency (Hz) Maximal intensity (dBnHL) Average responses Sensibility (V/div) Recording electrodes Reference electrode Ground electrode Stimulation mode
10 100—3000 10 105 2000 5 A1, A2 Cz Fpz Monoaural
100 20—1000 5 90 500 20 Cz, T3, T4 A1-A2 Fpz Binaural
FCD, focal cortical dysplasia; X (SD), mean value (standard deviation).
5 7 8 14 13 16 Patients Left hemisphere lobectomy Right hemisphere lobectomy Healthy subjects
F M
9 6 8
33.07 (9.06) 34.69 (5.28) 33.68 (7.96)
21.14 (9.08) 22.53 (12.14) —
Duration of illness years X (SD)
14 13 —
Temporo-mesial resected volume and longitude
Age years X (SD) Sex N
Clinical and demographical characteristics of the sample. Table 1
ABR and MLR recording conditions.
than the minimal value in the control group were considered abnormal. The absence of the waveform was also considered as abnormal.
Temporo-mesial sclerosis N
FCD in temporal neocortex
Table 2
The longitude of resection was evaluated in twenty-two patients; nineteen of them were also submitted to volumetric measurements. The volume of temporo-mesial resected tissue was measured on MRI images six months after surgery (Magnetom Symphony SIEMENS of 1.5 T) in those cases where quantitative MRI was possible. The methodology to obtain the images and the volumetric measures has been described in detail elsewhere by Trápaga Quincoses and Morales Chacon (2008). The resected volumes of superior, medial and inferior temporal gyri, amygdala, hippocampus, parahippocampus, superior and middle temporal poles from both hemispheres were considered for analysis (n = 10). The residual index of these structures (residual volume of resected side/volume of not resected side × 100) was also calculated (n = 17), taking into account that a low value of the residual index of a structure means a mayor lesion. The absolute longitude of lateral and mesial resected tissue was measured by the neurosurgeon using slices of images in T1, T2 and FLAIR six months after surgery. The lateral (neocortical) aspect included the distance (in mm) between the posterior edge of the internal table and the anterior limit of the resected area, considering the middle temporal gyrus in the axial slices of MRI, whereas the mesial aspect was calculated from axial slices in parallel with the preserved hippocampus. Two tangential lines were drawn: one between the posterior border of the resection and the contralateral hippocampus, and the other between the anterior limit of the preserved hippocampus and the side of resection. The distance between these tangential lines was the mesial longitude.
Statistics Normality of the data was tested using Shapiro—Wilk’ Wtest. The results showed non-normal distribution of some variables. Therefore non-parametric inference was used for comparisons.
Effects of the anterior temporal lobectomy
Figure 1
Mean value of waves I and III latency before and after treatment (6, 12, and 24 months). Wilcoxon test,
The data analysis included the comparison between patients and control subjects before treatment (Mann—Whitney U-test) and the comparison of the auditory evoked responses obtained from epileptic patients at different times of the following (Wilcoxon test). Relationships between the normalized post-surgical electrophysiological data (6 months) and the volume, residual index, and longitude of dissected tissue were calculated (Pearson’ correlation test). Normalization of the data was carried out using the mean and standard deviation values of the control group. Differences were considered significant if p < 0.05 for all tests.
Results Characteristics of the patient’ sample No difference was found between left and right hemisphere lobectomized patients (L-HL and R-HL respectively)
Figure 2 p < 0.05).
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√
p < 0.05.
regarding age, gender, and duration of illness before treatment (Mann—Whitney U-test, p > 0.05). The hearing threshold level showed no significant differences between ears in pre-surgical evaluation, and there were no changes after treatment in both groups in comparison with the first measurement (Wilcoxon test, p > 0.05).
Electrophysiology Pre-operative findings There were statistically significant differences between patients and controls in I—V interval duration (higher in patients) secondary to a pronounced delay of wave V latency. A lower amplitude of wave III in comparison with healthy subjects was also found bilaterally (Mann—Whitney U-test, p < 0.05). Considering the side of the epileptogenic zone, the differences were in the R-HL group. Furthermore, significant differences in the latency of Nb waveform (longer in patients) were found (Mann—Whitney
Mean value of MLR amplitude before and after treatment (6, 12, and 24 months). Cz electrode (Wilcoxon test,
√
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U-test, p < 0.05). These results were independent of the epileptogenic zone lateralization. No difference was observed between patients with and without FCD in relation to electrophysiological variables (Mann—Whitney U-test, p < 0.05). Post-operative changes Left hemisphere lobectomized (L-HL) patients showed a significant delay of wave I six months after treatment in relation to pre-surgical values in the ear ipsilateral to the resection (Wilcoxon test, p < 0.05). Similar results were observed in R-HL patients, in addition to a significant delay in wave I latency contralateral to the resection and wave III ipsilateral. There were no significant differences twelve and twentyfour months after surgery. However, these values did not return to the pre-surgical level (Fig. 1). In R-HL patients differences for Na waveform latency were statistically significant twelve months after surgery (Wilcoxon test, p < 0.05). Regarding the amplitude of these evoked responses, we could not find significant changes for ABR waves (data not shown). The Na and Pa components showed a tendency to increase in amplitude that became statistically significant twelve months after surgery on the region under the Cz electrode for R-HL patients (Wilcoxon test, p < 0.05) (Fig. 2). Similar results were found only for the Pa waveform in the medial temporal electrodes (T3 or T4) ipsilateral to the resection for all patients.
