Real-time tracking of memory formation in the human rhinal cortex and hippocampus

Science

Volumn 285, Issue 5433, 1999, Pages 1582-1585

  Fernández, Guillén ^a   Effern, Arndt ^a   Grunwald, Thomas ^a   Pezer, Nico ^a   Lehnertz, Klaus ^a   Dümpelmann, Matthias ^a   Van Roost, Dirk ^a   Elger, Christian E ^a  

^a UNIVERSITY OF BONN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BRAIN MAPPING; CLINICAL ARTICLE; ENTORHINAL CORTEX; EVENT RELATED POTENTIAL; HEMISPHERIC DOMINANCE; HIPPOCAMPUS; HUMAN; LEFT HEMISPHERE; MEMORY; PRIORITY JOURNAL; RECALL; TEMPORAL LOBE; TEMPORAL LOBE EPILEPSY; VERBAL MEMORY;

ADULT; ANALYSIS OF VARIANCE; BRAIN MAPPING; ELECTRODES, IMPLANTED; EPILEPSY, TEMPORAL LOBE; EVOKED POTENTIALS; FEMALE; HIPPOCAMPUS; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MEMORY; MENTAL RECALL; MIDDLE AGED; NEURONS; TEMPORAL LOBE; TIME FACTORS;

HIPPOCAMPUS HIPPOCAMPUS;

EID: 0041982056     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.285.5433.1582     Document Type: Article

References (56)

