Abolition of long-term stability of new hippocampal place cell maps by NMDA receptor blockade

Science

Volumn 280, Issue 5372, 1998, Pages 2121-2126

  Kentros, Clifford ^a   Hargreaves, Eric ^a   Hawkins, Robert D ^a   Kandel, Eric R ^a   Shapiro, Matthew ^a   Muller, Robert V ^a  

^a NONE

Author keywords

[No Author keywords available]

Indexed keywords

N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

COGNITION; HIPPOCAMPUS; LONG TERM POTENTIATION; MEMORY; NONHUMAN; PRIORITY JOURNAL; REVIEW; SPATIAL DISCRIMINATION; SPATIAL MEMORY;

ANIMALS; BRAIN MAPPING; EVOKED POTENTIALS; EXCITATORY AMINO ACID ANTAGONISTS; HIPPOCAMPUS; LONG-TERM POTENTIATION; MALE; MEMORY; NEURONAL PLASTICITY; PIPERAZINES; PYRAMIDAL CELLS; RATS; RECEPTORS, N-METHYL-D-ASPARTATE; SPACE PERCEPTION; TIME FACTORS;

EID: 0032568888     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.280.5372.2121     Document Type: Review

References (48)

1. J. O'Keefe and J. Dostrovsky, Brain Res. 34, 171 (1971).
2. J. Bures et al., Proc. Natl. Acad. Sci. U.S.A. 94, 343 (1997); R. V. Muller, Neuron 17, 813 (1996).
3. J. Bures et al., Proc. Natl. Acad. Sci. U.S.A. 94, 343 (1997); R. V. Muller, Neuron 17, 813 (1996).
4. J. O'Keefe and L. Nadel, The Hippocampus as a Cognitive Map (Clarendon, Oxford, UK, 1978); J. O'Keefe and A. Speakman, Exp. Brain Res. 68, 1 (1987).
5. J. O'Keefe and L. Nadel, The Hippocampus as a Cognitive Map (Clarendon, Oxford, UK, 1978); J. O'Keefe and A. Speakman, Exp. Brain Res. 68, 1 (1987).
6. R. U. Muller, J. L. Kubie, J. B. Ranck Jr., J. Neurosci. 7, 1935 (1987); L. T. Thompson and P. J. Best, Brain Res. 509, 189 (1990).
7. R. U. Muller, J. L. Kubie, J. B. Ranck Jr., J. Neurosci. 7, 1935 (1987); L. T. Thompson and P. J. Best, Brain Res. 509, 189 (1990).
8. J. L. Kubie and J. B. Ranck, in Neurobiology of the Hippocampus, W. Seifert, Ed. (Academic Press, New York, 1983), pp. 433-447.
9. R. U. Muller and J. L. Kubie, J. Neurosci. 7, 1951 (1987).
10. E. Bostock, R. U. Muller, J. L. Kubie, Hippocampus 1, 193 (1991).
11. A. J. Hill, Exp. Neurol. 62, 282 (1978); M. A. Wilson and B. L. McNaughton, Science 261, 1055 (1993).
12. A. J. Hill, Exp. Neurol. 62, 282 (1978); M. A. Wilson and B. L. McNaughton, Science 261, 1055 (1993).
13. Recently reviewed by J. T. Isaac et al., J. Physiol. Paris 90, 299 (1996); R. A. Nicoll and R. C. Malenka, Nature 377, 115 (1995).
14. Recently reviewed by J. T. Isaac et al., J. Physiol. Paris 90, 299 (1996); R. A. Nicoll and R. C. Malenka, Nature 377, 115 (1995).
15. Recently reviewed by R. G. Morris and U. Frey, Philos. Trans. R. Soc. London B Biol. Sci. 352, 1489 (1997); D. P. Cain, Curr. Opin. Neurobiol. 7, 235 (1997); C. Chen and S. Tonegawa, Annu. Rev. Neurosci. 20, 157 (1997).
16. Recently reviewed by R. G. Morris and U. Frey, Philos. Trans. R. Soc. London B Biol. Sci. 352, 1489 (1997); D. P. Cain, Curr. Opin. Neurobiol. 7, 235 (1997); C. Chen and S. Tonegawa, Annu. Rev. Neurosci. 20, 157 (1997).
17. Recently reviewed by R. G. Morris and U. Frey, Philos. Trans. R. Soc. London B Biol. Sci. 352, 1489 (1997); D. P. Cain, Curr. Opin. Neurobiol. 7, 235 (1997); C. Chen and S. Tonegawa, Annu. Rev. Neurosci. 20, 157 (1997).