AEP results vs magnitude of surgical resection Six months after surgery no relation was detected between ABR variables and the temporo-mesial resected volume and longitude. However, MLR showed different results. The resected volume of the middle temporal pole showed a positive relationship with the amplitude of Na and Pa waveforms measured in Cz for all patients (r = 0.84 and r = 0.65 respectively; p < 0.05) (Fig. 3). The residual index of amygdala had a negative relationship with the amplitude of Pa in all cases (r = −0.59; p < 0.05), while its resected volume had a positive relationship with the latency of this component in L-HL patients (r = 0.77; p < 0.05). The longitude of resected tissue in its lateral aspect (neocortex) correlated with the latency of Na waveform for R-HL patients (r = 0.61; p < 0.05) and in the mesial aspect with the latency of Pa waveform for all patients (r = 0.51; p < 0.05) (Fig. 4).
Discussion The results showed variations both in ABR and in MLR of patients before treatment in comparison with normal subjects. Additional changes were detected immediately after surgery and during the follow up period. Some of them were closely related to anatomical measurements. There are reports of variations in the functional state of the auditory system in temporal lobe epileptic patients. For example, temporal lobe epilepsy affects the automatic central auditory change-detection (Hara et al., 2012), the mechanisms of discrimination from sequential sounds and
Figure 3 Relationship between the normalized values of waveforms Na (A) and Pa (B) amplitude and the volume of the resected middle temporal pole of right hemisphere lobectomized patients six months after surgery. Cz electrode (Pearson’ correlation test, p < 0.05).
tone patterns, the selective attention to verbal and nonverbal sounds (Meneguello et al., 2006) and the semantic processing (Miyamoto et al., 2000). Some of these effects have been evaluated both before and after the temporal lobectomy by means of event-related potentials. It has been reported prolonged peak and interpeak latencies in some components of the ABR and MLR of temporal lobe epileptic patients different from normal subjects (Baez-Martin and Cabrera-Abreu, 2003, 2005; Cabrera-Abreu et al., 2004). Some authors argued that these facts could depend on the medication, particularly carbamazepine (Clemens et al., 2004; Poblano et al., 2002). For example, Japaridze et al. (1993) suggest that carbamazepine exerts suppressive influences both on modally specific (lemniscal) and nonspecific (extralemniscal) auditory structures. We assume that pre-operative findings in our patients might be related to medication, particularly at brainstem level. But, the existence of temporo-mesial sclerosis
Effects of the anterior temporal lobectomy
Figure 4 Relationship between the normalized values of waveform Pa latency and the mesial longitude of resection six months after surgery (all patients). Cz electrode; Pearson’ correlation test, p < 0.05.
(demonstrated by MRI) may contribute to MLR results. Although it might be thought that FCD could be a contributing factor, no statistically confirmed evidence of this relationship was found. In our patients, medical treatment persisted identical while new changes appeared in ABR and MLR after temporal lobectomy (i.e. prolonged waves I, III and Na latencies). This might suggest an indirect effect of the procedure on the functional state of the pathway at subcortical levels in all patients (wave I: auditory nerve; wave III: olivocochlear system) and in proportion with the longitude of the neocortical resected tissue in R-HL patients (Na generators: inferior colicullus). It is known that the stimulation of the primary auditory cortex, which is preserved during the surgery, inhibits the response of the ascending impulse conduction at different levels of the pathway (inferior colliculus and medial olivocochlear complex) mainly ipsilateral. Contrary, the stimulation of the secondary auditory areas potentiates the ascending impulses (Khalfa et al., 2001). These last areas could be removed, particularly in the right hemisphere lobectomized patients considering the minor risk to affect eloquent areas for language. As a result of this inhibitory—excitatory imbalance, afferent’ inhibition dominates in the ear ipsilateral to surgery reflected in the delay of conduction at subcortical levels. Similar results have been described by Khalfa et al. (2001) who compared the effects of the resection in the primary or secondary auditory cortex of epileptic patients. These authors argued that anatomical studies in rhesus monkey have shown that efferent fibers originate in the primary auditory cortex and the planum temporale run anteriorly to the temporal pole and then to the lower brainstem nuclei. This anterior pathway has also been identified in human functional neuroimaging studies, and it is activated by all sounds, supporting the perceptual and semantic processes (Schirmer et al., 2012). Probably, this anterior pathway could be damaged with anterior temporal lobectomy, affecting the functioning of the olivocochlear system.
753 At higher levels of the pathway (Pa component generators: auditory radiations-primary auditory cortex) the influence of the mesial resection’ magnitude was evident in all patients. Anterior temporal lobectomy includes the resection of amygdala and hippocampus with temporal neocortex, which are involved in the process of auditory activation-inhibition in humans (Bougeard and Fischer, 2002). The temporo-polar cortex is a probably convergence site for auditory and limbic input involved in the auditory processing. In consequence, we interpret that the lesion of these structures reinforces the efferent suppression and delays the latency of the cortical evoked response. Another critical aspect of our results was the increase in the amplitude of MLR after surgery, in close relationship with the resected volume of the middle temporal pole and the amygdala. It was significant at twelve months post-lobectomy for R-HL patients, both in the midline and ipsilateral temporal electrodes (Na, Pa), and for L-HL patients in the ipsilateral one (Pa). A physical factor like a decrease in skull impedance at the surgical site might contribute to this fact, although the evaluations were carried out six months later. The progressive increase of the amplitude during the follow up period in our patients suggests that the removal of the epileptogenic zone probably eliminates the desynchronizing influence of a tissue with several neuropathological signs. This hypothesis was proposed by Jacobson et al. (1990) who studied a smaller group of patients and did not consider the volume of resection. The main contribution of this study is the demonstration that the resection of temporal lobe structures not directly involved in the primary auditory pathway modifies the electrophysiological correlates of early auditory processing. Probably, long-term neuroplastic changes are involved in this interesting and surprising fact. The main limitation of this study was the impossibility to obtain the volumetric data during post surgical period in all cases, which could have masked correlations of the electrophysiological data with other structures in the temporal lobe. In summary, anterior temporal lobectomy provokes functional modifications to the auditory pathway of epileptic patients in direct proportion with the size of resection. These changes could be the consequence of an indirect modulation of the auditory pathway activity, more evident in R-HL subjects. They usually receive wider neocortical resections because of the minor risk to damage language eloquent areas.
