Pigeons (<Emphasis Type="Italic">Columba livia</Emphasis>) know when they will need hints: prospective metacognition for reference memory?

Despite their impressive cognitive abilities, avian species have shown less evidence for metacognition than mammals. We suspect that commonly used tasks such as matching to sample might be too demanding to allow metacognitive processing within birds’ working memory. Here, we examined whether pigeons could control their behavior as a function of knowledge levels on a three-item sequence learning task, a reference memory task supposedly requiring fewer working memory resources. The experiment used two types of lists differing in familiarity. One was familiar to the pigeons through repeated exposure, whereas the other was novel in every new session. In test sessions, pigeons could choose between a trial with a hint specifying the next item to peck and one with no hint. However, successful responses in trials with a hint resulted in lowered rates of primary reinforcement: .60 in the first test and .75 in the second. Results showed that two of four pigeons chose the trial with a hint significantly more often before receiving a novel list than the familiar list in the four sessions of the first test, and three did so in the second test. Impressively, one bird showed robust evidence in the very first sessions in both tests. These results suggest that pigeons may monitor their long-term knowledge states and thereby control their environment before starting to solve a task.     

Effects of short-term isolation on the locomotor activity of the angelfish (Pterophyllum scalare).

Two experiments were conducted to test in angelfish (Pterophyllum scalare) some implications of Gallup and Suarez's (1980) ethological model of open-field behavior and to differentiate between the initial locomotor effects of a novel environment and those of isolation per se. Juveniles placed alone in a novel environment initially showed increased locomotion compared with their previous level when kept as a group and with that of fish placed in the novel environment in groups of three and five. When placed alone in a novel tank, individuals that had already been isolated for 10 days moved about less than those that had been isolated for 4 days. During isolation, angelfish significantly reduced activity to a minimum after 3 to 4 days, and after 10 days the level was still lower than in the group situation. The results suggest that, in addition to birds and rodents, Gallup and Suarez's model is applicable to fish and may account for the effects of longer exposure to a novel environment.     

Rats’ novel object interaction as a measure of environmental familiarity

Environmental familiarization is a learning phenomenon embedded within most tasks used to study learning and motivation. Given its prevalence there is surprisingly little systematic behavioral research on factors affecting familiarization. The six experiments reported in the present report used rats’ tendency to interact more with a novel object in a familiar than in a novel environment as a measure of environmental familiarization. We found that 3 min of exposure to the environment was sufficient to increase object interaction above unfamiliar controls even when testing occurred up to 48 h after initial exposure to the environment; 1 or 1.5 min of exposure was not sufficient. Also, in the brief 2 min test, 10 min of environment exposure did not appear to increase object interaction above the 3-min condition. The 3-min of environment exposure was sufficient for familiarization whether environment exposure occurred in one 3 min placement or two 1.5 min placements. Environmental familiarization as measured by object interaction was also sensitive to ‘interference’ manipulations. That is, a distinct object present during initial exposure to the environment produced a level of object interaction in testing comparable to an unfamiliar control. Similarly, exposure to a second distinct alternate environment immediately after, but not before, initial exposure to the test environment partially disrupted environmental familiarization. In sum, object interaction might serve as a useful measure for studying processes mediating environmental familiarity.     

The obligatory effects of memory on eye movements

Previous work has shown that eye movement behaviour is affected by previous experience, such that alterations in viewing patterns can be observed to previously viewed compared to novel displays. The current work addresses the extent to which such effects of memory on eye movement behaviour are obligatory; that is, we examined whether prior experience could alter subsequent eye movement behaviour under a variety of testing conditions, for stimuli that varied on the nature of the prior exposure. While task demands influenced whether viewing was predominantly directed to the novel versus familiar faces, viewing of the familiar faces was distinguished from viewing of the novel faces, regardless of whether the task required incidental encoding or intentional retrieval. Changes in scanning of previously viewed over novel faces emerged early in viewing; in particular, viewing duration of the first fixation to the familiar faces was often significantly different from the duration of the first fixation directed to the novel faces, regardless of whether prior exposure was solely in the context of the experiment or due to real-world exposure. These findings suggest that representations maintained in memory may be retrieved and compared with presented information obligatorily.     