1. L. R. Squire and S. Zola-Morgan, Science 253, 1380 (1991).
2. E. Tulving, in Organization of Memory, E. Tulving and W. Donaldson, Eds. (Academic Press, New York, 1972), pp. 381-403.
3. W. B. Scoville and B. Milner, J. Neurol. Neurosurg. Psychiatry 20, 11 (1957).
4. J. B. Brewer, Z. Zhao, J. E. Desmond, G. H. Glover, J. D. E. Gabrieli, Science 281, 1185 (1998); A. D. Wagner et al., ibid., p. 1188.
5. J. B. Brewer, Z. Zhao, J. E. Desmond, G. H. Glover, J. D. E. Gabrieli, Science 281, 1185 (1998); A. D. Wagner et al., ibid., p. 1188.
6. R. J. Dolan and P. F. Fletcher, Hippocampus 9, 25 (1999); G. Fernández et al., J. Neurosci. 18, 1841 (1998); G. Fernández, J. B. Brewer, Z. Zhao, G. H. Glover, J. D. E. Gabrieli, Hippocampus 9, 35 (1999); K. Henke, B. Weber, S. Kneifel, H. G. Wieser, A. Buck, Proc. Natl. Acad. Sci. U.S.A. 96, 5884 (1999).
7. R. J. Dolan and P. F. Fletcher, Hippocampus 9, 25 (1999); G. Fernández et al., J. Neurosci. 18, 1841 (1998); G. Fernández, J. B. Brewer, Z. Zhao, G. H. Glover, J. D. E. Gabrieli, Hippocampus 9, 35 (1999); K. Henke, B. Weber, S. Kneifel, H. G. Wieser, A. Buck, Proc. Natl. Acad. Sci. U.S.A. 96, 5884 (1999).
8. R. J. Dolan and P. F. Fletcher, Hippocampus 9, 25 (1999); G. Fernández et al., J. Neurosci. 18, 1841 (1998); G. Fernández, J. B. Brewer, Z. Zhao, G. H. Glover, J. D. E. Gabrieli, Hippocampus 9, 35 (1999); K. Henke, B. Weber, S. Kneifel, H. G. Wieser, A. Buck, Proc. Natl. Acad. Sci. U.S.A. 96, 5884 (1999).
9. R. J. Dolan and P. F. Fletcher, Hippocampus 9, 25 (1999); G. Fernández et al., J. Neurosci. 18, 1841 (1998); G. Fernández, J. B. Brewer, Z. Zhao, G. H. Glover, J. D. E. Gabrieli, Hippocampus 9, 35 (1999); K. Henke, B. Weber, S. Kneifel, H. G. Wieser, A. Buck, Proc. Natl. Acad. Sci. U.S.A. 96, 5884 (1999).
10. D. G. Amaral and R. Insausti, in The Human Nervous System, G. Paxinos, Ed. (Academic Press, San Diego, CA, 1990), pp. 711-755; W. A. Suzuki and D. G. Amaral, J. Neurosci. 14, 1856 (1994).
11. D. G. Amaral and R. Insausti, in The Human Nervous System, G. Paxinos, Ed. (Academic Press, San Diego, CA, 1990), pp. 711-755; W. A. Suzuki and D. G. Amaral, J. Neurosci. 14, 1856 (1994).
12. M. Lepage, R. Habib, E. Tulving, Hippocampus 8, 313 (1998); D. L. Schacter and A. D. Wagner, ibid. 9, 7 (1999).
13. M. Lepage, R. Habib, E. Tulving, Hippocampus 8, 313 (1998); D. L. Schacter and A. D. Wagner, ibid. 9, 7 (1999).
14. L. R. Squire and S. M. Zola, Hippocampus 8, 205 (1998); F. Vargha-Khadem et al., Science 277, 376 (1997); S. Zola-Morgan, L. R. Squire, D. G. Amaral, J. Neurosci. 6, 2950 (1986).
15. L. R. Squire and S. M. Zola, Hippocampus 8, 205 (1998); F. Vargha-Khadem et al., Science 277, 376 (1997); S. Zola-Morgan, L. R. Squire, D. G. Amaral, J. Neurosci. 6, 2950 (1986).
16. L. R. Squire and S. M. Zola, Hippocampus 8, 205 (1998); F. Vargha-Khadem et al., Science 277, 376 (1997); S. Zola-Morgan, L. R. Squire, D. G. Amaral, J. Neurosci. 6, 2950 (1986).
17. J. P. Aggleton and M. W. Brown, Behav. Brain. Sci., in press; N. J. Cohen and H. Eichenbaum, Memory, Amnesia, and the Hippocampal System. (MIT Press, Cambridge, MA, 1993); H. Eichenbaum, T. Otto, N. J. Cohen, Behav. Brain Sci. 17, 449 (1994); M. Mishkin, W. A. Suzuki, D. G. Gadian, F. Vargha-Khadem, Philos. Trans. R. Soc. London Ser. B 352, 1461 (1997); S. Zola-Morgan, L. R. Squire, S. J. Ramus, Hippocampus 4, 483 (1994).
18. J. P. Aggleton and M. W. Brown, Behav. Brain. Sci., in press; N. J. Cohen and H. Eichenbaum, Memory, Amnesia, and the Hippocampal System. (MIT Press, Cambridge, MA, 1993); H. Eichenbaum, T. Otto, N. J. Cohen, Behav. Brain Sci. 17, 449 (1994); M. Mishkin, W. A. Suzuki, D. G. Gadian, F. Vargha-Khadem, Philos. Trans. R. Soc. London Ser. B 352, 1461 (1997); S. Zola-Morgan, L. R. Squire, S. J. Ramus, Hippocampus 4, 483 (1994).
19. J. P. Aggleton and M. W. Brown, Behav. Brain. Sci., in press; N. J. Cohen and H. Eichenbaum, Memory, Amnesia, and the Hippocampal System. (MIT Press, Cambridge, MA, 1993); H. Eichenbaum, T. Otto, N. J. Cohen, Behav. Brain Sci. 17, 449 (1994); M. Mishkin, W. A. Suzuki, D. G. Gadian, F. Vargha-Khadem, Philos. Trans. R. Soc. London Ser. B 352, 1461 (1997); S. Zola-Morgan, L. R. Squire, S. J. Ramus, Hippocampus 4, 483 (1994).