Acknowledgments We thank the Cuban Neuroscience Center for image processing. Furthermore, we thank Odalys Morales-Chacon for the English revision of the manuscript, and Jorge Bergado-Rosado for his contributions. We also are grateful to our reviewers for their helpful comments.
References Ashburner, J., Friston, K.J., 2000. Voxel-based morphometry — the methods. Neuroimage 11, 805—821.
754 Babb, T.L., Wilson, C.L., Crandall, P.H., 1982. Asymmetry and ventral course of the human geniculostriate pathway as determined by hippocampal visual evoked potentials and subsequent visual field defects after temporal lobectomy. Exp. Brain Res. 47, 317—328. Baez Martin, M.M., del Carmen Perez, T.Y., Chacon, L.M., Diaz, B.E., Trapaga-Quincoses, O., Maeso, I.G., Bender, J.E., Galvizu, R., Garcia, M.E., Abreu, I.C., Rodriguez, G.S., 2010. Innovative evaluation of visual field defects in epileptic patients after standard anterior temporal lobectomy, using partial field visual evoked potentials. Epilepsy Res. 90, 68—74. Baez-Martin, M.M., Cabrera-Abreu, I., 2003. Mid-latency auditory evoked potential. Rev. Neurol. 37, 579—586. Baez-Martin, M.M., Cabrera-Abreu, I., 2005. Effects of lobectomy on the auditory mid-latency response in temporal lobe epileptic patients. Rev. Neurol. 41, 81—85. Bougeard, R., Fischer, C., 2002. The role of the temporal pole in auditory processing. Epileptic Disord. 4 (Suppl. 1), S29—S32. Cabrera-Abreu, I., Baez-Martin, M.M., Morales-Chacon, L.M., 2004. Características del potencial evocado auditivo de tallo cerebral en pacientes con epilepsia del lóbulo temporal. Rev. Mex. Neuroci. 5, 294—297. Clemens, B., Menes, A., Nagy, Z., 2004. Objective assessment of neurotoxicity while shifting from carbamazepine to oxcarbazepine. Acta Neurol. Scand. 109, 324—329. Compston, A., 2005. From the archives. ‘Visual field changes following anterior temporal lobectomy: their significance in relation to ‘‘Meyer’s loop’’ of the optic radiation’ and ‘The architecture of the optic radiation in the temporal lobe of man’. Brain 128, 1959—1961. Engel Jr., J., 2009. Overview of surgical treatment for epilepsy. In: Shorvon, S., Perucca, E, Engel, J. (Eds.), The Treatment of Epilepsy. , third ed. Wiley-Blackwell, Oxford, pp. 743—756. Gronich, G., Arno, L., Dualib, K., 2002. Neurofisiologia nao-invasiva (EEG) das diferentes síndromes epilépticas. In: Cukiert, A. (Ed.), Tratamento clínico e cirúrgico das epilepsias de dificil controle. Lemos, Sao Paulo, p. 157. Hara, K., Ohta, K., Miyajima, M., Hara, M., Iino, H., Matsuda, A., Watanabe, S., Matsushima, E., Maehara, T., Matsuura, M., 2012. Mismatch negativity for speech sounds in temporal lobe epilepsy. Epilepsy Behav. 23, 335—341. Jacobson, G.P., Privitera, M., Neils, J.R., Grayson, A.S., Yeh, H.S., 1990. The effects of anterior temporal lobectomy (ATL) on the middle-latency auditory evoked potential (MLAEP). Electroencephalogr. Clin. Neurophysiol. 75, 230—241. Japaridze, G., Kvernadze, D., Geladze, T., Kevanishvili, Z., 1993. Effects of carbamazepine on auditory brainstem response, middle-latency response, and slow cortical potential in epileptic patients. Epilepsia 34, 1105—1109. Karceski, S., Morrell, M., 2006. Principles of epilepsy management: diagnosis and treatment. In: Noseworthy, J.H. (Ed.),
M.M. Báez-Martín et al. Neurological Therapeutics. Principles and Practice. , second ed. Informa Healthcare, Rochester, pp. 341—354. Khalfa, S., Bougeard, R., Morand, N., Veuillet, E., Isnard, J., Guenot, M., Ryvlin, P., Fischer, C., Collet, L., 2001. Evidence of peripheral auditory activity modulation by the auditory cortex in humans. Neuroscience 104, 347—358. Kiernan, J.A., 2012. Anatomy of the temporal lobe. Epilepsy Res. Treat. 2012, 176157, http://dx.doi.org/10.1155/2012/176157. Legatt, A.D., 2005. Brainstem auditory evoked potentials: methodology, interpretation, and clinical application. In: Aminoff, M. (Ed.), Electrodiagnosis in Clinical Neurology. , fifth ed. Churchill Livingstone, New York, pp. 489—523. Lin, Y.Y., Hsiao, F.J., Shih, Y.H., Yiu, C.H., Yen, D.J., Kwan, S.Y., Wong, T.T., Wu, Z.A., Ho, L.T., 2007. Plastic phase-locking and magnetic mismatch response to auditory deviants in temporal lobe epilepsy. Cereb. Cortex 17, 2516—2525. Meneguello, J., Leonhardt, F.D., Pereira, L.D., 2006. Auditory processing in patients with temporal lobe epilepsy. Braz. J. Otorhinolaryngol. 