Carryover effects associated with the single-trial passive avoidance learning task in the young chick

The single-trial passive avoidance task is a useful procedure for examining learning and memory in the young chick. However, it has recently been suggested that discrepant results reported by different laboratories are due to differences in training procedure. The present study investigated a number of parameters surrounding the passive avoidance task, using day-old White Leghorn, Black Australorp cockerels. The results suggested that presentation of a water-dipped bead immediately after the aversive bead significantly altered retention levels. In addition, when the water-dipped bead was presented after the aversive bead, chicks failed to discriminate between beads for a period of 10 min following exposure to the aversant experience. A novel variant of the passive avoidance procedure, involving pretraining with a water-dipped red bead, training with an aversant-coated red bead, and testing with a dry red bead, was evaluated. A measure of avoidance was calculated using all three trials. It is suggested that the use of a single bead, measured both before and after the training experience and using both aversant- and water-trained controls, results in the most concise characterization of memory-related phenomena in the chick which is not contaminated by a carryover effect from the aversive training experience to the nonaversive bead.     

Inhibition of monoADP-ribosylation prevents long-term memory consolidation of a single-trial passive avoidance task in the day-old chick

The cytosolic posttranslational protein-modifying mechanism of monoADP-ribosylation has been implicated in long-term potentiation, a synaptic model of memory formation. The current study investigated the effect of inhibiting mono(ADP-ribosyl) transferase on memory for the passive avoidance task in day-old chicks (white Leghorn-black Australorp). Various doses of novobiocin or menadione sodium bisulfite were administered intracranially at different times before or after training. Control chicks were administered saline at matched times. Novobiocin (650 microM) or menadione sodium bisulfite (250 microM) administered between 5.0 min pretraining and 2.5 min posttraining was found to cause a persistent loss of retention from 120 min posttraining. These data provide the first demonstration that monoADP-ribosylation is required for the maintenance of long-term memory. Furthermore, the temporal characteristics of the memory loss caused by monoADP-ribosylation inhibition appears to exclude this mechanism as a downstream effect of the well-established nitric oxide activity previously shown to occur within 40 min of passive avoidance training.     

D-Lactate inhibition of memory in a single trial discrimination avoidance task in the young chick

L-Lactate is a metabolite possibly able to meet some neuronal energy demands. However, a clear role for L-lactate in behaviour remains elusive. Administration of the inactive isomer D-lactate (1.75 mM; ic), immediately post-training, resulted in a persistent retention loss from 40 min post-training when used in conjuction with a single trial discrimination avoidance task designed for the young chick. Furthermore, 1mM noradrenaline (ic) administered 20 min post-training overcame the retention loss induced by D-lactate. Although not directly demonstrated in the current study, it is plausible that D-lactate inhibited memory processing by competing with L-lactate for uptake into neurons. The time of onset of the retention loss induced by D-lactate is in accord with findings where the action of noradrenaline is inhibited. The successful challenge of D-lactate inhibition by a high concentration of noradrenaline may suggest a relationship by some unidentified mechanism.     

Inhibition of endogenous carbon monoxide production induces transient retention losses in the day-old chick when trained using a single trial passive avoidance learning task

