Some Audiological Aspects of Temporal Lobe Epilepsy

By Julia Bak, B.S. Speech, Language, and Hearing Department, University of Arizona, Tucson, AZ

 

Though often under the audiology diagnostic radar, many patients with temporal lobe epilepsy (TLE) (or epilepsy in general) have central auditory processing deficits (CAPD) and related auditory problems (Ehrlé, et al., 2001). Temporal lobe epilepsy, itself, will seldom affect pure-tone thresholds but it can and does affect performance on more complex tests of auditory function such as those used in the assessment of CAPD (Weihing, Chermak & Musiek, 2015; Meneguello et. al., 2006). The following is a brief review of selected, pertinent studies supporting the opening statements of this article.

The prevalence of epilepsy in developed countries is approximately 4 – 10 cases per 1000, and 60 percent of those are TLE (Téllez-Zenteno & Hernández-Ronquillo, 2012). This prevalence statistic would indicate that most practicing audiologists will see patients with TLE in their practice. Therefore, it is logical that audiologists understand their own role in the identification and evaluation of this clinical population. TLE is seen in both adults and children, presenting some remarkable audiological profiles that should be of interest to the audiology community.

A key factor in TLE and central auditory dysfunction is the simple anatomical relationship to the auditory cortex. Seizure activity in the temporal lobe has a likelihood of affecting the auditory cortex and associated areas of central hearing. The seizure activity itself often damages neural tissue and therefore the more frequent and the greater the duration of seizures the more the neural compromise. Speaking to this concept, Gramstad and colleagues (2006) found that the longer the duration of epilepsy, the greater the chance of structural and functional abnormalities in the temporal lobe (including Heschl’s gyrus). Related to this, duration of TLE seems to be an important factor, as patients with long-standing TLE are likely to show deficits on central auditory tests such as pattern perception and dichotic listening (Meneguello et. al., 2006). Han and colleagues concluded that patients with TLE are more susceptible to CAPD.  These investigators showed deficits in temporal processing in their clinical population. Specifically noted in the Han et al., (2011) study were deficits in frequency pattern perception in almost 4/5 of the patients with TLE. Lavasani and colleagues showed similar research results on patients with TLE for the duration pattern test. Lavasani et al., also noted in their TLE data that lesions in the left hemisphere resulted in greater pattern perception deficits than did lesions in the right hemisphere. Further support in this regard came from Meneguello et al. reported a nearly 30 percent poorer performance on the duration pattern test (bilaterally) for TLE patients compared to controls.

Ehrlé, et al., (2001) made an interesting observation on their patients with unilateral TLE. They commented that it was likely that both temporal lobes needed to be intact to accurately process pattern stimuli.  This is consistent with long-held theoretical constructs for pattern perception presented 40 years ago (Musiek et al., 1980).

It is important to realize, however, that temporal processing deficits in TLE are not limited to pattern perception problems.  Lavasani and colleagues evaluated auditory temporal processing in patients with right temporal lobe epilepsy (RTLE) and left temporal lobe epilepsy (LTLE). These researchers employed the gaps in noise test (GIN) which is a test of temporal resolution (Musiek et al., 2005). Participants with temporal lobe epilepsy had higher GIN threshold and a lower mean percentage of correct responses than the control group. Other studies have supported the work of Lavasani and colleagues showing GIN thresholds significantly higher (poorer) for TLE patients compared to normal control groups (see Aravindkumar et al., 2012; Rabelo et al., 2015). Interestingly in the three studies just mentioned, there were no significant differences for TLE on the right versus left hemispheres in terms of GIN thresholds.

The next audiological test category relevant to assessing TLE is dichotic listening. Various dichotic tests and paradigms have long been employed with success in the evaluation of the central auditory system. The now well-known classic findings are contralateral ear deficits (to the involved hemisphere) except in situations where the corpus callosum fibers are compromised. In one of the early studies by Collard (1984) using a variety of dichotic tests, those with TLE demonstrated lower scores than a control group with contralateral ear deficits commonly, but not exclusively seen. These kinds of findings have been reported in a number of other subsequent studies generating conclusions that dichotic listening can be a valued auditory/language evaluation tool in TLE (Gramstad, Engelsen, & Hugdahl, 2006; Roberts, Varney, Paulsen and Richardson, 1990; Hugdahl, et al., 1997). Of further interest, is a study by Fernandes et al. (2006) showing correlations between fMRI activation patterns and dichotic listening in children with epilepsy. This supported the dichotic – anatomic and TLE relationship.

It should be mentioned that seizure activity can spread across the corpus callosum and result in dysfunction of auditory/language areas in both hemispheres and or in the callosal transfer of information. This kind of seizure contamination can result in not only the contralateral ear but also bilateral deficits on dichotic listening.

