Activation of phasic pontine-wave generator prevents rapid eye movement sleep deprivation-induced learning impairment in the rat: A mechanism for sleep-dependent plasticity

被引:126
作者
Datta, S
Mavanji, V
Ulloor, J
Patterson, EH
机构
[1] Boston Univ, Sch Med, Dept Psychiat, Sleep Res Lab, Boston, MA 02118 USA
[2] Boston Univ, Sch Med, Program Behav Neurosci, Boston, MA 02118 USA
关键词
pontine wave; learning and memory; REM sleep; plasticity; carbachol; brainstem; locus subcoeruleus; rat; two-way active avoidance; consolidation;
D O I
10.1523/JNEUROSCI.4111-03.2004
中图分类号
Q189 [神经科学];
学科分类号
071006 ;
摘要
Animal and human studies of sleep and learning have demonstrated that training on various tasks increases subsequent rapid eye movement (REM) sleep and phasic pontine-wave (P-wave) activity, followed by improvement in performance on the learned task. It is well documented that REM sleep deprivation after learning trials blocks the expected improvement in performance on subsequent retesting. Our aim was to test whether experimentally induced P-wave generator activation could eliminate the learning impairment produced by post-training REM sleep deprivation. Rats were trained on a two-way active avoidance-learning task. Immediately thereafter, two groups of those rats received a control vehicle (100 nl saline) microinjection and one group received a carbachol ( 50 ng in 100 nl saline) microinjection into the P-wave generator. The carbachol-injected group and one of the two control saline microinjected groups were selectively deprived of REM sleep during a 6 hr polygraphic recording session. All rats were then tested on the avoidance-learning task. The rats that received both the control saline injection and REM sleep deprivation showed learning deficits compared with the control saline-injected rats that were allowed to sleep normally. In contrast, the rats that received the carbachol microinjection and REM sleep deprivation demonstrated normal learning. These results demonstrate, for the first time, that carbachol-induced activation of the P-wave generator prevents the memory-impairing effects of post-training REM sleep deprivation. This evidence supports our hypothesis that the activation of the P-wave generator during REM sleep deprivation enhances a physiological process of memory, which occurs naturally during post-training REM sleep.
引用
收藏
页码:1416 / 1427
页数:12
相关论文
共 105 条
[71]   CORRELATION BETWEEN THRESHOLD TO INDUCE LONG-TERM POTENTIATION IN THE HIPPOCAMPUS AND PERFORMANCE IN A SHUTTLE BOX AVOIDANCE-RESPONSE IN RATS [J].
RAMIREZ, OA ;
CARRER, HF .
NEUROSCIENCE LETTERS, 1989, 104 (1-2) :152-156
[72]   SLEEP-DEPRIVATION IN THE RAT BY THE DISK-OVER-WATER METHOD [J].
RECHTSCHAFFEN, A ;
BERGMANN, BM .
BEHAVIOURAL BRAIN RESEARCH, 1995, 69 (1-2) :55-63
[73]   Effects of method, duration, and sleep stage on rebounds from sleep deprivation in the rat [J].
Rechtschaffen, A ;
Bergman, BM ;
Gilliland, MA ;
Bauer, K .
SLEEP, 1999, 22 (01) :11-31
[74]  
RECHTSCHAFFEN A, 1989, SLEEP, V12, P68
[75]  
RempelClower NL, 1996, J NEUROSCI, V16, P5233
[76]   Brain gene expression during REM sleep depends on prior waking experience [J].
Ribeiro, S ;
Goyal, V ;
Mello, CV ;
Pavlides, C .
LEARNING & MEMORY, 1999, 6 (05) :500-508
[77]   Induction of hippocampal long-term potentiation during waking leads to increased extrahippocampal zif-268 expression during ensuing rapid-eye-movement sleep [J].
Ribeiro, S ;
Mello, CV ;
Velho, T ;
Gardner, TJ ;
Jarvis, ED ;
Pavlides, C .
JOURNAL OF NEUROSCIENCE, 2002, 22 (24) :10914-10923
[78]   BRAIN-STEM PGO-ON CELLS PROJECTING DIRECTLY TO THE CAT DORSAL LATERAL GENICULATE-NUCLEUS [J].
SAKAI, K ;
JOUVET, M .
BRAIN RESEARCH, 1980, 194 (02) :500-505
[79]   EFFECTS OF PONTO-MESENCEPHALIC LESIONS AND ELECTRICAL-STIMULATION UPON PGO WAVES AND EMPS IN UNANESTHETIZED CATS [J].
SAKAI, K ;
PETITJEAN, F ;
JOUVET, M .
ELECTROENCEPHALOGRAPHY AND CLINICAL NEUROPHYSIOLOGY, 1976, 41 (01) :49-63
[80]   RETICULAR STIMULATION FACILITATES RETRIEVAL OF A FORGOTTEN MAZE HABIT [J].
SARA, SJ ;
DEWEER, B ;
HARS, B .
NEUROSCIENCE LETTERS, 1980, 18 (02) :211-217