Carbon monoxide (CO) is most often thought of as an exogenous toxin rather than as a possible endogenous nootrope. However, a limited number of studies have suggested that CO is necessary in memory processing for at least some tasks. While nitric oxide (NO) and CO are known activators of guanylyl cyclase (GC), only the effect of NO on GC has been extensively investigated as a mechanism underlying memory processing. The aim of the present study was to determine if inhibition of CO production would have an effect on memory processing. Using chicks trained on a single trial passive avoidance task, inhibition of CO production using zinc (II) deuteroporphyrin IX 2,4-bis ethylene glycol (ZnBG; 5 microM) resulted in two transient retention losses occurring at around 40 and 130 min post-training. The timing of these transient retention losses was similar to those observed following inhibition of GC, using the same species and task in a previous study. This supports the notion that CO is necessary in memory processing for this task and may act through a GC-dependent mechanism. As ZnBG also directly inhibits GC or nitric oxide synthase (NOS) at high concentrations, a second experiment was carried-out to confirm the specificity of ZnBG for heme oxygenase (HO) at the concentration used. The action of ZnBG was challenged with the HO agonist hemin (100 microM) and the transient deficits were abolished. This confirmed that the action of ZnBG on memory was through a CO-related mechanism rather than directly on GC or NOS. In this way the specificity of ZnBG (5 microM) for HO could be confirmed. The results support a role for endogenous CO in memory processing, possibly through activation of GC. In addition, the transient retention losses observed following administration of ZnBG suggest that CO may be necessary for memory retrieval and not formation as previously thought.     

Exposure to a rhythmic auditory stimulus facilitates memory formation for the passive avoidance task in the day-old chick.

Previous research regarding the beneficial effects of auditory stimuli on learning and memory in humans has been inconsistent. In the current study, day-old chicks were used to reduce the impact of individual differences on responses. Chicks were trained on a passive avoidance task and exposed to various auditory stimuli. Exposure to a complex rhythmic sequence for 1 min strongly facilitated chicks' long-term memory. The optimal time of presentation of the stimulus was between 10 min before and 20 min after training. Moreover, the enhancing effect was not generalized to the other auditory stimuli tested. It is suggested that this effect may be due to arousal because arousal hormones are critical to long-term memory formation. This study indicates that the temporal characteristics and type of stimulus may be important considerations when investigating the effects of auditory stimuli on cognitive functioning.     

A scavenger of peroxynitrite prevents long-term memory formation using a single trial passive avoidance task for the day-old chick

The important role of nitric oxide (NO) in memory processing has been recognised for some time. However, the mechanisms through which NO may act are only partially understood. One highly reactive radical brought about by the reaction of NO and superoxide ions is peroxynitrite. The current study investigated the effect of peroxynitrite scavenging on retention for a single trial passive avoidance task developed for the day-old chick. Administration of a range of concentrations of the peroxynitrite scavenger Trolox (0.1 microM-1.2 mM) yielded a bimodal retention curve. This dose-response curve had nadirs at 300 and 800 microM. A time of administration study was conducted for each optimal concentration of Trolox and in both studies, the effective range of administration times extended from at least 10 min before training to 20 min post-training. Finally, a retention function was conducted for each optimum concentration of Trolox and in both studies a persistent retention loss was observed from 40 min post-training until the conclusion of the experiment 24 h post-training. The findings suggest that physiological levels of peroxynitrite may be required for the consolidation of long-term memory in this model of memory formation. Interestingly, the effective times of administration and time of retention loss onset are consistent with previous studies which blocked NO synthesis. Therefore it may be suggested that NO acts to facilitate long-term memory formation through the production of peroxynitrite.     

Inhibition of guanylate cyclase and protein kinase G impairs retention for the passive avoidance task in the day-old chick

Nitric oxide (NO) is a highly labile chemical messenger which has previously been implicated in memory processes in a variety of learning paradigms and species. However, there is only limited evidence to suggest which enzymes are acted upon by NO during the formation of memory. The present study investigates the role of guanylate cyclase (GC) and protein kinase G (PKG) in a form of passive avoidance learning known to be dependent on nitric oxide activity. It was determined that in vivo pharmacological inhibition of GC using either 1H-[1,2,4]oxadiazolo[4,3,-a]quinoxalin-1-one or 6-anilino-5,8-quinolinedione resulted in two transitory memory retention deficits centred around 40 and 120 min posttraining, respectively. In contrast, inhibition of PKG with N-[2-(methylamino)ehtyl]-5-isoquinoline-sulfornamide hydrochloride (H-8) resulted in a single temporary retention loss centered at 120 min posttraining. These temporary retention losses appear to be specific to memory since they were dose-dependent and could not be explained by nonspecific performance effects. Further, these results suggest that these agents inhibit memory retrieval rather than formation, since memory is subsequently available. The current findings indicate that guanylyl cyclase mediates two memory retrieval processes, the latter of which appears to be PKG-dependent. In contrast, since inhibition of NO results in a permanent retention loss, it is suggested that NO is required for memory formation through GC-independent processes.     

