Paola Mandile

Characterization of transition sleep episodes in baseline EEG recordings of adult rats.

By scoring 5-s EEG epochs and calculating spectral power of consecutive EEG segments as short as 1-s, transition sleep (TS) episodes were identified in baseline recordings of adult rats. TS episodes were characterized by the abrupt appearance of theta and alpha waves within an ongoing period of slow-wave sleep (SS). They were followed by paradoxical sleep (PS) or, somewhat more frequently, by a period of wakefulness (W) that often led to an additional SS. Statistical values of the main variables of TS-->(W) and TS-->(PS) episodes are presented, together with comparable data concerning previous SS and following W or PS episodes. On the whole, TS episodes were more numerous than PS episodes, and less numerous than SS episodes. Their average duration was considerably shorter. As a consequence of the identification of TS and of brief W or PS epochs intervening within SS, the number of SS episodes was estimated to be considerably higher than previously assessed, and their average duration considerably shorter.

Trains of sleep sequences are indices of learning capacity in rats

In previous work dealing with the identification of four sleep sequences (SS-->W, SS-->PS, SS-->TS-->W and SS-->TS-->PS) in the baseline session of adult male Wistar rats [Mandile P, Vescia S, Montagnese P, Romano F, Giuditta A. Characterization of transition sleep episodes in baseline EEG recordings of adults rats, Physiol Behav 1996;60:1435-1439], we have shown that those containing an intervening episode of transition sleep (TS) strongly correlate with the number of avoidances scored the following day [Vescia S, Mandile P, Montagnese P, Romano F, Cataldo G, Cotugno M, Giuditta A. Baseline transition sleep and associated sleep episodes are related to the learning ability of rats, Physiol Behav 1996;60:1513-152]. More recently, clusters of sleep sequences (trains) separated by waking intervals longer than 60 s have been identified in the baseline session of the same rats [Piscopo S, Mandile P, Montagnese P, Cotugno M, Giuditta A, Vescia S. Identification of trains of sleep sequences in adult rats, Behav Brain Res, this volume], and distinguished in homogeneous or mixed trains according to the presence of a single sleep sequence or more than one sequence. Mixed trains have been further separated into trains containing the SS-->TS-->W sequence (+TSW trains) and trains lacking it (-TSW trains). Analysis of the distribution of variables of baseline trains (and of their sleep sequences and components) among fast learning (FL), slow learning (SL), or non-learning (NL) rats, indicates that variables of +TSW trains prevail in FL rats, while variables of -TSW trains prevail in NL rats. In addition, variables of +TSW trains correlate with the number of avoidances of the training session, while variables of -TSW trains do not significantly correlate, or show inverse correlations. Interestingly, sleep sequences such as SS-->W or SS-->TS-->W show direct or inverse correlations with avoidances depending on whether they are included in +TSW trains or in -TSW trains. The data are interpreted to suggest that the outcome of brain operations performed during a sleep sequence may selectively condition the appearance of later sequences within a time interval shorter than a given threshold. An analogous mechanism may be responsible for the aggregation of sleep components in sleep sequences.

Post-trial sleep sequences including transition sleep are involved in avoidance learning of adult rats

High resolution computerized EEG analyses, and behavioral observations were used to identify slow wave sleep (SS), paradoxical sleep (PS) and transition sleep (TS) in adult male Wistar rats exposed to a session of two-way active avoidance training. Of the four sleep sequences that could be identified, two included TS (SS-->TS-->W and SS-->TS-->PS), while the other two did not (SS-->W and SS-->PS). Comparison of post-trial sleep variables between fast learning rats (FL, reaching criterion in the training session), slow learning rats (SL, reaching criterion in the retention session the following day), and non learning rats (NL, failing to reach criterion) indicated that the total amounts of SS, TS and PS of the SS-->TS-->PS sequence was markedly higher in FL rats than in SL rats. In addition, in comparison with the corresponding baseline period, the average duration and total amount of SS and TS episodes of the SS-->TS-->PS sequence increased in FL rats, while the number of SS-->TS-->W sequences decreased. On the other hand, the average duration of SS episodes increased in the SS-->TS-->W and SS-->W sequences of SL rats, and in the SS-->W and SS-->TS-->PS sequences of NL rats. Correlative analyses between number of avoidances and post-trial sleep variables demonstrated that avoidances were directly correlated with the duration of SS episodes of the SS-->TS-->PS sequence and with the duration of TS episodes of the SS-->TS-->W sequence, but inversely correlated with the number and amount of SS episodes of the SS-->W sequence and with the duration and amount of SS episodes of the SS-->PS sequence. On the whole, the data supported the view that TS-containing sleep sequences are involved in long-term storage of novel adaptive behavior, while sleep sequences lacking TS are involved in the maintenance of innate behavioral responses.

Long-term habituation to spatial novelty modifies posttrial synchronized sleep in rats.

