Cortical auditory dysfunction in benign rolandic epilepsy.

PURPOSE: To evaluate cortical auditory function, including speech recognition, in children with benign rolandic epilepsy (BRE). METHODS: Fourteen children, seven patients with BRE and seven matched controls, underwent audiometric and behavioral testing, simultaneous EEG recordings, and auditory-evoked potential recordings with speech and tones. Speech recognition was tested under multiple listening conditions. RESULTS: All participants demonstrated normal speech recognition abilities in quiet, as well as normal peripheral and subcortical auditory function. BRE patients performed significantly worse than controls when speech recognition was tested under adverse listening conditions, including background noise. Five BRE patients who were impaired on two or more tests had centrotemporal spiking on awake EEG. There were no significant group differences in the latency or amplitude of early N100 cortical responses to speech or tones. Conversely, the mismatch negativity, a preattentive index of cortical processing that is elicited passively, was absent or prolonged for speech, but not tones, in BRE patients as compared to controls. DISCUSSION: Children with BRE demonstrated specific speech recognition impairments. Our evoked potential findings indicate that these behavioral impairments reflect dysfunction of nonprimary auditory cortex and cannot be attributed solely to attention difficulties. A possible association between auditory impairments and centrotemporal spiking (>1/min) on awake EEG was identified. The pattern of speech recognition impairments observed is a known risk factor for academic difficulties in school-age children. Our results underscore the importance of comprehensive auditory testing, using behavioral and electrophysiological measures, in children with BRE.

Cortical sites critical for speech discrimination in normal and impaired listeners.

We used statistical modeling to investigate variability in the cortical auditory representations of 24 normal-hearing epilepsy patients undergoing electrocortical stimulation mapping (ESM). Patients were identified as normal or impaired listeners based on recognition accuracy for acoustically filtered words used to simulate everyday listening conditions. The experimental ESM task was a binary (same-different) auditory syllable discrimination paradigm that both listener groups performed accurately at baseline. Template mixture modeling of speech discrimination deficits during ESM showed larger and more variable cortical distributions for impaired listeners than normal listeners, despite comparable behavioral performances. These results demonstrate that individual differences in speech recognition abilities are reflected in the underlying cortical representations.

Electrocorticographic high gamma activity versus electrical cortical stimulation mapping of naming.

Subdural electrocorticographic (ECoG) recordings in patients undergoing epilepsy surgery have shown that functional activation is associated with event-related broadband gamma activity in a higher frequency range (>70 Hz) than previously studied in human scalp EEG. To investigate the utility of this high gamma activity (HGA) for mapping language cortex, we compared its neuroanatomical distribution with functional maps derived from electrical cortical stimulation (ECS), which remains the gold standard for predicting functional impairment after surgery for epilepsy, tumours or vascular malformations. Thirteen patients had undergone subdural electrode implantation for the surgical management of intractable epilepsy. Subdural ECoG signals were recorded while each patient verbally named sequentially presented line drawings of objects, and estimates of event-related HGA (80-100 Hz) were made at each recording site. Routine clinical ECS mapping used a subset of the same naming stimuli at each cortical site. If ECS disrupted mouth-related motor function, i.e. if it affected the mouth, lips or tongue, naming could not be tested with ECS at the same cortical site. Because naming during ECoG involved these muscles of articulation, the sensitivity and specificity of ECoG HGA were estimated relative to both ECS-induced impairments of naming and ECS disruption of mouth-related motor function. When these estimates were made separately for 12 electrode sites per patient (the average number with significant HGA), the specificity of ECoG HGA with respect to ECS was 78% for naming and 81% for mouth-related motor function, and equivalent sensitivities were 38% and 46%, respectively. When ECS maps of naming and mouth-related motor function were combined, the specificity and sensitivity of ECoG HGA with respect to ECS were 84% and 43%, respectively. This study indicates that event-related ECoG HGA during confrontation naming predicts ECS interference with naming and mouth-related motor function with good specificity but relatively low sensitivity. Its favourable specificity suggests that ECoG HGA can be used to construct a preliminary functional map that may help identify cortical sites of lower priority for ECS mapping. Passive recordings of ECoG gamma activity may be done simultaneously at all electrode sites without the risk of after-discharges associated with ECS mapping, which must be done sequentially at pairs of electrodes. We discuss the relative merits of these two functional mapping techniques.

Cortical bases of speech perception: evidence from functional lesion studies.

Functional lesion studies have yielded new information about the cortical organization of speech perception in the human brain. We will review a number of recent findings, focusing on studies of speech perception that use the techniques of electrocortical mapping by cortical stimulation and hemispheric anesthetization by intracarotid amobarbital. Implications for recent developments in neuroimaging studies of speech perception will be discussed. This discussion will provide the framework for a developing model of the cortical circuitry critical for speech perception.

Right Hemisphere Language Dominance in a Right-Handed Patient with Late-Onset Seizures.

Right hemisphere language dominance is rare in right-handed individuals and usually the result of language transfer associated with early left hemisphere pathology. We studied a 33-year-old right-handed man, with a normal MRI scan, who developed left frontal lobe seizures at age 15 years. Language lateralization testing by intracarotid amobarbital injection and dichotic listening showed the patient to be strongly right hemisphere language dominant. The clinical features of this patient do not fit the profile of pathology-induced language transfer, but instead suggest that he was right hemisphere language dominant before developing seizures. This case underscores the importance of language lateralization testing in patients who are candidates for seizure surgery, even if they are strongly right-handed and have late-onset seizures, features usually associated with left hemisphere language dominance. One implication is that the incidence of right hemisphere language dominance in the right-handed population may be underestimated.

