Elsevier

Behavioural Brain Research

Volume 159, Issue 1, 15 April 2005, Pages 105-111
Behavioural Brain Research

Research report
Noradrenaline involvement in the memory-enhancing effects of exposure to a complex rhythm stimulus following discriminated passive avoidance training in the young chick

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Abstract

Previous research in our laboratory has demonstrated a significant memory-enhancing effect of exposure to a complex rhythm stimulus following weakly-reinforced passive avoidance learning in chicks. The aim of this study was to explore whether noradrenaline mediates this process. Chicks were trained on a strongly-reinforced single-trial passive avoidance task involving discrimination between two coloured beads. Intracerebral administration of the protein synthesis blocker, anisomycin, revealed that a phase of memory formation sensitive to arousal levels was extended by approximately 35 min following exposure to the complex rhythm stimulus. Administration of 2,4-dinitrophenol showed that this extension occurred during phase B of intermediate-term memory. Finally, a higher dose of the β-adrenergic receptor antagonist, propranolol, was required to inhibit long-term memory in the presence of the auditory stimulus than in its absence. These findings suggest that the memory-enhancing effects of the complex rhythm stimulus may be mediated by noradrenaline, possibly via an increase in physiological arousal.

Introduction

There is some evidence that exposure to rhythmic auditory stimuli may increase physiological arousal [9], [24], [29] as well as enhance learning (see [23]). Moreover, an increase in physiological arousal has been proposed to account for the facilitation of various aspects of cognition by auditory stimuli [8], [28], [36]. It can be speculated, therefore, that previous findings in our laboratory showing a strong memory-enhancing effect of exposure to a complex rhythm stimulus (CRS) following weakly-reinforced passive avoidance training (see [38], [39]), may be attributable to changes in arousal, which in this context is taken to encapsulate changes in the release of stress-related hormones. This proposition is consistent with research that has shown long-term memory (LTM) consolidation in weakly-reinforced chicks, following the administration of arousal- or stress-related hormones, such as corticosterone [14], [35] and noradrenaline [5].

The Gibbs and Ng [13], three-stage memory model provides an ideal paradigm with which to determine whether the memory-enhancing effects of exposure to the CRS are mediated by arousal- or stress-related hormones. One hormone of particular interest in the current context is noradrenaline (NA), which has been shown to be involved in the formation of relatively permanent memory [4]. According to this model, the memory trace is delineated by retention deficits 15 and 55 min post-training and is comprised of short-term memory, labile or intermediate-term memory (ITM) (divided into phases A and B), and LTM. These stages are thought to be sequentially linked such that consolidation of the learning task into LTM is dependent upon the appearance of ITM phase B (ITMB), which extends from 30 to 55 min after strongly-reinforced training [32].

The initiation of ITMB appears to be dependent upon the state of arousal around the time of training, which is determined, at least in part, by the strength of the training stimulus [2], [11]. However, changes in levels of NA alter the temporal parameters of the memory trace, irrespective of the strength of reinforcement [16]. That is, the duration of ITM is moderated by stress (such as isolation) and/or administration of hormones [2], [7], [16], [20], [34]. For example, Gibbs and colleagues [4], [14], [31] found that subcutaneous administration of corticosterone (CS), adrenocorticotropic hormone (ACTH) or noradrenaline immediately after strongly-reinforced training, delayed the onset of LTM for the passive avoidance task by 25 min, such that the second retention deficit occurred at 80 min post-training.

The aim of the experiments reported here was to establish whether exposure to a CRS produces effects similar to those observed when memory is modulated by hormones that are associated with arousal or stress such as NA. The involvement of such hormones can be inferred by an extended duration of ITM in chicks trained using a strongly-reinforced version of the single-trial passive avoidance task. Previously, memory enhancement following exposure to the CRS has been demonstrated using a weak dilution of methylanthranilate (MeA) (see [38], [39]). However, ITMB is not observed in chicks that have been given weakly-reinforced training [3], [4], [11]. Rather, memory tends to be present for only a short period after training, unless chicks are administered hormones, such as NA and ACTH [4]. To explore the temporal parameters of ITM, therefore, strongly-reinforced training, which generates a permanent memory trace, was used.