20. J. P. Aggleton and M. W. Brown, Behav. Brain. Sci., in press; N. J. Cohen and H. Eichenbaum, Memory, Amnesia, and the Hippocampal System. (MIT Press, Cambridge, MA, 1993); H. Eichenbaum, T. Otto, N. J. Cohen, Behav. Brain Sci. 17, 449 (1994); M. Mishkin, W. A. Suzuki, D. G. Gadian, F. Vargha-Khadem, Philos. Trans. R. Soc. London Ser. B 352, 1461 (1997); S. Zola-Morgan, L. R. Squire, S. J. Ramus, Hippocampus 4, 483 (1994).
21. J. P. Aggleton and M. W. Brown, Behav. Brain. Sci., in press; N. J. Cohen and H. Eichenbaum, Memory, Amnesia, and the Hippocampal System. (MIT Press, Cambridge, MA, 1993); H. Eichenbaum, T. Otto, N. J. Cohen, Behav. Brain Sci. 17, 449 (1994); M. Mishkin, W. A. Suzuki, D. G. Gadian, F. Vargha-Khadem, Philos. Trans. R. Soc. London Ser. B 352, 1461 (1997); S. Zola-Morgan, L. R. Squire, S. J. Ramus, Hippocampus 4, 483 (1994).
22. U. Gleissner, C. Helmstaedter, M. Kurthen, C. E. Elger, Neuroreport 8, 2893 (1997); J. L. Ringo, J. Neurophysiol. 73, 1712 (1995).
23. U. Gleissner, C. Helmstaedter, M. Kurthen, C. E. Elger, Neuroreport 8, 2893 (1997); J. L. Ringo, J. Neurophysiol. 73, 1712 (1995).
24. K. A. Paller, M. Kutas, A. R. Mayes, Electroencephalogr. Clin. Neurophysiol. 67, 360 (1987).
25. G. Fernández et al., Psychophysiology 35, 709 (1998); H. J. Neville, M. Kutas, G. Chesney, A. L. Schmidt, J. Mem. Lang. 25, 75 (1986); K. A. Paller, J. Exp. Psychol. Learn. Mem. Cogn. 16, 1021 (1990).
26. G. Fernández et al., Psychophysiology 35, 709 (1998); H. J. Neville, M. Kutas, G. Chesney, A. L. Schmidt, J. Mem. Lang. 25, 75 (1986); K. A. Paller, J. Exp. Psychol. Learn. Mem. Cogn. 16, 1021 (1990).
27. G. Fernández et al., Psychophysiology 35, 709 (1998); H. J. Neville, M. Kutas, G. Chesney, A. L. Schmidt, J. Mem. Lang. 25, 75 (1986); K. A. Paller, J. Exp. Psychol. Learn. Mem. Cogn. 16, 1021 (1990).
28. T. Picton, O. G. Lins, M. Scherg, in Handbook of Neuropsychology, F. Boller and J. Grafman, Eds. (Elsevier, Amsterdam, 1995), vol. 10, pp. 3-73.
29. G. McCarthy, A. C. Nobre, S. Bentin, D. D. Spencer, J. Neurosci. 15, 1080 (1995).
30. C. E. Elger et al., Neuropsychologia 35, 657 (1997); T. Grunwald, K. Lehnertz, H. J. Heinze, C. Helmstaedter, C. E. Elger, Proc. Natl. Acad. Sci. U.S.A. 95, 3193 (1998); E. Halgren et al., Science 210, 803 (1980). G. Heit, M. E. Smith, E. Halgren, Nature 333, 773 (1988); A. C. Nobre, T. Allison, G. McCarthy, ibid. 372, 260 (1994).
31. C. E. Elger et al., Neuropsychologia 35, 657 (1997); T. Grunwald, K. Lehnertz, H. J. Heinze, C. Helmstaedter, C. E. Elger, Proc. Natl. Acad. Sci. U.S.A. 95, 3193 (1998); E. Halgren et al., Science 210, 803 (1980). G. Heit, M. E. Smith, E. Halgren, Nature 333, 773 (1988); A. C. Nobre, T. Allison, G. McCarthy, ibid. 372, 260 (1994).
32. C. E. Elger et al., Neuropsychologia 35, 657 (1997); T. Grunwald, K. Lehnertz, H. J. Heinze, C. Helmstaedter, C. E. Elger, Proc. Natl. Acad. Sci. U.S.A. 95, 3193 (1998); E. Halgren et al., Science 210, 803 (1980). G. Heit, M. E. Smith, E. Halgren, Nature 333, 773 (1988); A. C. Nobre, T. Allison, G. McCarthy, ibid. 372, 260 (1994).
33. C. E. Elger et al., Neuropsychologia 35, 657 (1997); T. Grunwald, K. Lehnertz, H. J. Heinze, C. Helmstaedter, C. E. Elger, Proc. Natl. Acad. Sci. U.S.A. 95, 3193 (1998); E. Halgren et al., Science 210, 803 (1980). G. Heit, M. E. Smith, E. Halgren, Nature 333, 773 (1988); A. C. Nobre, T. Allison, G. McCarthy, ibid. 372, 260 (1994).
34. C. E. Elger et al., Neuropsychologia 35, 657 (1997); T. Grunwald, K. Lehnertz, H. J. Heinze, C. Helmstaedter, C. E. Elger, Proc. Natl. Acad. Sci. U.S.A. 95, 3193 (1998); E. Halgren et al., Science 210, 803 (1980). G. Heit, M. E. Smith, E. Halgren, Nature 333, 773 (1988); A. C. Nobre, T. Allison, G. McCarthy, ibid. 372, 260 (1994).
