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Volumn 271, Issue 5257, 1996, Pages 1870-1873

Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; HIPPOCAMPUS; HIPPOCAMPUS THETA RHYTHM; LONG TERM POTENTIATION; MALE; MEMORY; NERVE CONDUCTION; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SLEEP; SPIKE WAVE;

EID: 0030012117     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.271.5257.1870     Document Type: Article
Times cited : (838)

References (48)
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    • The CA1 cell body layer can be recognized by several cntena, including the presence of 100- to 300-Hz "ripples" in electroencephalograms recorded from the tetrodes, "sharp waves" in the electroencephalograms that reverse polarity about 50 μm below the CA1 layer, and most importantly, the sudden appearance, at a depth about 2 mm below the dura, of large numbers of simultaneously recorded cells firing complex spikes [(9), J O'Keefe, Exp. Neurol. 51, 78 (1976), G. Buzsáki, Z. Horváth, R Unoste, J. Hetke, K Wise, Science 256, 1025 (1992); S S Suzuki and G. K. Smrth, Electroencephalogr. Clin Neurophysiol. 69, 541 (1987)]. The electrode arrays were implanted stereotaxically, under pentobarbital (Nembutal) anesthesia; all procedures were carried out in accordance with an institutionally approved animal care protocol. The CA1 layer was identified by standard electrophysiological criteria, and pyramidal cells (31 to 57 per recording session) were identified on the basis of action-potential wave forms and interspike interval histograms To be classified as a pyramidal cell, a unit was required (i) to fire at least a small number of complex spike bursts during the recording session, (ii) to be recorded simultaneously with other cells firing complex spikes, (iii) to have a spike width (peak to valley) of at least 300 μs, and (iv) to have an overall mean rate below 5 Hz during the recording session [J B. Ranck Jr., Exp. Neurol 41, 461 (1973); S Fox and J. B. Ranck Jr, Exp Brain Res. 41, 399 (1981), G. Buzsáki, L S Leung, C. H. Vanderwolf, Brain Res Rev 6, 139 (1983)].
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    • The CA1 cell body layer can be recognized by several cntena, including the presence of 100- to 300-Hz "ripples" in electroencephalograms recorded from the tetrodes, "sharp waves" in the electroencephalograms that reverse polarity about 50 μm below the CA1 layer, and most importantly, the sudden appearance, at a depth about 2 mm below the dura, of large numbers of simultaneously recorded cells firing complex spikes [(9), J O'Keefe, Exp. Neurol. 51, 78 (1976), G. Buzsáki, Z. Horváth, R Unoste, J. Hetke, K Wise, Science 256, 1025 (1992); S S Suzuki and G. K. Smrth, Electroencephalogr. Clin Neurophysiol. 69, 541 (1987)]. The electrode arrays were implanted stereotaxically, under pentobarbital (Nembutal) anesthesia; all procedures were carried out in accordance with an institutionally approved animal care protocol. The CA1 layer was identified by standard electrophysiological criteria, and pyramidal cells (31 to 57 per recording session) were identified on the basis of action-potential wave forms and interspike interval histograms To be classified as a pyramidal cell, a unit was required (i) to fire at least a small number of complex spike bursts during the recording session, (ii) to be recorded simultaneously with other cells firing complex spikes, (iii) to have a spike width (peak to valley) of at least 300 μs, and (iv) to have an overall mean rate below 5 Hz during the recording session [J B. Ranck Jr., Exp. Neurol 41, 461 (1973); S Fox and J. B. Ranck Jr, Exp Brain Res. 41, 399 (1981), G. Buzsáki, L S Leung, C. H. Vanderwolf, Brain Res Rev 6, 139 (1983)].
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    • The CA1 cell body layer can be recognized by several cntena, including the presence of 100- to 300-Hz "ripples" in electroencephalograms recorded from the tetrodes, "sharp waves" in the electroencephalograms that reverse polarity about 50 μm below the CA1 layer, and most importantly, the sudden appearance, at a depth about 2 mm below the dura, of large numbers of simultaneously recorded cells firing complex spikes [(9), J O'Keefe, Exp. Neurol. 51, 78 (1976), G. Buzsáki, Z. Horváth, R Unoste, J. Hetke, K Wise, Science 256, 1025 (1992); S S Suzuki and G. K. Smrth, Electroencephalogr. Clin Neurophysiol. 69, 541 (1987)]. The electrode arrays were implanted stereotaxically, under pentobarbital (Nembutal) anesthesia; all procedures were carried out in accordance with an institutionally approved animal care protocol. The CA1 layer was identified by standard electrophysiological criteria, and pyramidal cells (31 to 57 per recording session) were identified on the basis of action-potential wave forms and interspike interval histograms To be classified as a pyramidal cell, a unit was required (i) to fire at least a small number of complex spike bursts during the recording session, (ii) to be recorded simultaneously with other cells firing complex spikes, (iii) to have a spike width (peak to valley) of at least 300 μs, and (iv) to have an overall mean rate below 5 Hz during the recording session [J B. Ranck Jr., Exp. Neurol 41, 461 (1973); S Fox and J. B. Ranck Jr, Exp Brain Res. 41, 399 (1981), G. Buzsáki, L S Leung, C. H. Vanderwolf, Brain Res Rev 6, 139 (1983)].