Section snippets

Subjects

One to two-day-old White Leghorn cross Black-Australorp cockerels were used in all experiments and were obtained on the morning of each experimental day from a local hatchery (Research Poultry Farm, Vic., Australia).

Drugs

Anisomycin (ANI), a well-known protein-synthesis inhibitor [12], was bilaterally injected at a dose of 38 nmol/hem (3.8 mM concentration) [13] immediately after training. The pharmacological agent, 2,4-dinitrophenol (DNP) inhibits oxidative metabolism and was administered at a dose of

Experiment 1: extension of intermediate memory following exposure to the complex rhythm stimulus

In the Gibbs and Ng [13] model, the protein synthesis dependent LTM stage is expressed by 60 min post-training, with ANI inducing retention loss beginning at 55 min post-training. It is argued, therefore, that the ITM stage lasts until 50 min post-training, with the transition to the LTM stage occurring at around 55 min. As mentioned previously, hormones such as NA, ACTH and CS extend the duration of ITM until around 80–90 min following training [15]. If the CRS promotes retention through the

Experiment 2: extension of phase B of the intermediate memory stage following exposure to the complex rhythm stimulus

The two phases of ITM can be differentiated on the basis that the formation and maintenance of ITMA can be disrupted by intracranial injections of the inhibitor of oxidative phosphorylation, DNP [2], [16], [30]. The maintenance of ITMA is dependent upon oxidative metabolism and is impaired within 10 min of DNP administration, given between 5 and 25 min post-training, but not after 25 min [15], [32]. If the duration of ITMA is extended, however, the time window during which DNP can be administered

Experiment 3: noradrenaline involvement in the extension of intermediate memory, phase B, following exposure to the complex rhythm stimulus

The permanence of a memory trace is largely determined by the state of arousal around the time of learning [5], [10], [22]. Experiments 1 and 2 have shown that exposure to the CRS is likely to promote memory by increasing arousal levels in the chick. However, these data do not differentiate between the various arousal/stress hormones. There is good reason to believe that NA is the most likely candidate for this role. NA is released in the brain and has been shown to be essential for the

General discussion

The findings presented in this study suggest that the memory-enhancing effects of exposure to the CRS may be mediated by NA. Support for this proposition is three-fold. First, it was shown that the duration of ITM, following exposure to the CRS, was extended to at least 90 min post-training. Past research (see [16]) has shown that an extension of ITM typically occurs with administration of exogenous hormones.

Second, the effective times of administration of the metabolic inhibitor DNP were the

Acknowledgments

We would like to gratefully acknowledge the support received from the Monash University Postgraduate Publications Award and the laboratory assistance of Dr. Tom Edwards.

References (39)

  • M.E. Gibbs et al.

    Enhancement of memory consolidation in chicks by beta(3)-adrenoceptor agonists

    Eur J Pharmacol

    (2001)
  • M.E. Gibbs et al.

    Role of adrenoceptor subtypes in memory consolidation

    Prog Neurobiol

    (2002)
  • M.E. Gibbs et al.

    Alpha 2-adrenoceptors in the basal ganglia have a role in memory consolidation and reinforcement

    Neuropharmacology

    (2003)
  • M. Kossut et al.

    Differential 2-deoxyglucose uptake into chick brain structures during passive avoidance training

    Neuroscience

    (1984)
  • M.R. Rosenzweig et al.

    Short-term, intermediate-term, and long-term memories

    Behav Brain Res

    (1993)
  • C. Sandi et al.

    Corticosterone enhances long-term retention in one-day-old chicks trained in a weak passive avoidance learning paradigm

    Brain Res

    (1994)
  • R.J. Andrew

    The chick in experiment: techniques and tests

  • S.F. Crowe et al.

    Memory consolidation of weak training experiences by hormonal treatments

    Pharmacol Biochem Behav.

    (1990)
  • N.A. Foster et al.

    The effect of concurrent music on autobiographical recall in dementia clients

    Music Sci

    (1998)
  • Cited by (0)

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