Limbic ERPs predict verbal memory after left-sided hippocampectomy

Grünwald, Thomas; Lehnertz, Klaus; Helmstaedter, Christoph; Kutas, Marta; Pezer, Nico; Kurthen, Martin; Roost, Dirk Van; Elger, Christian E.

doi:10.1097/00001756-199810260-00007

Cited by 56 publications

(48 citation statements)

References 7 publications

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“…Our findings are also consistent with the reported correlations between verbal memory performance and AMTL-N400s to new words (21,42) and neuronal densities in the CA1 subfield (50,51). Impairment of NMDA receptor-mediated encoding processes may thus explain the significant memory deficits in human patients with bilateral lesions confined to the CA1 subfield (52,53).…”

Section: Discussionsupporting

confidence: 91%

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Evidence relating human verbal memory to hippocampal N -methyl- d- aspartate receptors

Grünwald¹,

Beck²,

Lehnertz³

et al. 1999

Proc. Natl. Acad. Sci. U.S.A.

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132

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Studies in rodents and nonhuman primates have linked the activity of N-methyl-D-aspartate (NMDA) receptors within the hippocampus to animals' performance on memory-related tasks. However, whether these receptors are similarly essential for human memory is still an open question. Here we present evidence suggesting that hippocampal NMDA receptors, most likely within the CA1 region, do participate in human verbal memory processes. Words elicit a negative event-related potential (ERP) peaking around 400 ms within the anterior mesial temporal lobe (AMTL-N400). Ketamine, an NMDA-receptor antagonist, reduces the amplitude of the AMTL-N400 (in contrast to other hippocampal potentials) on initial presentation, eliminates the typical AMTL-N400 amplitude reduction with repetition, and leads to significant memory impairment. Of the various hippocampal subfields, only the density of CA1 neurons correlates with the word-related ERPs that are reduced by ketamine. Altogether, our behavioral, anatomical, and electrophysiological results indicate that hippocampal NMDA receptors are involved in human memory. L ong-term potentiation (LTP) is a long-lasting increase in synaptic efficacy after high-frequency stimulation of afferent fibers. It depends on high levels of postsynaptic calcium. The primary source of the calcium influx during the induction of hippocampal LTP occurs through an ion channel that is coupled to the N-methyl-D-aspartate (NMDA) subtype of glutamate receptor (1, 2). NMDA receptors are thus hypothesized to play a crucial role in the induction of associative LTP within the hippocampal CA1-region (3); this is viewed as a putative mechanism for Hebbian learning. This form of synaptic plasticity has been offered as a cellular model of memory processes in hippocampal slice preparations (4). Numerous studies in rodents and primates have linked hippocampal LTP with spatial learning and memory (5) although there are some contradictory results (6).NMDA receptors are also abundant within the human hippocampus (14, 15). NMDA receptor antagonists block LTP induction in surgically resected specimens from the human temporal cortex (16). The human mesial temporal lobe system is considered essential for declarative memory (7, 8), contributing to both encoding and retrieval (9-13). Despite the suggestive findings of animal studies, however, the question of whether hippocampal NMDA receptors contribute to human memory processes remains unsettled.The occasional need to place depth electrodes within the mesial temporal lobes during the presurgical evaluation of patients with pharmacoresistant temporal lobe epilepsy affords us the opportunity to record depth potentials directly from the human hippocampal formation. Analyses of limbic event-related potentials (ERPs) can contribute to the presurgical workup with respect to both the lateralization of the epileptogenic focus (17-19) and the prediction of surgical outcome (20,21). Limbic ERPs also offer unique opportunities for investigating the relationship between hippocampal structures ...

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Section: Discussionsupporting

confidence: 91%

“…Analyses of limbic event-related potentials (ERPs) can contribute to the presurgical workup with respect to both the lateralization of the epileptogenic focus (17-19) and the prediction of surgical outcome (20,21). Limbic ERPs also offer unique opportunities for investigating the relationship between hippocampal structures and their functions (22).…”

mentioning

confidence: 99%

Evidence relating human verbal memory to hippocampal N -methyl- d- aspartate receptors

Grünwald¹,

Beck²,

Lehnertz³

et al. 1999

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

132

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“…These locations match those that have been demonstrated to generate potentials at this latency in the same or similar paradigms (see Introduction). In particular, although words in an explicit recognition paradigm do evoke N400e-like activity in the region of the left superior temporal sulcus (Halgren et al, 1994a;Guillem et al, 1995;Elger et al, 1997), the most prominent generators are in the anteroventral temporal (Smith et al, 1986;Halgren et al, 1994a;McCarthy et al, 1995;Fernandez et al, 1998;Grunwald et al, 1998), orbitofrontal, and posteroventral prefrontal (Halgren et al, 1994b;Guillem et al, 1999) cortices. Thus, the distributed source modeling technique used here identifies a distributed network of N400 generators similar to that previously demonstrated with intracranial recordings.…”