To assess the role of posttrial synchronized sleep in the processing of a nonassociative task, adult male Sprague-Dawley rats with chronically implanted cortical electrodes for EEG recording were exposed to a Làt-maze, and horizontal (HA; corner crossing) and vertical (VA; rearings) activities were monitored during two 10-min test trials made at a 3-h (experiment 1) or 24-h (experiment 2) interval. EEG conventional recording was taken during 3 h under baseline conditions (day 1), and following exposure to the maze (day 2), and analyzed as to the amount (a), number (n), and mean duration (d) of synchronized sleep (SS) episodes followed by wakefulness (SS-->W) or by paradoxical sleep (SS-->PS). In both experiments there was a significant intertrial decrement (long-term habituation: LTH) for horizontal activity (LTH-HA), vertical activity (LTH-VA), and emotionality (LTH-E). In experiment 1, in comparison to baseline values, the posttrial SS-->PS(a) increased, mainly for the appearance of SS-->PS episodes in the 1st h. SS-->W(a) also increased in the first h. Correlative analyses among behavioral and sleep parameters showed that SS-->PS(n) and (d) covaried positively with LTH-HA relative to the entire test, and with LTH-VA relative to the second part of the test in the third h. Negative correlations were present between SS-->PS(n) and (d), and LTH-E. In experiment 2, exposed rats showed a lower SS-->PS(n) in the first hour and an increased SS-->PS(d) in the second hour. No change was observed as to SS-->W episodes.(ABSTRACT TRUNCATED AT 250 WORDS)

Identification of trains of sleep sequences in adult rats.

In previous studies based on high resolution EEG analyses of the 7 h baseline session of 18 adult male Wistar rats [6,14], we have identified four sleep sequences initiating with slow wave sleep (SS) and terminating with waking (W) or paradoxical sleep (PS). Two of these sequences contained an intervening episode of transition sleep (TS). Several variables of these sequences (SS-->W, SS-->TS-->W, SS-->TS-->PS, and SS-->PS) were selectively correlated with the capacity of rats to learn a two-way active avoidance task the following day, and were differently distributed in fast learning, slow learning and non learning rats [21]. The temporal organization of different sleep components in sequences suggested that a comparable temporal organization might concern the different sleep sequences, albeit on a longer time scale. We have now used waking periods longer than 60 s to separate clusters of baseline sleep sequences (trains) in the same rats. Trains containing the same sleep sequence (homogeneous trains) have been distinguished from trains containing different sleep sequences (mixed trains). In addition, mixed trains including the SS-->TS-->W sequence (+TSW trains) have been separated from mixed trains lacking that sequence (-TSW trains). Mixed trains of the +TSW type were longest and most numerous, while homogeneous trains were shortest and least abundant. Mixed trains of the -TSW type displayed intermediate values. Several variables of sleep sequences and sleep components differed within mixed trains and among mixed and homogeneous trains. The data indicate that baseline sleep sequences aggregate in relatively long strings in a non random fashion. The mechanism of this association is discussed.

Waking EEG power spectra in the rat: correlations with training performance

Adult rats chronically implanted with supradural electrodes were telemetrically EEG recorded during a baseline session, a training session for a two-way active avoidance task, and a retention session. Rats were assigned to a fast learning (FL), slow learning (SL) and non learning (NL) group if they achieved criterion during the training session, the retention session, or in neither session. High-resolution EEG analyses indicated that intergroup differences were present in the low frequency range of waking baseline power spectra. Moreover, baseline delta emissions directly correlated with freezings, and inversely correlated with avoidances, while emissions at 7-10 Hz directly correlated with avoidances and inversely correlated with freezings. Interestingly, during the first training period, waking delta emission selectively increased in FL rats in concomitance with a marked performance improvement; instead, SL and NL rats displayed increments at 7-9 Hz. In addition, freezings scored during the first two training periods directly correlated with post-training waking emission at 2 Hz, and inversely correlated with emission at 7-10 Hz. Conversely, escapes and avoidances directly correlated with waking emission at 7-10 Hz. The data indicate that (i) waking baseline power spectra differ among behavioral groups, and correlate with behavioral performance the following day; (ii) selective modifications of waking power spectra occur in each behavioral group during training; and (iii) behavioral responses during training correlate with post-training waking power spectra. Notably, the delta increment selectively occurring in training FL rats is assumed to reflect online memory processing leading to better performance. The latter observation supports the primary involvement of delta waves in learning.

Post-Trial Sleep in Old Rats Trained for a Two-Way Active Avoidance Task

Nine male Wistar rats aged 27 months were trained for a two-way active avoidance task and tested for retention the following day. At variance with young adult rats, most of which succeed in mastering the task, all old rats displayed a large majority of freezing responses throughout the training and the retention sessions, thereby confirming the condition of learning impairment of aged rats. Comparison of baseline and post-trial sleep indicated the presence of a transient, but marked, increment in the average duration and total amount of post-trial slow-wave sleep followed by waking, and of a decrease in total amount of quiet waking. On the other hand, variables of paradoxical sleep and of slow-wave sleep followed by paradoxical sleep or by transition sleep did not show significant variations. Because these sleep variables are known to undergo significant variations in learning in young adult rats, the present data confirm that the latter effects are related to memory-processing events rather than to nonspecific effects of training. An additional outcome of training consisted in a marked post-trial decrement in the number of spike-wave discharges, which are known to occur in old rats during periods of quiet waking.

Training old rats selectively modulates synaptosomal protein synthesis

We have previously shown that the local synthesis of two synaptic proteins of 66.5‐kDa and 87.6‐kDa is selectively enhanced in male adult rats trained for a two‐way active avoidance task. We report here that a comparable but not identical response occurs in 2‐year‐old male rats trained for the same task. In the latter age group, the local synthesis of the 66.5‐kDa protein markedly increases in cerebral cortex, brainstem, and cerebellum, with a somewhat lower increment in synthesis of the 87.6‐kDa protein. On the other hand, the newly synthesized 87.6‐kDa protein correlates with avoidances and escapes and inversely correlates with freezings in cerebral cortex and brainstem, whereas the correlations of the newly synthesized 66.5‐kDa protein remain below significance. These correlative patterns are sharply at variance with those present in trained adult rats. Our data confirm that the local system of synaptic protein synthesis is selectively modulated by training and show that the synaptic response of old rats differs from that of adult rats as reflected in behavioral responses.