72, 496—504. Miyamoto, T., Katayama, J.I., Kohsaka, M., Koyama, T., 2000. Disturbance of semantic processing in temporal lobe epilepsy demonstrated with scalp ERPs. Seizure 9, 572—579. Palmini, A., Najm, I., Avanzini, G., Babb, T., Guerrini, R., FoldvarySchaefer, N., Jackson, G., Luders, H.O., Prayson, R., Spreafico, R., Vinters, H.V., 2004. Terminology and classification of the cortical dysplasias. Neurology 62, S2—S8. Poblano, A., Belmont, A., Sosa, J., Ibarra, J., Rosas, Y., Lopez, V., Garza, S., 2002. Effects of prenatal exposure to carbamazepine on brainstem auditory evoked potentials in infants of epileptic mothers. J. Child Neurol. 17, 364—368. Schirmer, A., Mickle Fox, P., Grandjean, D., 2012. On the spatial organization of sound processing in the human temporal lobe: a meta analysis. Neuroimage 63, 137—147. Sindou, M., Guenot, M., 2003. Surgical anatomy of the temporal lobe for epilepsy surgery. Adv. Tech. Stand. Neurosurg. 28, 315—343. Trápaga Quincoses, O., Morales Chacon, L.M., 2008. Volumetric measurement and digital electroencephalography in patients with medication-resistant medial temporal lobe epilepsy submitted to surgery. Rev. Neurol. 46, 77—83. Weate, S.J., Drake Jr., M.E., Newell, S.A., 1996. Middle latency auditory evoked potentials in epilepsy. Clin. Electroencephalogr. 27, 155—158. Winston, G.P., Daga, P., Stretton, J., Modat, M., Symms, M.R., McEvoy, A.W., Ourselin, S., Duncan, J.S., 2012. Optic radiation tractography and vision in anterior temporal lobe resection. Ann. Neurol. 71, 334—341. Yogarajah, M., Focke, N.K., Bonelli, S., Cercignani, M., Acheson, J., Parker, G.J., Alexander, D.C., McEvoy, A.W., Symms, M.R., Koepp, M.J., Duncan, J.S., 2009. Defining Meyer’s loop-temporal lobe resections, visual field deficits and diffusion tensor tractography. Brain 132, 1656—1668.
journal homepage: www.elsevier.com/locate/epilepsyres
Temporal lobe epilepsy surgery modulates the activity of auditory pathway Margarita Minou Báez-Martín a,∗, Lilia María Morales-Chacón a, Iván García-Maeso a, Bárbara Estupi˜ nán-Díaz a, Lourdes Lorigados-Pedre a, María Eugenia García a, Reynaldo Galvizu a, Juan E. Bender a, Ivette Cabrera-Abreu a, Yamila Pérez-Téllez a, Lídice Galán b a b
International Center for Neurological Restoration (CIREN), Ave. 25 #15805% 158-160, Havana 11300, Cuba Cuban Neuroscience Center (CNC), Ave. 25 #15202% 158-160, Havana 11300, Cuba
Received 26 August 2013; received in revised form 6 February 2014; accepted 28 February 2014 Available online 12 March 2014
KEYWORDS Auditory brainstem response; Drug-resistant epilepsy; Magnetic resonance imaging; Middle latency response; Temporal lobectomy
∗
Summary The purpose of this paper is to evaluate the effects of the anterior temporal lobectomy on the functional state of the auditory pathway in a group of drug-resistant epileptic patients, linking the electrophysiological results to the resection magnitude. Twenty-seven patients with temporal lobe epilepsy and a matched control group were studied. Auditory brainstem and middle latency responses (ABR and MLR respectively) were carried out before and after 6, 12 and 24 months surgical treatment. The volume and longitude of temporo-mesial resected structures were estimated on magnetic resonance images taken 6 months after surgery. Before the intervention the patients showed a significant delay of latency in waves III, V, Pa and Nb, with an increase in duration of I—V interval in comparison with healthy subjects (Mann—Whitney Utest, p < 0.05). After resection, additional significant differences in waves I and Na latency were observed. Na and Pa waveforms showed a tendency to increase in amplitude, which became statistically significant 12 months after surgery for right hemisphere lobectomized patients in the midline electrode, and in Pa waveform for all patients in the temporal electrodes ipsilateral to resection (Wilcoxon test, p < 0.05). In general, latency variations of MLR correlated with resection longitude, while changes in amplitude correlated with the volume of the resection in the middle temporal pole and amygdala (Pearson’ correlation test, p < 0.05). As a result, we assume that anterior temporal lobectomy provokes functional modifications into the auditory pathway, probably related to an indirect modulation of its activity by the temporo-mesial removed structures. © 2014 Published by Elsevier B.V.
Corresponding author. Tel.: +53 7 273 6356; fax: +53 7 273 6028. E-mail address: [email protected] (M.M. Báez-Martín).
http://dx.doi.org/10.1016/j.eplepsyres.2014.02.017 0920-1211/© 2014 Published by Elsevier B.V.