18. The methods used in this study are fundamentally similar to those previously summarized in detail (6, 7). Briefly, food-deprived adult male Long-Evans rats (Harlan) were trained to chase randomly dropped food pellets (Bio-Serv) in a 51-cm-high gray cylinder (76-cm diameter) with a white card mounted on one wall to provide an asymmetrical cue. After being thoroughly familiarized with the task and environment, animals were implanted stereotactically (anterior, -2 mm; lateral, 1.8 mm; dorsal, 2 mm) with a drivable 10-wire (25-μm nichrome) microelectrode array about 1 mm dorsal to the CA1 hippocampal pyramidal cell layer. At least 5 days after surgery, animals were screened for units while chasing pellets in the gray cylinder. Units were amplified 10,000 times and bandpass filtered at 300 to 10,000 Hz. The amplifier output was digitized at 40 kHz. When at least two place cells could be simultaneously recorded in the gray cylinder, cue control was tested by rotating the cylinder 90°. In all cases, all fields rotated 90° (28). The next day, after one 8-min test session (D1G0) in the gray cylinder (the familiar environment), animals were injected intraperitoneally (ip) with either saline or CPP (10 mg/kg) and returned to their cages for an hour. All other recording sessions were 16 min. The intervals between sessions are shown in the legend for Fig. 1. Animals were always returned to their home cage between recording sessions. Units were analyzed offline with the Discovery CP Analysis and Autocut software packages (Datawave, Longmont, CO). Although it is possible that in some cases a "unit" was really two neurons, this would have worked against our main findings by increasing the variability of the data.
19. The rate maps produced by a given cell in two sessions were treated as two lists of numbers for the calculation of a correlation coefficient. The values of correlation coefficients for all cells from an animal were averaged to provide a mean "similarity" score. Cells that had an overall firing rate of less than 0.1 spikes per second in both sessions were excluded from quantitative analysis.
20. i is the mean firing rate for bin i, and R is the overall mean firing rate {from E. Markus et al. [Hippocampus 4, 410 (1994)]}. Running speed was calculated every 0.25 s and averaged across the session.
21. -3].
22. L. Ward et al., Pharmacol. Biochem. Behav. 35, 785 (1990).
23. H. V. Curran, Biol. Psychol. 23, 179 (1986); T. U. Jarbe, Acta Neurol. Scand. Suppl. 109, 37 (1986).
24. H. V. Curran, Biol. Psychol. 23, 179 (1986); T. U. Jarbe, Acta Neurol. Scand. Suppl. 109, 37 (1986).
25. D. M. Diamond et al., J. Neurosci. 8, 4079 (1988); J. Larson and G. Lynch, Brain Res. 441, 111 (1988).
26. D. M. Diamond et al., J. Neurosci. 8, 4079 (1988); J. Larson and G. Lynch, Brain Res. 441, 111 (1988).
27. Male Long-Evans rats (Charles River Laboratories) were anesthetized and implanted with two twisted pairs of Teflon-coated stainless steel wires (127-μm diameter) for stimulation and recording. The recording electrode was positioned in the pyramidal layer of the CA1 region of the hippocampus, and the stimulating electrode was positioned in the contralateral ventral hippocampal commissure. Electrode positions were confirmed by postmortem histology. After at least 5 days of recovery, evoked potentials were recorded in awake, freely behaving animals. The electroencephalogram was also recorded to insure that there were no after discharges and that the animals were not asleep. Population spike amplitude was measured between the negative peak and the maximum positive peak of the evoked potential. The stimulation intensity was adjusted to produce a population spike that was 30% of maximum at the beginning of the experiment, and the evoked potential was tested once every 12 s for at least 40 min. After a 5-min baseline period, primed-burst potentiation was induced during behavioral immobility, with a single stimulus pulse followed 170 ms later by a four-pulse, 200-Hz burst at an intensity that produced a maximal population spike. This procedure was repeated four times: during a baseline session, the next day both 90 and 180 min after injection of CPP (10 mg/kg ip), and again 24 hours after the CPP injection.