Intracerebroventricular effects of angiotensin II on a step-through passive avoidance task in rats

A wealth of evidence indicates that angiotensin II (Ang II) is involved in learning and memory. However, the precise role of this peptide in these cognitive processes is still controversial, with data indicating either an inhibitory or an enhancing action. The present study was designed to further investigate the effects of intracerebroventricular injections of Ang II (0.5, 1 or 3nmol/5microl) on a step-through passive avoidance task in male adult Wistar rats. When administered pretraining, Ang II did not affect the acquisition of passive avoidance, but markedly improved avoidance performance when given before the retrieval test. The latter effect was observed in retest sessions performed up to 72h after training. Administration of the peptide five minutes after training impaired retention of inhibitory avoidance. Therefore, Ang II may exert opposite effects on passive avoidance memory according to its interference with brain mechanisms leading to the storage or retrieval of this aversively motivated task.     

Reward dominance and passive avoidance learning in adolescent psychopaths

This study tests predictions that adolescent psychopaths are hyperresponsive to rewards (Quay, 1988) and deficient in passive avoidance learning (Newman & Kosson, 1986). Forty male adolescent juvenile offenders were divided into psychopaths and nonpsychopaths using cluster analysis. Subjects were administered a passive avoidance learning task which required learning when to respond to cards associated with either reward or punishment. Results showed a greater responsivity to reward in psychopaths, with no group differences in passive avoidance errors. Results lend support to the view that psychopaths tend to focus on the prospect of reward under conditions of mixed incentives and, when sufficiently motivated, are capable of improved performance. Together with findings of recent psychophysiological studies, these results suggest that adolescent psychopaths may have latent abilities which could have treatment implications.The authors are greatly indebted to the boys and staff of the testing institution for their kind cooperation in this study. Thanks are also due to Dr. Rand Wilcox for statistical consultation and Cheryl Eurton and Marni Ayers for assistance in data coding.     

Fox urine as an aversive stimulus: modification of a passive avoidance task

Predator urine, specifically fox urine, is a noxious but harmless olfactory stimulus. The results of previous studies have shown that fox urine is aversive to rats, and that rats react to fox urine in a similar manner as to other psychostressors. In the present study, the authors further investigated the use of fox urine as an aversive or stressful stimulus, specifically examining behavior change in open-field place-preference task. Three methods of presenting the fox urine were examined. Results indicated that fox urine decreased behavior, especially locomotion, during both fox-urine presentation and during a post-fox-urine recovery session. Data suggested that (a) there were fewer ambulatory episodes and less distance was traveled during the presentation of fox urine, regardless of presentation method, and (b) there were fewer vertical movements during fox-urine presentation when a fox-urine-laced cotton ball was set in the wood shavings than when it was placed on a bare floor or in a cup. The data suggested that fox urine may be an effective but nonharmful stimulus alternative for use in avoidance tasks.     

Predictability as a task demand in single-trial free recall

In a series of five single-trial free recall experiments it was demonstrated how manipulations of predictability in a list learning task caused reliable effects on the recency portions of the nominal serial position curve. Predictability was defined as knowledge of when the next item in the list should appear ( interval predictability) and knowledge of when the list should end and thus when recall could start ( signal predictability). Predictability was manipulated by varying the inter-item intervals within a list according to different "encoding functions", e.g. a successive increase (Condition I ) or decrease (Condition D ) of the inter-item intervals. Predictability was also manipulated by means of post-list recall signals. The data obtained show, that depending on how the interval and the signal predictabilities were manipulated, either Condition I or Condition D lists could be made more beneficial to the recall of recency items than lists with constant inter-item intervals (Condition C ). Previous encoding, storage and retrieval models were found not to give satisfactory accounts of the obtained recency effects. Neither could any traditional rehearsal model explain the data. Instead it is proposed that the predictability of stimuli in a list learning task explains how changes in recall of recency items come about. It was also hypothesized that the temporal demands, afforded to the subjects by the different encoding functions, explained the obtained output order variations.     