Effects of the anterior temporal lobectomy
Introduction Temporal lobe epilepsy is the most common type of focal epilepsy in adults. In most cases it involves the temporomesial structures (Gronich et al., 2002). The complex partial seizures in this entity often become drug-resistant, but it is a surgically remediable syndrome (Engel, 2009), showing a resolution of seizures in as much as 70—85% of patients after resection of the epileptogenic area (Karceski and Morrell, 2006). The anterior temporal lobectomy may cause changes in the visual and auditory pathways considering their close relationships with the temporal horn of the lateral ventricles, and the projections to the occipital calcarine banks and the temporal operculum respectively (Sindou and Guenot, 2003). Some efferent projection fibers of the temporal cortex go to the amygdala and hippocampus (Kiernan, 2012), structures that are also total or partially resected during the anterior temporal lobectomy. The most common sensorial sequel is a superior quadrantanopia contralateral to the side of resection secondary to the damage of the Meyer’ loop of the geniculocalcarine tract (Compston, 2005; Winston et al., 2012). It has been well established using both anatomical (Winston et al., 2012; Yogarajah et al., 2009) and functional procedures (Babb et al., 1982; Baez Martin et al., 2010). However, few reports have considered the possibility of changes in the primary auditory pathway after the resection of temporo-mesial structures (Bougeard and Fischer, 2002; Jacobson et al., 1990; Khalfa et al., 2001). Standardized anterior temporal lobectomy removed 4—7 cm of the anterior temporal lobe, including mesial temporal structures (Engel, 2009) and sparing the superior temporal gyrus involved in auditory processing. After this procedure, hearing may be impaired and dichotic listening scores reduced on the ear contralateral to the operated temporal lobe (Bougeard and Fischer, 2002). Contrary to these results, the improvement of the automatic central auditory change-detection after a successful resection of the temporal pole has been demonstrated using the mismatch negativity magnetic equivalent (Lin et al., 2007). Auditory brainstem and middle latency responses (ABR and MLR respectively) have been widely used to evaluate the functional state of the auditory pathway. They represent the electrical activity associated with the sequential activation of the auditory pathway from the cochlear nerve to the primary auditory cortex (Legatt, 2005). The midline Na component of MLR appears to originate subcortically in either the inferior colliculi or medial geniculate body of the thalamus, while the Pa component is related to the activity of the auditory radiations and primary auditory cortex in the Heschl gyrus (Baez-Martin and Cabrera-Abreu, 2003). Other studies in patients with temporal and extratemporal epilepsy suggest that MLR may be generated subcortically but modulated by temporal lobe structures (Weate et al., 1996) some of them could be damaged during the temporal lobectomy. This paper proposes the use of ABR and MLR to evaluate the effect of the anterior temporal lobectomy in the functional state of the auditory pathway of drug-resistant
749 epileptic patients, measuring the relationship of the electrophysiological results with the magnitude of resection.
Subjects and methods Subjects Twenty-seven temporal lobe epileptic patients were evaluated at the Telemetric Unit of the International Center for Neurological Restoration in a prospective study. Presurgical evaluation was performed including the localization of ictal zone combining EEG-video, ictal and interictal SPECT, qualitative and quantitavive MRI (voxel-based morphometry) (Ashburner and Friston, 2000) and neuropsychological tests. Clinical and demographical data of patients and controls are shown in Table 1. The most frequently used drugs for treatment were valproate, carbamazepine and clonazepam. Treatment was not changed after the surgical procedure. All patients underwent standard anterior temporal lobectomy guided by electrocorticography. Tissue samples obtained during surgery were processed for histology. Hippocampal sclerosis was defined and focal cortical dysplasia in temporal neocortex classified according to Palmini’ criteria (Palmini et al., 2004) (Table 1). Sixteen age- and gender-matched healthy subjects (free of neurological and audiological diseases) were also neurophysiologically studied. Hearing threshold level was evaluated both in patients and healthy subjects. All of them were right-handed and gave their signed consent to participate in the study.
Electrophysiological tests To record the auditory evoked responses, surface electrodes (Ag/ClAg) were attached to the scalp according to the international 10-20 system (Table 2). The electrode impedance was kept below 5 k. Records were made by an experienced technician under the supervision of a neurophysiologist, who controlled that subjects stayed awake during the recording of the MLR. They were invited to lie on bed in a climate-controlled room during the tests. Patients were evaluated before surgical resection, as well as six, twelve and twenty-four months after surgery. Recording conditions and equipment Recording conditions are summarized in Table 2. The stimuli were 0.1 ms. alternating clicks delivered through a headphone (DR-531B-7, Elegas Acous Co. Ltd, Japan). The records were obtained using the evoked potentials measuring systems Neuropack four-mini and Neuropack M1 (Nihon Kohden, Japan). Evaluation of records Records were evaluated off-line in a visual inspection mode by two clinical neurophysiologists. Measured variables were absolute latency, interpeak intervals and amplitude of I, III, V, Na, Pa and Nb waveforms. Latencies 2.5 SD longer than the average value from normal subjects, and amplitudes lower
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4 3 5 5
1 2
—
4 3
NO 2A 1B 1A
Parameters
ABR
MLR
Analysis time (ms) Filters (Hz) Stimulus frequency (Hz) Maximal intensity (dBnHL) Average responses Sensibility (V/div) Recording electrodes Reference electrode Ground electrode Stimulation mode
10 100—3000 10 105 2000 5 A1, A2 Cz Fpz Monoaural
100 20—1000 5 90 500 20 Cz, T3, T4 A1-A2 Fpz Binaural
FCD, focal cortical dysplasia; X (SD), mean value (standard deviation).
5 7 8 14 13 16 Patients Left hemisphere lobectomy Right hemisphere lobectomy Healthy subjects
F M
9 6 8
33.07 (9.06) 34.69 (5.28) 33.68 (7.96)
21.14 (9.08) 22.53 (12.14) —
Duration of illness years X (SD)
14 13 —
Temporo-mesial resected volume and longitude
Age years X (SD) Sex N
Clinical and demographical characteristics of the sample. Table 1
ABR and MLR recording conditions.
than the minimal value in the control group were considered abnormal. The absence of the waveform was also considered as abnormal.
Temporo-mesial sclerosis N
FCD in temporal neocortex
Table 2
The longitude of resection was evaluated in twenty-two patients; nineteen of them were also submitted to volumetric measurements. The volume of temporo-mesial resected tissue was measured on MRI images six months after surgery (Magnetom Symphony SIEMENS of 1.5 T) in those cases where quantitative MRI was possible. The methodology to obtain the images and the volumetric measures has been described in detail elsewhere by Trápaga Quincoses and Morales Chacon (2008). The resected volumes of superior, medial and inferior temporal gyri, amygdala, hippocampus, parahippocampus, superior and middle temporal poles from both hemispheres were considered for analysis (n = 10). The residual index of these structures (residual volume of resected side/volume of not resected side × 100) was also calculated (n = 17), taking into account that a low value of the residual index of a structure means a mayor lesion. The absolute longitude of lateral and mesial resected tissue was measured by the neurosurgeon using slices of images in T1, T2 and FLAIR six months after surgery. The lateral (neocortical) aspect included the distance (in mm) between the posterior edge of the internal table and the anterior limit of the resected area, considering the middle temporal gyrus in the axial slices of MRI, whereas the mesial aspect was calculated from axial slices in parallel with the preserved hippocampus. Two tangential lines were drawn: one between the posterior border of the resection and the contralateral hippocampus, and the other between the anterior limit of the preserved hippocampus and the side of resection. The distance between these tangential lines was the mesial longitude.