The final aspect of this brief review involves auditory evoked potentials (AEPs) and TLE. The middle- and late-auditory evoked potentials are generated, for the most part by the auditory cortex and therefore would be logically considered in the possible audiological evaluation of TLE. However, there are reports on the auditory brainstem response (ABR) in patients with epilepsy, though not necessarily of the temporal lobe, that deserves some comment first. There are reports that demonstrate either an extension of interwave latencies (usually I – III) or delayed waves or an increase in thresholds compared to controls or normative values (Rodin et. al., 1982, Soliman et. al., 1993). However, there is also evidence that patients with a seizure disorder that ABRs are normal — which would be expected given the neural generators of the ABR occur in the brainstem, not the cortex… (Japaridze et al., 1997). Recent research relates that chronic seizures originating in cerebral areas of the brain (i.e., temporal lobe) may result in reduced connectivity in the brainstem via dysfunction of the ascending reticular activating system (https://medicalxpress.com, 2018). This situation would likely be rare but a possibility.

The middle latency response (MLR) has been used to investigate individuals with epilepsy. Soliman et al., (1993) evaluated patients with epilepsy (TLE & grand mal) who demonstrated normal hearing by measuring their MLR thresholds. According to the authors, MLR thresholds were elevated in slightly over 40 percent of the epileptic patients. It has also been shown that there is a significant increase in latency of the MLR Pa and Pb component waves in a large group of patients with generalized seizures (uncategorized) (Azumi, Nakashima, Takahashi, 1994). Another study showed an increase in latency and decrease in amplitude of the P50 response (i.e., the Pb of the MLR) in epileptic patients compared to a normal control group. This study used a paired stimulus paradigm which was different than the two previous studies. On the other hand, a study by Japaridze et al., (1997) showed no difference between a partial epileptic group and control group for the MLR.

Though there have been a few studies that have looked at the cortical (late) N1 and P2 potentials showingsignificant findings for delayed latency and or reduced amplitude (e.g., Japaridze et. al., 1997), the overwhelming amount of research has been conducted on the P300. Therefor to provide a more fruitful commentary, this last section will be directed towards the P300 and epilepsy (not limited to TLE). Specifically, the study by Zong, Mengmeng, Chen et. al. (2019) which is a Meta-analysis, will be reviewed as it adds considerable weight to the key points of this script. Zong et.al., (2019) performed a Meta-analysis on 27 studies concerned with the P300 findings in patients with various types of epilepsy that were compared to control groups. Pooled data from the studies showed latency measures were significantly greater for those with epilepsy (all types) compared to controls. The same trend was documented for amplitude measures of the P300. These findings were congruent for a subgroup of patients that had TLE.

 

Key Points

This commentary, based on a review of selected studies related to auditory function of individuals with epilepsy orspecifically TLE, seeks to highlight several aspects of audiological interest. One is the fact that TLE and general epilepsy has a prevalence that is high enough that audiologists will see these patients in their practice. The second aspect is that there is an anatomical factor that underlies the finding that many of these patients with epilepsy have audiological dysfunction. The third aspect is that there are a variety of either behavioral or electrophysiological auditory tests that can be of great value in evaluating the functional auditory integrity of these patients.

Audiologists who see these patients with TLE or other types of epilepsy should seek to evaluate them with the proper test procedures, so that a diagnosis of subsequent auditory deficits can be established.. This in turn will profit this clinical population and the field of audiology.

 

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References:

  1. Aravindkumar, R., Shivashankar, N., Satishchandra, P., Sinha, S., Saini, J., & Subbakrishna, D. (2012). Temporal resolution deficits in patients with refractory complex partial seizures and mesial temporal sclerosis (MTS). Epilepsy & Behavior, 24(1), 126–130. doi: 10.1016/j.yebeh.2012.03.004
  2. Azumi, T., Nakashima, K., & Takahashi, K. (1994). Auditory middle latency responses in patients with epilepsy. Electromyography and clinical neurophysiology, 34(3), 185-191.
  3. Casali, R. L., Amaral, M. I. R. D., Boscariol, M., Lunardi, L. L., Guerreiro, M. M., Matas, C. G., & Colella-Santos, M. F. (2016). Comparison of auditory event-related potentials between children with benign childhood epilepsy with centrotemporal spikes and children with temporal lobe epilepsy. Epilepsy & Behavior, 59, 111–116. doi: 10.1016/j.yebeh.2016.03.024
  4. Chayasirisobhon, W. V., Chayasirisobhon, S., Tin, S. N., Leu, N., Tehrani, K., & McGuckin, J. S. (2007). Scalp-recorded auditory P300 event-related potentials in new-onset untreated temporal lobe epilepsy. Clinical EEG and neuroscience, 38(3), 168-171.
  5. Collard, M., (1984) Central auditory tests in patients with intractable seizures. Seminars in Hearing, 3, 277-295.
  6. Ehrlé, N., Samson, S., & Baulac, M. (2001). Processing of rapid auditory information in epileptic patients with left temporal lobe damage. Neuropsychologia, 39(5), 525-531.
  7. Fernandes, M, Smith, M. Logan, W., Crawley, A.,  McAndrews, M. (2006) Comparing language lateralization determined by dichotic listening and fMRI activation in frontal and temporal lobes in children with epilepsy. Brain and Language, 96, 106–114.
  8. Gramstad, A., Engelsen, B. A., & Hugdahl, K. (2006). Dichotic listening with forced attention in patients with temporal lobe epilepsy: significance of left hemisphere cognitive dysfunction. Scandinavian Journal of Psychology, 47(3), 163-170.
  9. Han, M. W., Ahn, J. H., Kang, J. K., Lee, E. M., Lee, J. H., Bae, J. H., & Chung, J. W. (2011). Central auditory processing impairment in patients with temporal lobe epilepsy. Epilepsy & Behavior, 20(2), 370-374.
  10. Japaridze, G., Kvernadze, D., Geladze, T., & Kevanishvili, Z. (1997). Auditory brainstem response, middle-latency response, and slow cortical potential in patients with partial epilepsy. Seizure, 6(6), 449-456.
  11. Lavasani, A. N., Mohammadkhani, G., Motamedi, M., Karimi, L. J., Jalaei, S., Shojaei, F. S., & Azimi, H. (2016). Auditory temporal processing in patients with temporal lobe epilepsy. Epilepsy & Behavior, 60, 81-85.
  12. Lin, W., Li, G., Zhong, R., Chen, Q., & Li, J. (2019). The P300 event-related potential component and cognitive impairment in epilepsy: A systematic review and meta-analysis. Frontiers in neurology, 10, 943.
  13. Meneguello, J., Leonhardt, F. D., & Pereira, L. D. (2006). Auditory processing in patients with temporal lobe epilepsy. Brazilian journal of otorhinolaryngology, 72(4), 496-504.
  14. Musiek, F.E., Pinheiro, M.L. & Wilson, D.  (1980).  Auditory Pattern Perception in Split-Brain Patients.  Arch Otolaryngology. Head and Neck Surg., 106, 610-612.
  15. Musiek, F., Shinn, J., Jirsa, R., Bamiou, D., Baran, J., & Zaidan, E.  (2005).  The GIN (Gaps in Noise) Test Performance in Subjects with and without Confirmed Central Auditory Nervous System Involvement. Ear & Hearing, 26, 608-618.
  16. Rabelo, C. M., Weihing, J. A., & Schochat, E. (2015). Temporal resolution in individuals with neurological disorders. Clinics, 70(9), 606-611.
  17. Roberts, R., Varney, N., Paulsen, J., Richardson, E. (1990) Dichotic listening and complex partial seizures. Journal of Clinical and Experimental Neuropsychology, 12, 447- 458.
  18. Rodin, E., Chayasirisobhon, S., & Klutke, G. (1982). Brainstem auditory evoked potential recording in patients with epilepsy. Clinical Electroencephalography, 13(3), 154-161.
  19. Shinn, J. B., & Musiek, F. (2003). Temporal processing: The basics. Hearing Journal, 56(7), 52.
  20. Soliman, S., Mostafa, M., Kamal, N., Raafat, M., & Hazzaa, N. (1993). Auditory evoked potentials in epileptic patients. Ear and hearing, 14(4), 235-241.
  21. Téllez-Zenteno, J. and Hernández-Ronquillo, L. (2012)  A Review of the Epidemiology of Temporal Lobe Epilepsy. Epilepsy Research and Treatment Volume, 2012, Article ID 630853, 2012.
  22. Weihing, J., Chermak, G. D., & Musiek, F. E. (2015, November). Auditory training for central auditory processing disorder. In Seminars in hearing, 36(4),199-215. Thieme Medical Publishers.
  23. Zhong R. Li M., Chen Q., Li J., Li G.,Li, W., (2019) The P300 Event-Related Potential Component and Cognitive Impairment in Epilepsy: A Systematic Review and Meta-analysis, Frontiers in Neurology, 10, 943

About Pathways

Pathways is both a column that covers topics related to CAPD and Neuroaudiology and a society for people interested in central auditory disorders that regularly meets to discuss these issues.

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