Modulatory influence of dopamine receptors on consolidation of object recognition memory

The role of dopamine receptors in regulating the formation of recognition memory remains poorly understood. Here we show the effects of systemic administration of dopamine receptor agonists and antagonists on the formation of memory for novel object recognition in rats. In Experiment I, rats received an intraperitoneal (i.p.) injection of vehicle, the selective D1 receptor agonist SKF38393 (1.0 and 5.0mg/kg), or the D2 receptor agonist quinpirole (1.0 and 5.0mg/kg) immediately after training. In Experiment II, rats received an injection of vehicle, the dopamine receptor antagonist SCH23390 (0.1 and 0.05 mg/kg), or the D2 receptor antagonist raclopride (0.5 and 0.1mg/kg) before training, followed by an injection of vehicle or the nonselective dopamine receptor agonist apomorphine (0.05 mg/kg) immediately after training. SKF38393 at 5mg/kg produced an enhancement of novel object recognition memory measured at both 24 and 72 h after training, whereas the dose of 10mg/kg impaired 24-h retention. Posttraining administration of quinpirole did not affect 24-h retention. Apomorphine enhanced memory in rats given pretraining raclopride, suggesting that the effect was mediated by selective activation of D1 receptors. The results indicate that activation of D1 receptors can enhance recognition memory consolidation. Importantly, pharmacological activation of D1 receptors enhanced novel object recognition memory even under conditions in which control rats showed significant retention.     

Noradrenergic activation of the basolateral amygdala modulates consolidation of object recognition memory

Noradrenergic activation of the basolateral complex of the amygdala (BLA) modulates the consolidation of memory for many kinds of highly emotionally arousing training tasks. The present experiments investigated whether posttraining noradrenergic activation of the BLA is sufficient to enable memory consolidation of a low-arousing training experience. Sprague-Dawley rats received intra-BLA infusions of norepinephrine, the beta-adrenoceptor antagonist propranolol or saline immediately after either 3 or 10 min of object recognition training. Saline-infused controls exhibited poor 24-h retention when given 3 min of object recognition training and good retention when given 10 min of training. Norepinephrine administered after 3 min of object recognition training produced dose-dependent enhancement of 24-h object recognition memory whereas propranolol administered after 10 min of training produced dose-dependent impairment of memory. These findings provide evidence that posttraining noradrenergic activation of the BLA enhances memory of a low-arousing training experience that would otherwise not induce long-term memory. Thus, regardless of the degree of emotional arousal induced by an experience, noradrenergic activation of the BLA after the experience ensures that it will be better remembered.     

The consolidation of object and context recognition memory involve different regions of the temporal lobe

These experiments investigated the involvement of several temporal lobe regions in consolidation of recognition memory. Anisomycin, a protein synthesis inhibitor, was infused into the hippocampus, perirhinal cortex, insular cortex, or basolateral amygdala of rats immediately after the sample phase of object or object-in-context recognition memory training. Anisomycin infused into perirhinal or insular cortices blocked long-term (24 h), but not short-term (90 min) object recognition memory. Infusions into the hippocampus or amygdala did not impair object recognition memory. Anisomycin infused into the hippocampus blocked long-term, but not short-term object-in-context recognition memory, whereas infusions administered into the perirhinal cortex, insular cortex, or amygdala did not affect object-in-context recognition memory. These results clearly indicate that distinct regions of the temporal lobe are differentially involved in long-term object and object-in-context recognition memory. Whereas perirhinal and insular cortices are required for consolidation of familiar objects, the hippocampus is necessary for consolidation of contextual information of recognition memory. Altogether, these results suggest that temporal lobe structures are differentially involved in recognition memory consolidation.     