Statistics Normality of the data was tested using Shapiro—Wilk’ Wtest. The results showed non-normal distribution of some variables. Therefore non-parametric inference was used for comparisons.
Effects of the anterior temporal lobectomy
Figure 1
Mean value of waves I and III latency before and after treatment (6, 12, and 24 months). Wilcoxon test,
The data analysis included the comparison between patients and control subjects before treatment (Mann—Whitney U-test) and the comparison of the auditory evoked responses obtained from epileptic patients at different times of the following (Wilcoxon test). Relationships between the normalized post-surgical electrophysiological data (6 months) and the volume, residual index, and longitude of dissected tissue were calculated (Pearson’ correlation test). Normalization of the data was carried out using the mean and standard deviation values of the control group. Differences were considered significant if p < 0.05 for all tests.
Results Characteristics of the patient’ sample No difference was found between left and right hemisphere lobectomized patients (L-HL and R-HL respectively)
Figure 2 p < 0.05).
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p < 0.05.
regarding age, gender, and duration of illness before treatment (Mann—Whitney U-test, p > 0.05). The hearing threshold level showed no significant differences between ears in pre-surgical evaluation, and there were no changes after treatment in both groups in comparison with the first measurement (Wilcoxon test, p > 0.05).
Electrophysiology Pre-operative findings There were statistically significant differences between patients and controls in I—V interval duration (higher in patients) secondary to a pronounced delay of wave V latency. A lower amplitude of wave III in comparison with healthy subjects was also found bilaterally (Mann—Whitney U-test, p < 0.05). Considering the side of the epileptogenic zone, the differences were in the R-HL group. Furthermore, significant differences in the latency of Nb waveform (longer in patients) were found (Mann—Whitney
Mean value of MLR amplitude before and after treatment (6, 12, and 24 months). Cz electrode (Wilcoxon test,
√
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U-test, p < 0.05). These results were independent of the epileptogenic zone lateralization. No difference was observed between patients with and without FCD in relation to electrophysiological variables (Mann—Whitney U-test, p < 0.05). Post-operative changes Left hemisphere lobectomized (L-HL) patients showed a significant delay of wave I six months after treatment in relation to pre-surgical values in the ear ipsilateral to the resection (Wilcoxon test, p < 0.05). Similar results were observed in R-HL patients, in addition to a significant delay in wave I latency contralateral to the resection and wave III ipsilateral. There were no significant differences twelve and twentyfour months after surgery. However, these values did not return to the pre-surgical level (Fig. 1). In R-HL patients differences for Na waveform latency were statistically significant twelve months after surgery (Wilcoxon test, p < 0.05). Regarding the amplitude of these evoked responses, we could not find significant changes for ABR waves (data not shown). The Na and Pa components showed a tendency to increase in amplitude that became statistically significant twelve months after surgery on the region under the Cz electrode for R-HL patients (Wilcoxon test, p < 0.05) (Fig. 2). Similar results were found only for the Pa waveform in the medial temporal electrodes (T3 or T4) ipsilateral to the resection for all patients.
AEP results vs magnitude of surgical resection Six months after surgery no relation was detected between ABR variables and the temporo-mesial resected volume and longitude. However, MLR showed different results. The resected volume of the middle temporal pole showed a positive relationship with the amplitude of Na and Pa waveforms measured in Cz for all patients (r = 0.84 and r = 0.65 respectively; p < 0.05) (Fig. 3). The residual index of amygdala had a negative relationship with the amplitude of Pa in all cases (r = −0.59; p < 0.05), while its resected volume had a positive relationship with the latency of this component in L-HL patients (r = 0.77; p < 0.05). The longitude of resected tissue in its lateral aspect (neocortex) correlated with the latency of Na waveform for R-HL patients (r = 0.61; p < 0.05) and in the mesial aspect with the latency of Pa waveform for all patients (r = 0.51; p < 0.05) (Fig. 4).
Discussion The results showed variations both in ABR and in MLR of patients before treatment in comparison with normal subjects. Additional changes were detected immediately after surgery and during the follow up period. Some of them were closely related to anatomical measurements. There are reports of variations in the functional state of the auditory system in temporal lobe epileptic patients. For example, temporal lobe epilepsy affects the automatic central auditory change-detection (Hara et al., 2012), the mechanisms of discrimination from sequential sounds and
Figure 3 Relationship between the normalized values of waveforms Na (A) and Pa (B) amplitude and the volume of the resected middle temporal pole of right hemisphere lobectomized patients six months after surgery. Cz electrode (Pearson’ correlation test, p < 0.05).
tone patterns, the selective attention to verbal and nonverbal sounds (Meneguello et al., 2006) and the semantic processing (Miyamoto et al., 2000). Some of these effects have been evaluated both before and after the temporal lobectomy by means of event-related potentials. It has been reported prolonged peak and interpeak latencies in some components of the ABR and MLR of temporal lobe epileptic patients different from normal subjects (Baez-Martin and Cabrera-Abreu, 2003, 2005; Cabrera-Abreu et al., 2004). Some authors argued that these facts could depend on the medication, particularly carbamazepine (Clemens et al., 2004; Poblano et al., 2002). For example, Japaridze et al. (1993) suggest that carbamazepine exerts suppressive influences both on modally specific (lemniscal) and nonspecific (extralemniscal) auditory structures. We assume that pre-operative findings in our patients might be related to medication, particularly at brainstem level. But, the existence of temporo-mesial sclerosis
Effects of the anterior temporal lobectomy
Figure 4 Relationship between the normalized values of waveform Pa latency and the mesial longitude of resection six months after surgery (all patients). Cz electrode; Pearson’ correlation test, p < 0.05.