35. K. A. Paller, G. McCarthy, E. Roessler, T. Allison, C. C. Wood, Electroencephalogr. Clin. Neurophysiol. 84, 269 (1992).
36. Because seizure onset could not be determined unequivocally by noninvasive investigations, electrodes were implanted stereotactically along the longitudinal axis of each hippocampus (Fig. 1) as described [D. Van Roost, L. Solymosi, J. Schramm, B. van Oosterwyck, C. E. Elger, Neurosurgery 43, 819 (1998)]. Depth electroencephalograms were referenced to linked mastoids, bandpass-filtered (0.03 to 85 Hz, 6 dB per octave), and recorded with a sampling rate of 173 Hz (12-bit analog-digital conversion). Each averaging epoch lasted 2.2 s, including 0.2 s before stimulus onset. Electrode contacts were mapped by transferring their positions from MRI to standardized anatomical drawings (Fig. 2) (6) [G. D. Jackson and J. S. Duncan, MRI Neuroanatomy (Churchill Livingstone, New York, 1996)]. MRI scans were acquired In sagittal and adjusted coronal planes, perpendicular to the longitudinal axis of the hippocampus (repetition time = 3719 ms, echo time = 120 ms, flip angle = 90°, field of view = 22 cm; thickness, 2.0 mm; gap, 0.3 mm; 1.5 T) (ACS-II, Philips, Eindhoven, Netherlands).
37. Because seizure onset could not be determined unequivocally by noninvasive investigations, electrodes were implanted stereotactically along the longitudinal axis of each hippocampus (Fig. 1) as described [D. Van Roost, L. Solymosi, J. Schramm, B. van Oosterwyck, C. E. Elger, Neurosurgery 43, 819 (1998)]. Depth electroencephalograms were referenced to linked mastoids, bandpass-filtered (0.03 to 85 Hz, 6 dB per octave), and recorded with a sampling rate of 173 Hz (12-bit analog-digital conversion). Each averaging epoch lasted 2.2 s, including 0.2 s before stimulus onset. Electrode contacts were mapped by transferring their positions from MRI to standardized anatomical drawings (Fig. 2) (6) [G. D. Jackson and J. S. Duncan, MRI Neuroanatomy (Churchill Livingstone, New York, 1996)]. MRI scans were acquired In sagittal and adjusted coronal planes, perpendicular to the longitudinal axis of the hippocampus (repetition time = 3719 ms, echo time = 120 ms, flip angle = 90°, field of view = 22 cm; thickness, 2.0 mm; gap, 0.3 mm; 1.5 T) (ACS-II, Philips, Eindhoven, Netherlands).
38. All 12 patients (8 women; mean age 33.8 years, range 24 to 47) were native speakers of German and right-handed (left MTL seizure origin: n = 6; right MTL seizure origin: n = 6). At the time of the experiment all patients received carbamazepine (plasma concentration, 8 to 12 μ/ml) as the only centrally acting drug. No seizure occurred within 24 hours before the experiment Each patient gave written informed consent. The study was approved by the local medical ethics committee.
39. To prove the unilaterality of the epileptic zone, we controlled the site of seizure onset in invasive recordings and the effect of resective surgery on seizure frequency. During the presurgical evaluation, at least three spontaneous seizures were recorded invasively from each patient Each recorded seizure originated from the temporal lobe contralateral to the hemisphere investigated here. In the year before surgery, the range of the mean seizure frequencies per patient was 3.2 to 6.1 per month, and no month without any seizure occurred. After resection of the epileptic MTL, all patients remained seizure-free (follow-up, 5 to 13 months).
40. After the entire procedure was explained to each patient, two training blocks were conducted immediately before the experiment to ensure that the patients had understood the task. Words were presented in uppercase letters (white against black background), in central vision (horizontal visual angle 3.0°), and for a duration of 400 ms (randomized interstimulus interval: mean 2.5 s, range 2.3 to 2.7 s). Patients were required to use a rote strategy to memorize each word; they could not use memory aids such as making rows, sentences, stories, or pictures. During the distraction task, which lasted 30 s, patients were instructed to count