Auditory processing studied prospectively in two hemidecorticectomy patients.

Auditory processing of speech and nonspeech sounds was studied prospectively in two hemidecorticectomy patients (ages 10-11 years) with Rasmussen's syndrome. We tested auditory word recognition under four listening conditions: in quiet, in noise, after acoustic filtering, and dichotically. Recognition of environmental sounds and discrimination of tones and digitized syllables were also tested. Presurgical testing confirmed normal processing of speech and nonspeech, for both patients, under all listening conditon. One year after surgery, both patients demonstrated intact recognition of words and environmental sounds in quiet but impaired word recognition in noise. The left hemidecorticectomy patient also demonstrated impaired recognition of low-pass filtered words. These findings suggest that either hemisphere can process speech or nonspeech sounds in quiet, whereas both hemispheres are needed to process speech in background noise. Hemispheric contributions to processing speech in noise appear to differ, with the left hemisphere compensating for loss of phonologic information and the right hemisphere compensating for increased attention demands.

Human ECoG analysis during speech perception using matching pursuit: a comparison between stochastic and dyadic dictionaries.

We use the matching pursuit (MP) algorithm to detect induced gamma activity in human EEG during speech perception. We show that the MP algorithm is particularly useful for detecting small power changes at high gamma frequencies (> 70 Hz). We also compare the performance of the MP using a stochastic versus a dyadic dictionary and show that despite the frequency bias the time-frequency power plot (averaged over 100 trials) generated by the dyadic MP is almost identical (> 98.5%) to the one generated by the stochastic MP. However, the dyadic MP is computationally much faster than the stochastic MP.

Variability in cortical representations of speech sound perception.

Recent brain mapping studies have provided new insights into the cortical systems that mediate human speech perception. Electrocortical stimulation mapping (ESM) is a brain mapping method that is used clinically to localize cortical functions in neurosurgical patients. Recent ESM studies have yielded new insights into the cortical systems that mediate speech perception and how these systems vary as a function of individual differences. ESM methods are described and findings from recent ESM studies of speech perception are reviewed. The clinical implications of these findings are discussed as they relate to current understanding of how individual differences in listening abilities are reflected in the underlying cortical representations.

A pilot study transitioning children onto levetiracetam monotherapy to improve language dysfunction associated with benign rolandic epilepsy.

Benign rolandic epilepsy (BRE) and Landau-Kleffner syndrome (LKS) are similar epilepsy syndromes with sleep-accentuated epileptiform activity, sporadic seizures, and language dysfunction. Levetiracetam has been associated with improved language function in LKS and seizure reduction in BRE. We hypothesized levetiracetam would improve language function in children with BRE. A pilot study was performed with six children (aged 6-12) with BRE and evidence of impaired auditory comprehension and verbal memory. Children were transitioned from their current anticonvulsant to 40 mg/kg/day levetiracetam over a 2-week period and retested at 6 months. At 6 months, three of four children with baseline auditory comprehension impairments performed normally (P=0.06), and five had improved auditory verbal memory (P=0.08). Seizures improved in five, decreasing from 2.7 to 1.0 seizure per 6 months (P=0.11). Results from this pilot study suggest that levetiracetam may have a beneficial effect on language in children with BRE.

Cortical auditory systems: speech and other complex sounds.

The neural systems that mediate human perception of speech and other complex sounds are currently the focus of considerable research. Brain mapping studies have provided new insights into the cortical processing of complex sounds. Findings from three lines of brain mapping research--stroke-lesion, neuroimaging, and electrocortical mapping studies--are reviewed. Unresolved questions regarding the relative contributions of cortical and subcortical auditory processing and the existence of separate, functionally specialized, cortical auditory systems for processing speech and nonspeech sounds are discussed. An integrated approach is proposed for future research on the neural bases of complex sound processing.

Speech recognition impairments in patients with intractable right temporal lobe epilepsy.

PURPOSE: To evaluate speech recognition in patients with focal intractable epilepsy and surgical resections in the nondominant (right) hemisphere. METHODS: Speech recognition was tested prospectively, under different listening conditions, in 22 patients with right temporal lobe (11 patients) or extra-temporal lobe epilepsy. All were left-hemisphere dominant for language on preoperative intracarotid sodium amobarbital testing. RESULTS: All patients demonstrated normal auditory recognition of words and environmental sounds before and after surgery. However, when real-world listening conditions were simulated by using acoustically degraded (filtered) words, patients with temporal lobe epilepsy performed significantly worse than patients with frontal or parietooccipital lobe epilepsy before and after surgery (p<0.0001). CONCLUSIONS: Patients with intractable right temporal lobe epilepsy are at risk for speech recognition impairments in real-world listening environments, independent of surgery. The impact of speech recognition difficulties on verbal communication, coupled with the prevalence of adverse listening environments, underscores the importance of testing speech recognition under different listening conditions in patients with intractable right temporal lobe epilepsy.

Landau-Kleffner syndrome responsive to levetiracetam.

A 5-year-old girl with Landau-Kleffner syndrome is discussed. The child began having seizures at age 4 associated with language deterioration despite anticonvulsant therapy. With levetiracetam monotherapy to a dose of 60 mg/kg/day and discontinuation of carbamazepine and valproic acid, her language has improved and seizures are controlled. Levetiracetam should be considered as therapy for Landau-Kleffner syndrome.