The obligatory effects of memory on eye movements

Previous work has shown that eye movement behaviour is affected by previous experience, such that alterations in viewing patterns can be observed to previously viewed compared to novel displays. The current work addresses the extent to which such effects of memory on eye movement behaviour are obligatory; that is, we examined whether prior experience could alter subsequent eye movement behaviour under a variety of testing conditions, for stimuli that varied on the nature of the prior exposure. While task demands influenced whether viewing was predominantly directed to the novel versus familiar faces, viewing of the familiar faces was distinguished from viewing of the novel faces, regardless of whether the task required incidental encoding or intentional retrieval. Changes in scanning of previously viewed over novel faces emerged early in viewing; in particular, viewing duration of the first fixation to the familiar faces was often significantly different from the duration of the first fixation directed to the novel faces, regardless of whether prior exposure was solely in the context of the experiment or due to real-world exposure. These findings suggest that representations maintained in memory may be retrieved and compared with presented information obligatorily.     

Cross-modal working memory binding and L1-L2 word learning

The ability to create temporary binding representations of information from different sources in working memory has recently been found to relate to the development of monolingual word recognition in children. The current study explored this possible relationship in an adult word-learning context. We assessed whether the relationship between cross-modal working memory binding and lexical development would be observed in the learning of associations between unfamiliar spoken words and their semantic referents, and whether it would vary across experimental conditions in first- and second-language word learning. A group of English monolinguals were recruited to learn 24 spoken disyllable Mandarin Chinese words in association with either familiar or novel objects as semantic referents. They also took a working memory task in which their ability to temporarily bind auditory-verbal and visual information was measured. Participants’ performance on this task was uniquely linked to their learning and retention of words for both novel objects and for familiar objects. This suggests that, at least for spoken language, cross-modal working memory binding might play a similar role in second language-like (i.e., learning new words for familiar objects) and in more native-like situations (i.e., learning new words for novel objects). Our findings provide new evidence for the role of cross-modal working memory binding in L1 word learning and further indicate that early stages of picture-based word learning in L2 might rely on similar cognitive processes as in L1.     

Effects of reserpine on retention of escape reversal in mice: absence of state-dependent learning.

A discriminated escape training paradigm was used to study the effects of reserpine on learning and memory in mice. Intraperitoneal injection of reserpine before reversal training had no effect on acquisition but did produced a time-and dose-dependent impairment of retention test performance 10 days later. These results suggested that reserpine may have interfered with some aspect of memory storage. Retention impairments observed when a 2.0 mg/kg reserpine injection was given 2 hr before reversal training were not attenuated by readministering the drug before testing, a finding that provides no support for a state-dependency interpretation. Furthermore, animals treated with reserpine exhibited inferior retention of previous training, regardless of the pharmacological state present during that learning. This was interpreted as a drug-induced impairment of memory retrieval. In addition, performance during the initial discriminated escape training session suggested that reserpine may also impair acquisition under some conditions. In the last experiment, it was found that when the catecholamine precursor L-dihydroxyphenylalamine (100 mg/kg) and the indole amine precursor D,L-5-hydroxytryptophan (125 mg/kg) were both given after reserpine treatment, subsequent retention performance was not significantly impaired. The results are discussed in terms of the possible roles of biogenic amines in arousal, learning, and memory.     

Simplifying environmental cues in a Morris-type water maze improves place learning in old NMRI mice.

Old virgin female NMRI mice aged 17 months were compared with mice aged 3 months for their spatial learning abilities in two versions of the Morris water maze. The first one was a simplified version with a salient configuration of cues comparable to a black/white discrimination and the second one was the classical version of the Morris test with many distal cues surrounding the maze. In the simplified version, old mice presented a slower rate of acquisition and a transient poorer retention compared to young mice. However, old mice achieved a final level of performance statistically comparable to their young counterparts as assessed by latencies to escape onto the concealed platform and by the spatial bias measured in probe trials at intervals during testing. When subsequently subjected to classical Morris maze learning, the same old animals showed marked learning deficits and were persistently impaired in their latencies to escape onto the platform. They presented no spatial bias for the location of the platform in the different probe trials. When the goal was cued at the end of the experiment, the performances of old mice rapidly improved, showing that motivation, motor disabilities, or fatigue and ability to use proximal cues cannot explain the place learning deficit. Our results were discussed in terms of cognitive versus sensory/perceptual disabilities in aged rats and mice.     