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    • note
    • The rats varied in familiarity with the task, some having been trained on the same track daily for only 6 days (but extensively trained on other, similar types of apparatus), others having performed the same task daily for several weeks, always at approximately the same time of day. Three of the rats were young adults, about 9 months old, the other three were elderly, 27 to 30 months old. One of the young rats was recorded from twice, on both triangle and rectangle, 2 weeks apart, the other five rats were recorded from once each For each recording session, the rat was first placed on a small round platform near the track, and unit activity was monitored until a period of sleep lasting 30 min or more was recorded. Next, the rat was placed on the track, where it ran for food reward for 20 to 30 min. Finally, the rat was returned to the platform and recorded from for a further 30 to 60 min of sleep. During many of the sessions, the sleep periods were broken by brief intervals of drowsy wakefulness or arousal, during which place-specific firing of some units was seen on the platform, but this activity bore no apparent relation to the activity seen on the track. From each sleep session, a period of 15 min with minimal signs of arousal (that is, movement and theta activity in the EEG) was selected for analysis. It is difficult, with the information available, to distinguish clearly between SWS and a state of drowsy wakefulness. or between the physiology of these two states. The design of the study proceeded as follows Initially, a data set with a large number of cells was chosen for preliminary analyses, working out the computational and statistical techniques. Next, we performed the same analyses on six more data sets, choosing this number because seven out of seven is significant at the 0.01 level in a sign test, given an a priori probability of 0.5. The criteria were that there be a good number of cells, good behavior on the apparatus, and at least 15 min of good sleep both before and after the behavioral session These were informal critena, but the data sets were chosen before any analyses were performed on them. The data were taken from animals involved in a variety of experiments, including, for example, a study of the effects of aging on rat hippocampal activity. Every data set that was analyzed is presented in this report.
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    • note
    • ji This reversal of sign as a consequence of exchanging the cells makes the temporal bias measure quite different from a simple correlation measure of the type used by Wilson and McNaughton (8), which keeps the same value if the two cells are exchanged. To minimize the possibility of artifacts caused by shrinkage of spike amplitude when a cell is highly active, we used only pairs of cells recorded from different tetrodes in the analyses.
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    • note
    • Our main concern in this study was to establish the reality of the phenomenon in as straightforward a way as possible Therefore, we thought it preferable to avoid any manipulations of the data that were not absolutely necessary, such as rescaling or thresholding. It is likely that the relations reported here would be stronger if, for example, only pairs of cells with overlapping place fields were included
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    • note
    • As mentioned previously, we calculated the temporal bias in these analyses using a time window of ±200 ms. We also experimented with time windows of 50, 100, 500, and 1000 ms. Significant effects could be seen for some of the recording sessions with time windows of 100 and 500 ms, but they appeared to be less consistent. We also expenmented with different time windows for the sleep and track-running sessions, but again, time windows of 200 ms for both yielded the most consistent evidence for reproduction of temporal bias. During track running, a time window of 200 ms captures the relation of most pars of cells with overlapping place fields but yields zero for most pairs whose fields are more widely separated; during sleep, atime window of 200 ms captures relations that occur within individual sharp waves but rarely encompasses two consecutive sharp waves Buzsáki (5) suggested that behavioral sequences may be compressed into the time window of individual sharp waves, and Skaggs et al. (17) have shown evidence that sequences are compressed within individual theta cycles.
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    • note
    • Supported by National Institutes of Health grant AG12609, National Institute of Mental Health grant MH46823, and the McDonnell-Pew Foundation. We thank M A. Wilson for contributing in numerous ways to the analysis and C. A. Barnes, K. Moore, M Suster, R. D'Monte, K. Weaver, C Duffield, and K Stengel for assistance with data acquisition and analysis.


* 이 정보는 Elsevier사의 SCOPUS DB에서 KISTI가 분석하여 추출한 것입니다.