(demonstrated by MRI) may contribute to MLR results. Although it might be thought that FCD could be a contributing factor, no statistically confirmed evidence of this relationship was found. In our patients, medical treatment persisted identical while new changes appeared in ABR and MLR after temporal lobectomy (i.e. prolonged waves I, III and Na latencies). This might suggest an indirect effect of the procedure on the functional state of the pathway at subcortical levels in all patients (wave I: auditory nerve; wave III: olivocochlear system) and in proportion with the longitude of the neocortical resected tissue in R-HL patients (Na generators: inferior colicullus). It is known that the stimulation of the primary auditory cortex, which is preserved during the surgery, inhibits the response of the ascending impulse conduction at different levels of the pathway (inferior colliculus and medial olivocochlear complex) mainly ipsilateral. Contrary, the stimulation of the secondary auditory areas potentiates the ascending impulses (Khalfa et al., 2001). These last areas could be removed, particularly in the right hemisphere lobectomized patients considering the minor risk to affect eloquent areas for language. As a result of this inhibitory—excitatory imbalance, afferent’ inhibition dominates in the ear ipsilateral to surgery reflected in the delay of conduction at subcortical levels. Similar results have been described by Khalfa et al. (2001) who compared the effects of the resection in the primary or secondary auditory cortex of epileptic patients. These authors argued that anatomical studies in rhesus monkey have shown that efferent fibers originate in the primary auditory cortex and the planum temporale run anteriorly to the temporal pole and then to the lower brainstem nuclei. This anterior pathway has also been identified in human functional neuroimaging studies, and it is activated by all sounds, supporting the perceptual and semantic processes (Schirmer et al., 2012). Probably, this anterior pathway could be damaged with anterior temporal lobectomy, affecting the functioning of the olivocochlear system.
753 At higher levels of the pathway (Pa component generators: auditory radiations-primary auditory cortex) the influence of the mesial resection’ magnitude was evident in all patients. Anterior temporal lobectomy includes the resection of amygdala and hippocampus with temporal neocortex, which are involved in the process of auditory activation-inhibition in humans (Bougeard and Fischer, 2002). The temporo-polar cortex is a probably convergence site for auditory and limbic input involved in the auditory processing. In consequence, we interpret that the lesion of these structures reinforces the efferent suppression and delays the latency of the cortical evoked response. Another critical aspect of our results was the increase in the amplitude of MLR after surgery, in close relationship with the resected volume of the middle temporal pole and the amygdala. It was significant at twelve months post-lobectomy for R-HL patients, both in the midline and ipsilateral temporal electrodes (Na, Pa), and for L-HL patients in the ipsilateral one (Pa). A physical factor like a decrease in skull impedance at the surgical site might contribute to this fact, although the evaluations were carried out six months later. The progressive increase of the amplitude during the follow up period in our patients suggests that the removal of the epileptogenic zone probably eliminates the desynchronizing influence of a tissue with several neuropathological signs. This hypothesis was proposed by Jacobson et al. (1990) who studied a smaller group of patients and did not consider the volume of resection. The main contribution of this study is the demonstration that the resection of temporal lobe structures not directly involved in the primary auditory pathway modifies the electrophysiological correlates of early auditory processing. Probably, long-term neuroplastic changes are involved in this interesting and surprising fact. The main limitation of this study was the impossibility to obtain the volumetric data during post surgical period in all cases, which could have masked correlations of the electrophysiological data with other structures in the temporal lobe. In summary, anterior temporal lobectomy provokes functional modifications to the auditory pathway of epileptic patients in direct proportion with the size of resection. These changes could be the consequence of an indirect modulation of the auditory pathway activity, more evident in R-HL subjects. They usually receive wider neocortical resections because of the minor risk to damage language eloquent areas.
Acknowledgments We thank the Cuban Neuroscience Center for image processing. Furthermore, we thank Odalys Morales-Chacon for the English revision of the manuscript, and Jorge Bergado-Rosado for his contributions. We also are grateful to our reviewers for their helpful comments.
References Ashburner, J., Friston, K.J., 2000. Voxel-based morphometry — the methods. Neuroimage 11, 805—821.