On the role of hippocampal protein synthesis in the consolidation and reconsolidation of object recognition memory

Upon retrieval, consolidated memories are again rendered vulnerable to the action of metabolic blockers, notably protein synthesis inhibitors. This has led to the hypothesis that memories are reconsolidated at the time of retrieval, and that this depends on protein synthesis. Ample evidence indicates that the hippocampus plays a key role both in the consolidation and reconsolidation of different memories. Despite this fact, at present there are no studies about the consequences of hippocampal protein synthesis inhibition in the storage and post-retrieval persistence of object recognition memory. Here we report that infusion of the protein synthesis inhibitor anisomycin in the dorsal CA1 region immediately or 180 min but not 360 min after training impairs consolidation of long-term object recognition memory without affecting short-term memory, exploratory behavior, anxiety state, or hippocampal functionality. When given into CA1 after memory reactivation in the presence of familiar objects, ANI did not affect further retention. However, when administered into CA1 immediately after exposing animals to a novel and a familiar object, ANI impaired memory of both of them. The amnesic effect of ANI was long-lasting, did not happen after exposure to two novel objects, following exploration of the context alone, or in the absence of specific stimuli, suggesting that it was not reversible but was contingent on the reactivation of the consolidated trace in the presence of a salient, behaviorally relevant novel cue. Our results indicate that hippocampal protein synthesis is required during a limited post-training time window for consolidation of object recognition memory and show that the hippocampus is engaged during reconsolidation of this type of memory, maybe accruing new information into the original trace.     

Infusion of protein synthesis inhibitors in the entorhinal cortex blocks consolidation but not reconsolidation of object recognition memory

Memory consolidation and reconsolidation require the induction of protein synthesis in some areas of the brain. Here, we show that infusion of the protein synthesis inhibitors anisomycin, emetine and cycloheximide in the entorhinal cortex immediately but not 180 min or 360 min after training in an object recognition learning task hinders long-term memory retention without affecting short-term memory or behavioral performance. Inhibition of protein synthesis in the entorhinal cortex after memory reactivation involving either a combination of familiar and novel objects or two familiar objects does not affect retention. Our data suggest that protein synthesis in the entorhinal cortex is necessary early after training for consolidation of object recognition memory. However, inhibition of protein synthesis in this cortical region after memory retrieval does not seem to affect the stability of the recognition trace.     

Indirect object recognition: evidence for associative processes in recognition memory

Rats' exploration of stimulus P (e.g., a domestic object) is reduced following either its direct exposure or its indirect exposure and is taken to indicate recognition memory. Procedures for demonstrating indirect object recognition involve an initial presentation of object P with stimulus X (and of an object Q with stimulus Y). On test, stimulus X is presented with objects P and Q and rats' exploration of Q exceeds their exploration of P. One interpretation here is that the presentation of stimulus X on test associatively activates the memory of object P, which diminishes exploration of P relative to Q. It is possible, instead, that performance is simply the result of a novel pattern of stimulation generated by the unfamiliar combination of X and Q. The authors modified this procedure to reduce the likelihood of such a process. Their procedure involved first the presentation of PX and QY before the presentation of stimulus X alone. During the test that followed, objects P and Q were presented but stimulus X was removed. The authors found that exploration of Q remained greater than that of P despite these modifications and discuss some theoretical implications of indirect, associative processes in recognition memory.     

A neural network model of implicit memory for object recognition

People name well-known objects shown in pictures more quickly if they have studied them previously. The most common interpretation of this priming effect is that processing is facilitated by an implicit memory trace in a perceptual representation system. We show that object priming can be explained instead as a bias in information processing, without recourse to an implicit memory system. Assumptions about psychological decision-making processes and bias were added to a neural network model for object identification, and the model accounted for performance both qualitatively and quantitatively in four object identification experiments.     

Epinephrine enhancement of human memory consolidation: interaction with arousal at encoding

Abundant evidence indicates that endogenous stress hormones like epinephrine and cortisol modulate memory consolidation in animals. Despite this evidence, there has been no demonstration that endogenous stress hormones modulate memory consolidation in humans. In the present study, healthy subjects viewed a series of 21 slides, and immediately after received an intravenous infusion of either saline or epinephrine (40 or 80 ng/kg/min). Memory for the first three (primacy) and last three (recency) slides viewed was assessed with an incidental free recall test one week later. Epinephrine dose-dependently increased memory for the primacy slides, but did not affect memory of the recency slides. A subsequent experiment involving new subjects revealed significantly higher electrodermal responses to the primacy compared with recency slides. These findings support the view (Gold & McGaugh, 1975) that endogenous stress hormones modulate memory consolidation for experiences that induce their release. Additionally, they suggest that in humans these hormones may interact with the degree of arousal at initial encoding of information to modulate memory consolidation processes for that information.     