backward by threes, starting at a number between 81 and 99 displayed on screen. The following free-recall test lasted 90 s. Stimuli consisted of 240 semantically unrelated German nouns (word frequency, mean 75.24 per million, range 15 to 175; word length, mean 5.95 letters, range 4 to 11) [R. H. Baayen, R. Piepenbrock, H. van Rijn, CELEX Lexical Database (Linguistic Data Consortium, University of Pennsylvania, Philadelphia, 1993)]. The order of words was pseudorandomized under the constraints that (i) across subjects, each word occurred equally often within each quarter of the session and once at each list position; (ii) word length was balanced between lists; and (iii) neither semantic nor phonological similarities occurred within lists.
41. V. Gregg, in Recall and Recognition. J. Brown, Ed. (Wiley, London, 1976), pp. 183-216; B. J. Underwood, Psychol. Rev. 76, 559 (1969).
42. V. Gregg, in Recall and Recognition. J. Brown, Ed. (Wiley, London, 1976), pp. 183-216; B. J. Underwood, Psychol. Rev. 76, 559 (1969).
43. Recall rates did not differ reliably between patients with left and right seizure onset (t = 1.87, not significant), nor did they correlate (r = 0.36, not significant) or vary with block position during the course of the session [one-way ANOVA (blocks 1-6 versus 8-13 versus 15-20): F(2. 10) < 2.0, not significant]. To verify a diminished recency effect, we compared recall rates of the initial, middle, and final two words of the study list. No effect of list position occurred [F(2. 10) < 2.0, not significant).
44. M. Klee and W. Rall, J. Neurophysiol. 40, 647 (1977); M. Kutas and A. Dale, in Cognitive Neuroscience, M. D. Rugg, Ed. (MIT Press, Cambridge, MA, 1997), pp. 197-242.
45. M. Klee and W. Rall, J. Neurophysiol. 40, 647 (1977); M. Kutas and A. Dale, in Cognitive Neuroscience, M. D. Rugg, Ed. (MIT Press, Cambridge, MA, 1997), pp. 197-242.
46. The early epoch (300 to 500 ms) represents the time period of the actual onset latency delay of the hippocampal relative to the rhinal subsequent memory effect, as indicated by the onset latency estimation (Fig. 2). The late epoch (500 to 700 ms) represents the following time window with an identical duration.
47. E. Halgren, P. Baudena, G. Heit, M. Clarke, K. Marinkovic, J. Physiol. (Paris) 88, 1 (1994).
48. M. Jones-Gotman, in Epilepsy Surgery, H. O. Lüders, Ed. (Raven, New York, 1991), pp. 469-476; B. Milner, Br. Med. Bull. 27, 272 (1971).
49. M. Jones-Gotman, in Epilepsy Surgery, H. O. Lüders, Ed. (Raven, New York, 1991), pp. 469-476; B. Milner, Br. Med. Bull. 27, 272 (1971).
50. W. M. Kelley et al., Neuron 20, 927 (1998).
51. R. Akaho, Psychiat. Clin. Neurosci. 50, 61 (1996); Y. J. Chen, W. M. Kang, W. C. So, Epilepsia 37, 81 (1996); G. R. Panagopoulos, T. Thomaides, G. Tagaris, C. L. Karageorgiou, Acta Neurol. Scand. 96, 62 (1997).
52. R. Akaho, Psychiat. Clin. Neurosci. 50, 61 (1996); Y. J. Chen, W. M. Kang, W. C. So, Epilepsia 37, 81 (1996); G. R. Panagopoulos, T. Thomaides, G. Tagaris, C. L. Karageorgiou, Acta Neurol. Scand. 96, 62 (1997).
53. R. Akaho, Psychiat. Clin. Neurosci. 50, 61 (1996); Y. J. Chen, W. M. Kang, W. C. So, Epilepsia 37, 81 (1996); G. R. Panagopoulos, T. Thomaides, G. Tagaris, C. L. Karageorgiou, Acta Neurol. Scand. 96, 62 (1997).
54. The posterior parahippocampus, related to declarative memory formation (4), was not covered by electrodes in our study. Thus, there might be an additional, but distinct, ERP effect generated, However, the relation between ERPs and event-related hemodynamic responses is not well understood, [M. D. Rugg, Hum. Brain Mapp. 6, 394 (1998)].Thus, the effects recorded here may not have induced any hemodynamic net effects, or they might be too small to be detectable.
55. M. D. Rugg, C. J. C. Cox, M. C. Doyle, T. Wells, Neuropsychologia 33, 471 (1995).
56. We thank J. D. E. Gabrieli, K. Paller, M. Reuber, W. Schwarz, and especially I. Tendolkar for advice on data analyses and for comments on the manuscript. We also thank H. Urbach, who acquired the MRIs.