754 Babb, T.L., Wilson, C.L., Crandall, P.H., 1982. Asymmetry and ventral course of the human geniculostriate pathway as determined by hippocampal visual evoked potentials and subsequent visual field defects after temporal lobectomy. Exp. Brain Res. 47, 317—328. Baez Martin, M.M., del Carmen Perez, T.Y., Chacon, L.M., Diaz, B.E., Trapaga-Quincoses, O., Maeso, I.G., Bender, J.E., Galvizu, R., Garcia, M.E., Abreu, I.C., Rodriguez, G.S., 2010. Innovative evaluation of visual field defects in epileptic patients after standard anterior temporal lobectomy, using partial field visual evoked potentials. Epilepsy Res. 90, 68—74. Baez-Martin, M.M., Cabrera-Abreu, I., 2003. Mid-latency auditory evoked potential. Rev. Neurol. 37, 579—586. Baez-Martin, M.M., Cabrera-Abreu, I., 2005. Effects of lobectomy on the auditory mid-latency response in temporal lobe epileptic patients. Rev. Neurol. 41, 81—85. Bougeard, R., Fischer, C., 2002. The role of the temporal pole in auditory processing. Epileptic Disord. 4 (Suppl. 1), S29—S32. Cabrera-Abreu, I., Baez-Martin, M.M., Morales-Chacon, L.M., 2004. Características del potencial evocado auditivo de tallo cerebral en pacientes con epilepsia del lóbulo temporal. Rev. Mex. Neuroci. 5, 294—297. Clemens, B., Menes, A., Nagy, Z., 2004. Objective assessment of neurotoxicity while shifting from carbamazepine to oxcarbazepine. Acta Neurol. Scand. 109, 324—329. Compston, A., 2005. From the archives. ‘Visual field changes following anterior temporal lobectomy: their significance in relation to ‘‘Meyer’s loop’’ of the optic radiation’ and ‘The architecture of the optic radiation in the temporal lobe of man’. Brain 128, 1959—1961. Engel Jr., J., 2009. Overview of surgical treatment for epilepsy. In: Shorvon, S., Perucca, E, Engel, J. (Eds.), The Treatment of Epilepsy. , third ed. Wiley-Blackwell, Oxford, pp. 743—756. Gronich, G., Arno, L., Dualib, K., 2002. Neurofisiologia nao-invasiva (EEG) das diferentes síndromes epilépticas. In: Cukiert, A. (Ed.), Tratamento clínico e cirúrgico das epilepsias de dificil controle. Lemos, Sao Paulo, p. 157. Hara, K., Ohta, K., Miyajima, M., Hara, M., Iino, H., Matsuda, A., Watanabe, S., Matsushima, E., Maehara, T., Matsuura, M., 2012. Mismatch negativity for speech sounds in temporal lobe epilepsy. Epilepsy Behav. 23, 335—341. Jacobson, G.P., Privitera, M., Neils, J.R., Grayson, A.S., Yeh, H.S., 1990. The effects of anterior temporal lobectomy (ATL) on the middle-latency auditory evoked potential (MLAEP). Electroencephalogr. Clin. Neurophysiol. 75, 230—241. Japaridze, G., Kvernadze, D., Geladze, T., Kevanishvili, Z., 1993. Effects of carbamazepine on auditory brainstem response, middle-latency response, and slow cortical potential in epileptic patients. Epilepsia 34, 1105—1109. Karceski, S., Morrell, M., 2006. Principles of epilepsy management: diagnosis and treatment. In: Noseworthy, J.H. (Ed.),
M.M. Báez-Martín et al. Neurological Therapeutics. Principles and Practice. , second ed. Informa Healthcare, Rochester, pp. 341—354. Khalfa, S., Bougeard, R., Morand, N., Veuillet, E., Isnard, J., Guenot, M., Ryvlin, P., Fischer, C., Collet, L., 2001. Evidence of peripheral auditory activity modulation by the auditory cortex in humans. Neuroscience 104, 347—358. Kiernan, J.A., 2012. Anatomy of the temporal lobe. Epilepsy Res. Treat. 2012, 176157, http://dx.doi.org/10.1155/2012/176157. Legatt, A.D., 2005. Brainstem auditory evoked potentials: methodology, interpretation, and clinical application. In: Aminoff, M. (Ed.), Electrodiagnosis in Clinical Neurology. , fifth ed. Churchill Livingstone, New York, pp. 489—523. Lin, Y.Y., Hsiao, F.J., Shih, Y.H., Yiu, C.H., Yen, D.J., Kwan, S.Y., Wong, T.T., Wu, Z.A., Ho, L.T., 2007. Plastic phase-locking and magnetic mismatch response to auditory deviants in temporal lobe epilepsy. Cereb. Cortex 17, 2516—2525. Meneguello, J., Leonhardt, F.D., Pereira, L.D., 2006. Auditory processing in patients with temporal lobe epilepsy. Braz. J. Otorhinolaryngol. 72, 496—504. Miyamoto, T., Katayama, J.I., Kohsaka, M., Koyama, T., 2000. Disturbance of semantic processing in temporal lobe epilepsy demonstrated with scalp ERPs. Seizure 9, 572—579. Palmini, A., Najm, I., Avanzini, G., Babb, T., Guerrini, R., FoldvarySchaefer, N., Jackson, G., Luders, H.O., Prayson, R., Spreafico, R., Vinters, H.V., 2004. Terminology and classification of the cortical dysplasias. Neurology 62, S2—S8. Poblano, A., Belmont, A., Sosa, J., Ibarra, J., Rosas, Y., Lopez, V., Garza, S., 2002. Effects of prenatal exposure to carbamazepine on brainstem auditory evoked potentials in infants of epileptic mothers. J. Child Neurol. 17, 364—368. Schirmer, A., Mickle Fox, P., Grandjean, D., 2012. On the spatial organization of sound processing in the human temporal lobe: a meta analysis. Neuroimage 63, 137—147. Sindou, M., Guenot, M., 2003. Surgical anatomy of the temporal lobe for epilepsy surgery. Adv. Tech. Stand. Neurosurg. 28, 315—343. Trápaga Quincoses, O., Morales Chacon, L.M., 2008. Volumetric measurement and digital electroencephalography in patients with medication-resistant medial temporal lobe epilepsy submitted to surgery. Rev. Neurol. 46, 77—83. Weate, S.J., Drake Jr., M.E., Newell, S.A., 1996. Middle latency auditory evoked potentials in epilepsy. Clin. Electroencephalogr. 27, 155—158. Winston, G.P., Daga, P., Stretton, J., Modat, M., Symms, M.R., McEvoy, A.W., Ourselin, S., Duncan, J.S., 2012. Optic radiation tractography and vision in anterior temporal lobe resection. Ann. Neurol. 71, 334—341. Yogarajah, M., Focke, N.K., Bonelli, S., Cercignani, M., Acheson, J., Parker, G.J., Alexander, D.C., McEvoy, A.W., Symms, M.R., Koepp, M.J., Duncan, J.S., 2009. Defining Meyer’s loop-temporal lobe resections, visual field deficits and diffusion tensor tractography. Brain 132, 1656—1668.
