Evidence Relating Human Verbal Memory to Hippocampal N-methyl-D-aspartate Receptors

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 1999 Oct 16

PMID 10518580

Citations 26

Authors

T Grunwald

H Beck

K Lehnertz

I Blumcke

N Pezer

M Kurthen

G Fernandez

D Van Roost

H J Heinze

M Kutas

C E Elger

Affiliations

Soon will be listed here.

Abstract

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.

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References

Nobre A, McCarthy G . Language-related field potentials in the anterior-medial temporal lobe: II. Effects of word type and semantic priming. J Neurosci. 1995; 15(2):1090-8. PMC: 6577813. View

Grunwald T, Lehnertz K, Helmstaedter C, Kutas M, Pezer N, Kurthen M . Limbic ERPs predict verbal memory after left-sided hippocampectomy. Neuroreport. 1998; 9(15):3375-8. DOI: 10.1097/00001756-199810260-00007. View

Grunwald T, Beck H, Lehnertz K, Blumcke I, Pezer N, Kutas M . Limbic P300s in temporal lobe epilepsy with and without Ammon's horn sclerosis. Eur J Neurosci. 1999; 11(6):1899-906. DOI: 10.1046/j.1460-9568.1999.00613.x. View

Elger C, Grunwald T, Lehnertz K, Kutas M, Helmstaedter C, Brockhaus A . Human temporal lobe potentials in verbal learning and memory processes. Neuropsychologia. 1997; 35(5):657-67. DOI: 10.1016/s0028-3932(96)00110-8. View

Meador K, Loring D, King D, GALLAGHER B, Gould M, Smith J . Cholinergic modulation of human limbic evoked potentials. Int J Neurosci. 1988; 38(3-4):407-14. DOI: 10.3109/00207458808990701. View

Tsien J, Huerta P, Tonegawa S . The essential role of hippocampal CA1 NMDA receptor-dependent synaptic plasticity in spatial memory. Cell. 1996; 87(7):1327-38. DOI: 10.1016/s0092-8674(00)81827-9. View

Breier A, Adler C, Weisenfeld N, Su T, Elman I, PICKEN L . Effects of NMDA antagonism on striatal dopamine release in healthy subjects: application of a novel PET approach. Synapse. 1998; 29(2):142-7. DOI: 10.1002/(SICI)1098-2396(199806)29:2<142::AID-SYN5>3.0.CO;2-7. View

Puce A, Kalnins R, Berkovic S, Donnan G, Bladin P . Limbic P3 potentials, seizure localization, and surgical pathology in temporal lobe epilepsy. Ann Neurol. 1989; 26(3):377-85. DOI: 10.1002/ana.410260311. View

Gabrieli J, Brewer J, Desmond J, Glover G . Separate neural bases of two fundamental memory processes in the human medial temporal lobe. Science. 1997; 276(5310):264-6. DOI: 10.1126/science.276.5310.264. View

10.

Smith M, Stapleton J, Halgren E . Human medial temporal lobe potentials evoked in memory and language tasks. Electroencephalogr Clin Neurophysiol. 1986; 63(2):145-59. DOI: 10.1016/0013-4694(86)90008-8. View

11.

Malhotra A, Pinals D, Weingartner H, Sirocco K, Missar C, Pickar D . NMDA receptor function and human cognition: the effects of ketamine in healthy volunteers. Neuropsychopharmacology. 1996; 14(5):301-7. DOI: 10.1016/0893-133X(95)00137-3. View

12.

Feuerstein T . [Ketamine inhibits n-methyl-d-aspartate (NMDA) receptor mediated acetylcholine release from rabbit caudate nucleus slices]. Anaesthesist. 1994; 43 Suppl 2:S48-51. View

13.

Squire L . The medial temporal lobe memory system. Science. 1991; 253(5026):1380-6. DOI: 10.1126/science.1896849. View

14.

McHugh T, Blum K, Tsien J, Tonegawa S, Wilson M . Impaired hippocampal representation of space in CA1-specific NMDAR1 knockout mice. Cell. 1996; 87(7):1339-49. DOI: 10.1016/s0092-8674(00)81828-0. View

15.

Halgren E, Baudena P, Heit G, Clarke J, Marinkovic K, Clarke M . Spatio-temporal stages in face and word processing. I. Depth-recorded potentials in the human occipital, temporal and parietal lobes [corrected]. J Physiol Paris. 1994; 88(1):1-50. DOI: 10.1016/0928-4257(94)90092-2. View

16.

Maren S, Baudry M . Properties and mechanisms of long-term synaptic plasticity in the mammalian brain: relationships to learning and memory. Neurobiol Learn Mem. 1995; 63(1):1-18. DOI: 10.1006/nlme.1995.1001. View

17.

Stern C, Corkin S, Gonzalez R, Guimaraes A, Baker J, Jennings P . The hippocampal formation participates in novel picture encoding: evidence from functional magnetic resonance imaging. Proc Natl Acad Sci U S A. 1996; 93(16):8660-5. PMC: 38729. DOI: 10.1073/pnas.93.16.8660. View

18.

Grunwald T, Lehnertz K, Pezer N, Kurthen M, Van Roost D, Schramm J . Prediction of postoperative seizure control by hippocampal event-related potentials. Epilepsia. 1999; 40(3):303-6. DOI: 10.1111/j.1528-1157.1999.tb00708.x. View

19.

Van Roost D, Solymosi L, Schramm J, van Oosterwyck B, Elger C . Depth electrode implantation in the length axis of the hippocampus for the presurgical evaluation of medial temporal lobe epilepsy: a computed tomography-based stereotactic insertion technique and its accuracy. Neurosurgery. 1998; 43(4):819-26; discussion 826-7. DOI: 10.1097/00006123-199810000-00058. View

20.

Malhotra A, Pinals D, Adler C, Elman I, Clifton A, Pickar D . Ketamine-induced exacerbation of psychotic symptoms and cognitive impairment in neuroleptic-free schizophrenics. Neuropsychopharmacology. 1997; 17(3):141-50. DOI: 10.1016/S0893-133X(97)00036-5. View