Newly learned spoken words show long-term lexical competition effects

Newly learned spoken words (e.g., “cathedruke”) become fully engaged in the mental lexicon, as measured via lexical competition with their pre-existing phonological neighbours (e.g., “cathedral”), over the course of several hours or days, and this lexical restructuring is associated with sleep (Dumay & Gaskell, 2007). Here, we investigated the longer-term effects of word learning for three sets of novel words learned at different times using phoneme monitoring and repetition tasks. The effects of these exposure sessions on lexical memory were assessed in a battery of tests. Lexical decision latencies to pre-existing neighbouring words showed that lexical competition effects for the novel words remained observable 8 months after initial exposure. Furthermore, the order-of-acquisition of the novel words affected their production speed (but not recognition speed), with an advantage for earlier acquired words. The results suggest that the consolidation of novel words results in a long-term and stable change in the lexical competition process.     

Newly learned spoken words show long-term lexical competition effects

Newly learned spoken words (e.g., “cathedruke”) become fully engaged in the mental lexicon, as measured via lexical competition with their pre-existing phonological neighbours (e.g., “cathedral”), over the course of several hours or days, and this lexical restructuring is associated with sleep (Dumay & Gaskell, 2007). Here, we investigated the longer-term effects of word learning for three sets of novel words learned at different times using phoneme monitoring and repetition tasks. The effects of these exposure sessions on lexical memory were assessed in a battery of tests. Lexical decision latencies to pre-existing neighbouring words showed that lexical competition effects for the novel words remained observable 8 months after initial exposure. Furthermore, the order-of-acquisition of the novel words affected their production speed (but not recognition speed), with an advantage for earlier acquired words. The results suggest that the consolidation of novel words results in a long-term and stable change in the lexical competition process.     

Interactive learning in the paradise fish (Macropodus opercularis): an ethological interpretation of the second-order conditioning paradigm

This study was aimed at the examination of ‘mental construction’ in paradise fish by interactive learning, which is suggested as an alternative hypothesis for backward or second-order conditioning. Avoidance of goldfish was established in paradise fish by presenting a harmless goldfish (a novel stimulus) after an aversive event (mild electric shocks) in the dark compartment of a shuttle tank. It was found that this avoidance depended on context pre-exposure. Experiment 1 was designed to study the effect of mild shocks on shuttling activity in a familiar context. Experiment 2 aimed at establishing fear-conditioning to the goldfish in a higher-order conditioning paradigm. In the course of training, unpaired stimuli were presented in the dark compartment of the shuttle tank in such a manner that the presentation of mild shocks (20 mA) preceded the encounter with a harmless fish (goldfish). Experiment 3 demonstrated the role of context pre-exposure in interactive learning. Results indicate that (1) while 60 mA shocks resulted in avoidance of the dark compartment, the 20 mA mild shocks affected exploratory behaviour; (2) after pre-exposure to the training environment, paradise fish avoided the dark compartment containing goldfish provided that subjects had previously encountered mild, explorative shocks there; (3) this conditioned fear, a ‘mental construction’ of a potential danger, was proved to be transferable to another context and was consequently aimed specifically at the goldfish, a living being, rather than the training context; (4) the pre-exposure to the shuttle tank was an important part of this training procedure, that is, only subjects habituated to the shuttle tank avoided the goldfish. Results are discussed in the framework of the Interactive Learning Hypothesis, which has been developed as an ethological approach to a higher-order conditioning paradigm. Received: 15 January 1999 / Accepted after revision: 18 August 1999     

Is the map in our head oriented north?

We examined how a highly familiar environmental space--one's city of residence--is represented in memory. Twenty-six participants faced a photo-realistic virtual model of their hometown and completed a task in which they pointed to familiar target locations from various orientations. Each participant's performance was most accurate when he or she was facing north, and errors increased as participants' deviation from a north-facing orientation increased. Pointing errors and latencies were not related to the distance between participants' initial locations and the target locations. Our results are inconsistent with accounts of orientation-free memory and with theories assuming that the storage of spatial knowledge depends on local reference frames. Although participants recognized familiar local views in their initial locations, their strategy for pointing relied on a single, north-oriented reference frame that was likely acquired from maps rather than experience from daily exploration. Even though participants had spent significantly more time navigating the city than looking at maps, their pointing behavior seemed to rely on a north-oriented mental map.     