28. T. J. McHugh et al., Cell 87, 1339 (1996).
29. R. J. Cole et al., Psychopharmacology 111, 465 (1993); M. P. Pellicano et al., Physiol. Behav. 54, 563 (1993); A. Ungerer et al., Brain Res. 549, 59 (1991).
30. R. J. Cole et al., Psychopharmacology 111, 465 (1993); M. P. Pellicano et al., Physiol. Behav. 54, 563 (1993); A. Ungerer et al., Brain Res. 549, 59 (1991).
31. R. J. Cole et al., Psychopharmacology 111, 465 (1993); M. P. Pellicano et al., Physiol. Behav. 54, 563 (1993); A. Ungerer et al., Brain Res. 549, 59 (1991).
32. S. Davis et al., J. Neurosci. Methods 75, 75 (1997); R. V. Hernandez et al. Brain Res. 656, 215 (1994); W. C. Abraham and S. E. Mason, ibid. 462, 40 (1988).
33. S. Davis et al., J. Neurosci. Methods 75, 75 (1997); R. V. Hernandez et al. Brain Res. 656, 215 (1994); W. C. Abraham and S. E. Mason, ibid. 462, 40 (1988).
34. S. Davis et al., J. Neurosci. Methods 75, 75 (1997); R. V. Hernandez et al. Brain Res. 656, 215 (1994); W. C. Abraham and S. E. Mason, ibid. 462, 40 (1988).
35. J. W. Rudy, S. Stadler-Morris, P. Albert, Behav. Neurosci. 101, 62 (1987).
36. K. B. Austin, W. F. Fortin, M. L. Shapiro, Soc. Neurosci. Abstr. 16, 263 (1990).
37. R. U. Muller et al., J. Gen. Physiol. 107, 663 (1996); P. A. Hetherington and M. L. Shapiro, Behav. Neurosci. 107, 434 (1993); R. U. Muller et al., Hippocampus 1, 243 (1991).
38. R. U. Muller et al., J. Gen. Physiol. 107, 663 (1996); P. A. Hetherington and M. L. Shapiro, Behav. Neurosci. 107, 434 (1993); R. U. Muller et al., Hippocampus 1, 243 (1991).
39. R. U. Muller et al., J. Gen. Physiol. 107, 663 (1996); P. A. Hetherington and M. L. Shapiro, Behav. Neurosci. 107, 434 (1993); R. U. Muller et al., Hippocampus 1, 243 (1991).
40. M. L. Shapiro and C. O'Connor, Behav. Neurosci. 106, 604 (1992); Z. Caramanos and M. L. Shapiro, ibid. 108, 30 (1994).
41. M. L. Shapiro and C. O'Connor, Behav. Neurosci. 106, 604 (1992); Z. Caramanos and M. L. Shapiro, ibid. 108, 30 (1994).
42. D. M. Bannerman, M. A. Good, S. P. Butcher, M. Ramsay, R. G. M. Morris, Nature 378, 182 (1995); D. Saucier and D. P. Cain, ibid., p. 186.
43. D. M. Bannerman, M. A. Good, S. P. Butcher, M. Ramsay, R. G. M. Morris, Nature 378, 182 (1995); D. Saucier and D. P. Cain, ibid., p. 186.
44. A. Rotenberg, M. Mayford, R. D. Hawkins, E. R. Kandel, R. U. Muller, Cell 87, 1351 (1996); A. Rotenberg, J. Abel, E. R. Kandel, R. U. Muller, Soc. Neurosci. Abstr. 23, 501 (1997); Y. Cho, K. P. Giese, H. Tanila, A. J. Silva, H. Eichenbaum, Science 279, 867 (1998).
45. A. Rotenberg, M. Mayford, R. D. Hawkins, E. R. Kandel, R. U. Muller, Cell 87, 1351 (1996); A. Rotenberg, J. Abel, E. R. Kandel, R. U. Muller, Soc. Neurosci. Abstr. 23, 501 (1997); Y. Cho, K. P. Giese, H. Tanila, A. J. Silva, H. Eichenbaum, Science 279, 867 (1998).
46. A. Rotenberg, M. Mayford, R. D. Hawkins, E. R. Kandel, R. U. Muller, Cell 87, 1351 (1996); A. Rotenberg, J. Abel, E. R. Kandel, R. U. Muller, Soc. Neurosci. Abstr. 23, 501 (1997); Y. Cho, K. P. Giese, H. Tanila, A. J. Silva, H. Eichenbaum, Science 279, 867 (1998).
47. C. Kentros et al., data not shown.
48. We thank M. Pellan for typing the manuscript. Supported by the Howard Hughes Medical Institute, the National Institute of Mental Health (R01 45923), the NIH (R01 20686), and the National Institute on Aging (T32 AGO 00189).