Defensive copers show a deficit in passive avoidance learning on Newman's go/no-go task: implications for self-deception and socialization

The present study investigated whether passive avoidance learning was retarded by defensive coping strategies designed to minimize exposure to negatively valenced stimuli. High-anxious individuals, low-anxious individuals, and defensive copers completed a computerized go/no-go task, in which they learned when to press or not to press a button, in response to contingent positive and negative feedback. The duration that feedback remained onscreen was self-regulated. Defensive copers showed preferential reflection away from negative feedback, committed more passive-avoidance errors, and were characterized by impaired learning, overall. Further, the ratio of reflection on negative feedback to reflection on positive feedback directly mediated both passive-avoidance errors and overall learning. Defensive coping strategies, therefore, appear to interfere with passive avoidance learning, thereby fostering perseverative, dysfunctional action patterns by reducing knowledge gained from previous mistakes. Implications for the learning of effective socialization strategies, and for psychopathy-which is commonly characterized by similar passive-avoidance deficits-are subsequently considered.     

Stimulus selection in passive avoidance learning and retention: weanling, periadolescent, and young adult rats

Periadolescent rats exhibit a number of behavioral differences in comparison with younger or older animals. For instance, periadolescents tend to show enhanced acquisition of simple active avoidance tasks, but impaired acquisition of more complex appetitive and aversive discriminations. In this experiment, rats were trained on a simple passive avoidance task at one of three ages, as weanlings (25 days), periadolescents (35 days), or young adults (45 days). Training occurred in the presence of both a redundant discriminative stimulus and a specified, redundant contextual stimulus. The periadolescents did not differ from either younger or older rats in rate of learning the passive avoidance task. The retention performance of these animals was then tested following a change in either, neither, or both of the redundant cues. When a measure of performance that controls for baseline activity was used, it was observed that periadolescents were not disrupted by a change in the redundant discriminative stimulus, a cue change that clearly disrupted performance in 25- and 45-day-old animals, and tended to be more disrupted by the contextual change than younger or older rats. It is hypothesized that the alterations in performance exhibited by periadolescents may be related to an ontogenetic alteration in stimulus selection modulated by the catecholaminergic systems.     

Vasopressin/oxytocin-related peptides influence long-term memory of a passive avoidance task in the cuttlefish,Sepia officinalis

The vasopressin (VP)/oxytocin (OT)-related peptides constitute a large superfamily found in a wide range of both vertebrate and invertebrate species. While intensive literature reports that these neuropeptides influence behavior, especially learning and memory, in numerous species from diverse vertebrate groups, their roles in behavioral regulation have never been studied in invertebrates. Here, we investigated the role of two VP/OT superfamily peptides, octopressin (OP) and cephalotocin (CT), on long-term memory (LTM) formation of a passive avoidance task in a cephalopod mollusc, the cuttlefish, Sepia officinalis. Subadult cuttlefish were intravenously injected, in a dose range of 3–60 μg/kg, 1 h after the training phase (consolidation design); retention performance was tested 24 h post-training. We found that administration of OP at low dose (3 μg/kg) enhanced LTM, whereas a dose of 60 μg/kg attenuated it. No effect of OP on LTM was observed for the 15 μg/kg dose. Conversely, an enhancement of retention performance was observed at all doses of CT tested. This study is the first to demonstrate the behavioral effects of VP/OT superfamily peptides in an invertebrate species. The valuable role of VP/OT-like peptides on memory processes offers new evolutionary perspectives on peptidergic transmission and neuromodulation.     