Learning strategies during fear conditioning

This paper describes a model of fear learning, in which subjects have an option of behavioral responses to impending social defeat. The model generates two types of learning: social avoidance and classical conditioning, dependent upon (1) escape from or (2) social subordination to an aggressor. We hypothesized that social stress provides the impetus as well as the necessary information to stimulate dichotomous goal-oriented learning. Specialized tanks were constructed to subject rainbow trout to a conditioning paradigm where the conditioned stimulus (CS) is cessation of tank water flow (water off) and the unconditioned stimulus (US) is social aggression from a larger conspecific. Following seven daily CS/US pairings, approximately half of the test fish learned to consistently escape the aggression to a neutral chamber through a small escape hole available only during the interaction. The learning curve for escaping fish was dramatic, with an 1100% improvement in escape time over 7 days. Fish that did not escape exhibited a 400% increase in plasma cortisol and altered brain monoamine response to presentation of the CS alone. Elevated plasma cortisol levels represent classical fear conditioning in non-escaping fish, while a lack of fear conditioning and a decreased latency to escape over the training period in escapers indicates learned escape.     

Phosphorylation state of CREB in the rat hippocampus: a molecular switch between spatial novelty and spatial familiarity?

The activation of cAMP response element-binding protein (CREB) after a learning experience is a common feature in the formation of several associative memories. We recently demonstrated that the increase in the hippocampal phosphorylated CREB (pCREB) levels 1 h after a short exploration of an open field (OF) was associated to detection of spatial novelty and was not related to the memory formation of habituation in this non-associative learning paradigm. Moreover, after a long training of three OF sessions, hippocampal pCREB levels were below to that observed in control rats. The present results show that such decrease does not correlate with memory retrieval or improvement in long-term memory of habituation. Instead, it is associated with the familiarity to the arena. Our experiments revealed that the relevant variable to induce CREB deactivation was the prolonged exploration of the arena (30 min). A 15 min OF exploration was ineffective. Furthermore, the last 5 min period of a prolonged exploration was crucial to change CREB phosphorylation state: when exploration took place in a novel arena the level of pCREB increased; in contrast, when it was performed in the familiar OF, pCREB levels decreased. Taken as a whole, our results suggest that CREB phosphorylation state in the hippocampus switches in response to exposure to a novel or to a familiar spatial environment.     

The novel object recognition memory: neurobiology, test procedure, and its modifications

Animal models of memory have been considered as the subject of many scientific publications at least since the beginning of the twentieth century. In humans, memory is often accessed through spoken or written language, while in animals, cognitive functions must be accessed through different kind of behaviors in many specific, experimental models of memory and learning. Among them, the novel object recognition test can be evaluated by the differences in the exploration time of novel and familiar objects. Its application is not limited to a field of research and enables that various issues can be studied, such as the memory and learning, the preference for novelty, the influence of different brain regions in the process of recognition, and even the study of different drugs and their effects. This paper describes the novel object recognition paradigms in animals, as a valuable measure of cognition. The purpose of this work was to review the neurobiology and methodological modifications of the test commonly used in behavioral pharmacology.     

Spatial learning in a T-maze by the crayfish Orconectes rusticus

The T-maze has commonly been used to investigate the mechanisms underlying spatial learning in vertebrates and has yielded much information about how animals use response and place cues to orient toward a goal. We designed a T-maze to study the spatial learning abilities of crayfish (Orconectes rusticus), using tactile stimuli as a place cue and escape from warm water for reinforcement. An initial experiment found that most animals did not display a side-turning bias when first placed in the maze, and hence animals were randomly assigned to escape from the left or the right arm, one of which contained a smooth floor and the other a rough floor. We found that, over repeated trials, the latency to escape and the number of turns made prior to escaping significantly decreased indicating that crayfish learned to escape from the maze more rapidly and efficiently. Learning occurred over the course of six trials on a single day, and over 5 days of testing, providing evidence for spatial memory lasting 24 hr. In probe trials, in which experienced animals started the maze in an arm opposite to that used during training trials, crayfish did not display a preference for either response-based learning or place-based learning. Instead they engaged in renewed exploration of the entire maze. These findings suggest that, in addition to remembering the location of the exit, crayfish also remembered the overall configuration of the maze.     