Section: Sentence-terminal Wordsmentioning

confidence: 96%

“…These include comparisons between congruous and incongruous sentence completions , related and unrelated word pairs (Nobre et al, 1994;Nobre and McCarthy, 1995), high-and lowfrequency words (Fernandez et al, 1998), content and function words , and repeated versus initial presentations of isolated words (Smith et al, 1986;Puce et al, 1991;Halgren et al, 1994a,b;Elger et al, 1997;Helmstaedter et al, 1997;Fernandez et al, 1998;Grunwald et al, 1998). Many of these studies have converged to suggest an N400 generator in the anterior medial temporal lobe (AMTL).…”

Section: Figmentioning

confidence: 99%

N400-like Magnetoencephalography Responses Modulated by Semantic Context, Word Frequency, and Lexical Class in Sentences

et al. 2002

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Words have been found to elicit a negative potential at the scalp peaking at ϳ400 ms that is strongly modulated by semantic context. The current study used whole-head magnetoencephalography (MEG) as male subjects read sentences ending with semantically congruous or incongruous words. Compared with congruous words, sentence-terminal incongruous words consistently evoked a large magnetic field over the left hemisphere, peaking at ϳ450 ms. Source modeling at this latency with conventional equivalent current dipoles (ECDs) placed the N400m generator in or near the left superior temporal sulcus. A distributed solution constrained to the cortical surface suggested a sequence of differential activation, beginning in Wernicke's area at ϳ250 ms, spreading to anterior temporal sites at ϳ270 ms, to Broca's area by ϳ300 ms, to dorsolateral prefrontal cortices by ϳ320 ms, and to anterior orbital and frontopolar cortices by ϳ370 ms. Differential activity was exclusively left-sided until >370 ms, and then involved right anterior temporal and orbital cortices. At the peak of the N400m, activation in the left hemisphere was estimated to be widespread in the anterior temporal, perisylvian, orbital, frontopolar, and dorsolateral prefrontal cortices. In the right hemisphere, the orbital, as well as, weakly, the right anterior temporal cortices were activated. Similar but weaker field patterns were evoked by intermediate words in the sentences, especially to low-frequency words occurring in early sentence positions where there is little preceding context. The locations of the N400m sources identified with the distributed solution correspond well with those previously demonstrated with direct intracranial recordings, and suggested by functional magnetic resonance imaging (fMRI). These results help identify a distributed cortical network that supports online semantic processing. © 2002 Elsevier Science (USA)

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“…Developments of magnetic resonance imaging (MRI) techniques have made important contributions to identifying the syndrome of MTLE with hippocampal sclerosis (1) and a better postoperative outcome than TLE without any structural lesion (23). Positron emission tomography (PET) may contribute to the prediction of postoperative seizure control in TLE (4), whereas single photon emission computed tomography (SPECT) seems to be more problematic in this group of patients (5).…”

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confidence: 99%

Prediction of Postoperative Seizure Control by Hippocampal Event‐Related Potentials

et al. 1999

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Summary:Purpose: In spite of unequivocal results of the presurgical evaluation, between 10 and 30% of patients with medial temporal lobe epilepsy (MTLE) do not become seizure free by temporal lobe surgery. Because event-related potentials (ERPs) recorded within the hippocampal formation have been shown to be sensitive to the epileptogenic process, we examined whether ERPs can help to improve the prediction of postoperative seizure control.Merhods: We recorded ERPs to words from bilateral intrahippocampal electrodes by using a visual word-recognition paradigm in 70 patients with unilateral hippocampal pathology and related these measurements to seizure outcome after temporal lobe surgery.Results: Words elicited N400 potentials, which were reduced in amplitude on repetition on the side contralateral to hippocampal sclerosis. This contralateral repetition effect, however, was significantly diminished in the group of patients who experienced seizure recurrence after the operation. Contralateral repetition effects thus permitted correct prediction of postoperative seizure control in 94% of all patients.Conclusions: Recording ERPs to words within the medial temporal lobes can improve the prediction of postoperative seizure control. Reduced repetition effects contralateral to the side of hippocampal sclerosis may indicate bilateral epileptogenicity.

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Limbic ERPs predict verbal memory after left-sided hippocampectomy

Cited by 56 publications

References 7 publications

Evidence relating human verbal memory to hippocampal N -methyl- d- aspartate receptors

Evidence relating human verbal memory to hippocampal N -methyl- d- aspartate receptors

N400-like Magnetoencephalography Responses Modulated by Semantic Context, Word Frequency, and Lexical Class in Sentences

Prediction of Postoperative Seizure Control by Hippocampal Event‐Related Potentials

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