Reversible disconnection of the hippocampal-prelimbic cortical circuit impairs spatial learning but not passive avoidance learning in rats

Wistar rats, treated with the GABA(A) receptor agonist muscimol, were used to investigate the role of the hippocampal-prelimbic cortical (Hip-PLC) circuit in spatial learning in the Morris water maze task, and in passive avoidance learning in the step-through task. In the water maze task, animals were trained for three consecutive days and tested 24 h after the end of training. In the step-through task, the animals were trained once and tested 24h after training. On the training days, daily infusion of muscimol (0.5 microg/0.25 microl) was given (1) bilaterally to the ventral hippocampus (vHip), (2) bilaterally to the prelimbic cortex (PLC), (3) to the unilateral vHip and the ipsilateral PLC, or (4) for disconnecting the Hip-PLC circuit, to both the unilateral vHip and the contralateral PLC 30 min before training. The results showed that inhibition of the vHip resulted in disruption of performance in both tasks. Inhibition of the PLC produced impaired water maze performance, but had no effect on the step-through task. Disconnection of the Hip-PLC circuit produced similar effects to PLC inhibition. However, simultaneous inhibition of the unilateral vHip and the ipsilateral PLC had little effect on performance of the water maze task. The results suggested that spatial learning depends on the Hip-PLC circuit, whereas passive avoidance learning is independent of this circuit.     

Reaction to punishment, reflectivity, and passive avoidance learning in extraverts

Passive avoidance learning occupies a central role in accounts of disinhibited behavior, ranging from psychopaths' persistent criminality (Hare 1970) to extraverts' gregariousness (Gray, 1972). To explore the mechanism underlying passive avoidance deficits, we assessed the relation of extraversion, neuroticism, and response latency after punishment to passive avoidance learning by using two successive go/no go discrimination tasks. The tasks were designed to examine two aspects of subjects' reactions to punishment: response speed on trials immediately following punishment (Experiment 1) and time to terminate punishment feedback between successive trials (i.e., reflectivity; Experiment 2). Consistent with previous findings, the results of Experiment 1 showed that extraverts commit more passive avoidance errors than introverts do (Newman, Widom, & Nathan, 1985) and fail to pause following punished errors (Nichols & Newman, 1986). In Experiment 2, only neurotic extraverts displayed this pattern of performance differences. In both experiments, longer pausing following punishment predicted better learning from punishment for both introverts and extraverts. These results suggest that, in the presence of salient cues for reward, extraverts' characteristic reaction to punishment interferes with processing punished errors and may contribute to their more general propensity for impulsive, nonreflective action.     

Gap junctions and memory: An investigation using a single trial discrimination avoidance task for the neonate chick

Gap junctions are important to how the brain functions but are relatively under-investigated with respect to their contribution towards behaviour. In the present study a single trial discrimination avoidance task was used to investigate the effect of the gap junction inhibitor 18-α-glycyrrhetinic acid (αGA) on retention. Past studies within our research group have implied a potential role for gap junctions during the short-term memory (STM) stage which decays by 15 min post-training. A retention function study comparing 10 μM αGA and vehicle given immediately post-training demonstrated a significant main effect for drug with retention loss at all times of test (10–180 min post-training). Given that the most common gap junction in the brain is that forming the astrocytic network it is reasonable to conclude that αGA was acting upon these. To confirm this finding and interpretation two additional investigations were undertaken using endothelin-1 (ET-1) and ET-1 + tolbutamide. Importantly, a retention function study using 10 nM ET-1 replicated the retention loss observed for αGA. In order to confirm that ET-1 was acting on astrocytic gap junctions the amnestic action of ET-1 was effectively challenged with increasing concentrations of tolbutamide. The present findings suggest that astrocytic gap junctions are important for memory processing.