The Effects of Intra-amygdala Infusion of the AMPA Receptor Antagonist CNQX on Retention Performance Following Aversive Training

The aim of these experiments was to determine whether impaired retention performance in aversively motivated tasks, induced by blockade of amygdala AMPA receptors, is due to influences on mechanisms underlying memory retrieval or to other influences on performance. Rats received either footshock escape training (1 or 10 trials), or no foot shock, in a two-compartment straight alley and bilateral intra-amygdala infusions of the AMPA receptor antagonist CNQX (0.5 μg) were subsequently administered prior to inhibitory avoidance retention testing 8 days later. The CNQX impaired, but did not block, inhibitory avoidance retention performance as indicated by the initial latencies to enter the shock compartment. The animals were then retained in the alley until they remained in the starting compartment for 100 consecutive s and entries into the shock compartment were recorded as errors. In both the controls and CNQX-treated groups, increases in amount of original training resulted in fewer errors, indicating memory for the escape training. Furthermore, regardless of the amount of original training (i.e., 0, 1, or 10 trials), CNQX-treated groups made more errors. Other experiments examined intra-amygdala CNQX effects on reactivity to footshock, locomotor activity, and anxiety. CNQX decreased reactivity to footshock, blocked shock-induced decreases in locomotor activity, and had an anxiolytic effect in an elevated plus maze comparable to that induced by midazolam (0.5 μg). These findings suggest that intra-amygdala infusions of CNQX prior to retention testing affect inhibitory avoidance retention performance following aversive training by altering locomotor activity, reducing sensitivity to footshock, and reducing anxiety. The implications of these findings for hypotheses concerning amygdala function in aversively motivated learning and memory is discussed.     

How the Learning Path and the Very Structure of a Multifloored Environment Influence Human Spatial Memory

Few studies have explored how humans memorize landmarks in complex multifloored buildings. They have observed that participants memorize an environment either by floors or by vertical columns, influenced by the learning path. However, the influence of the building’s actual structure is not yet known. In order to investigate this influence, we conducted an experiment using an object-in-place protocol in a cylindrical building to contrast with previous experiments which used rectilinear environments. Two groups of 15 participants were taken on a tour with a first person perspective through a virtual cylindrical three-floored building. They followed either a route discovering floors one at a time, or a route discovering columns (by simulated lifts across floors). They then underwent a series of trials, in which they viewed a camera movement reproducing either a segment of the learning path (familiar trials), or performing a shortcut relative to the learning trajectory (novel trials). We observed that regardless of the learning path, participants better memorized the building by floors, and only participants who had discovered the building by columns also memorized it by columns. This expands on previous results obtained in a rectilinear building, where the learning path favoured the memory of its horizontal and vertical layout. Taken together, these results suggest that both learning mode and an environment’s structure influence the spatial memory of complex multifloored buildings.     

Role of verbal encoding in shortand long-term odor recognition

The role of verbal encoding in odor recognition memory was investigated using odors of low familiarity to subjects before the experiment began. The experimental procedure included two phases—odor learning (first phase) and odor memory testing (second phase)—separated by a delay of 7 days. Five experimental conditions were established: three conditions of odor learning with names (labeling conditions), one condition of odor learning without names (sensory familiarization), and one condition of no learning prior to testing (control conditions). The labeling conditions differed from each other regarding label characteristics. The names were those of odor sources (veridical names), those personally generated by subjects (generated names), or those derived from the chemical names of the odorants (chemical names). Subjects were required to learn 20 fixed associations between odors (targets or distractors) and 20 names during two daily sessions. The learning sessions included two identification tests and ended by a verbal memory test in which subjects recalled odor names. The odor memory test was split into two parts separated by a retention interval of either 20 min (short-term memory) or 24 h (long-term memory). Data showed that olfactory recognition memory was enhanced in subjects who associated veridical or generated names to odors during the learning session. Chemical names were not appropriate to facilitate odor recognition. Similarly, the level of odor identification was higher for veridical and generated names than for chemical names, though the level of verbal memory for chemical names was substantial. Recognition response latencies were systematically longer for a target odor implying a positive response than for a distractor odor implying a negative response. Together, these data suggest that odor recognition and identification are sensitive to the semantic content of labels associated with odors. Odor memory was adversively influenced by time, but this influence was less pronounced when the names were endowed with a rich semantic content.