Visual recognition memory enhancement in children through differential outcomes

Objective

The use of differential outcomes has been shown to enhance discriminative learning and face recognition in children and adults. In this study, we further investigated whether the differential outcome procedure (DOP) would also be effective in improving recognition memory for a wide range of stimuli with varying visual complexity (familiar objects, abstract stimuli, and complex scenes) in 5- and 7-year-old children.

Method

Participants viewed a sample stimulus and, after a short (5 s) or a long (15 s) delay, they had to identify the previously seen stimulus among four choice alternatives. In the differential outcomes condition, each sample stimulus was paired with a specific outcome; whereas in the non-differential conditions outcomes were administered randomly. In Experiment 2, we replicated Experiment 1 but in addition we asked participants to perform an articulatory suppression task to prevent verbal rehearsal.

Results

Children showed a greater overall visual delayed recognition when differential outcomes were arranged in both experiments. The type of stimulus being used modulated this effect; a beneficial effect of the differential outcomes training was evident with abstract objects in Experiment 1 and with both, abstract objects and scenes in Experiment 2.     

On the delay-dependent involvement of the hippocampus in object recognition memory

The role of the hippocampus in object recognition memory processes is unclear in the current literature. Conflicting results have been found in lesion studies of both primates and rodents. Procedural differences between studies, such as retention interval, may explain these discrepancies. In the present study, acute lidocaine administration was used to temporarily inactivate the hippocampus prior to training in the spontaneous object recognition task. Male C57BL/6J mice were administered bilateral lidocaine (4%, 0.5 microl/side) or aCSF (0.5 microl/side) directly into the CA1 region of the dorsal hippocampus 5 min prior to sample object training, and object recognition memory was tested after a short ( 5 min) or long (24 h) retention interval. There was no effect of intra-hippocampal lidocaine on the time needed for mice to accumulate sample object exploration, suggesting that inactivation of the hippocampus did not affect sample session activity or the motivation to explore objects. Lidocaine-treated mice exhibited impaired object recognition memory, measured as reduced novel object preference, after a 24 h but not a 5 min retention interval. These data support a delay-dependent role for the hippocampus in object recognition memory, an effect consistent with the results of hippocampal lesion studies conducted in rats. However, these data are also consistent with the view that the hippocampus is involved in object recognition memory regardless of retention interval, and that object recognition processes of parahippocampal structures (e.g., perirhinal cortex) are sufficient to support object recognition memory over short retention intervals.     

Post-training reversible inactivation of the hippocampus enhances novel object recognition memory

Research on the role of the hippocampus in object recognition memory has produced conflicting results. Previous studies have used permanent hippocampal lesions to assess the requirement for the hippocampus in the object recognition task. However, permanent hippocampal lesions may impact performance through effects on processes besides memory consolidation including acquisition, retrieval, and performance. To overcome this limitation, we used an intrahippocampal injection of the GABA agonist muscimol to reversibly inactivate the hippocampus immediately after training mice in two versions of an object recognition task. We found that the inactivation of the dorsal hippocampus after training impairs object-place recognition memory but enhances novel object recognition (NOR) memory. However, inactivation of the dorsal hippocampus after repeated exposure to the training context did not affect object recognition memory. Our findings suggest that object recognition memory formation does not require the hippocampus and, moreover, that activity in the hippocampus can interfere with the consolidation of object recognition memory when object information encoding occurs in an unfamiliar environment.The medial temporal lobe plays an important role in recognition memory formation, as damage to this brain structure in humans, monkeys, and rodents impairs performance in recognition memory tasks (for review, see Squire et al. 2007). Within the medial temporal lobe, studies have consistently demonstrated that the perirhinal cortex is involved in this form of memory (Brown and Aggleton 2001; Winters and Bussey 2005; Winters et al. 2007, 2008; Balderas et al. 2008). In contrast, the role of the hippocampus in object recognition memory remains a source of debate. Some studies have reported novel object recognition (NOR) impairments in animals with hippocampal lesions (Clark et al. 2000; Broadbent et al. 2004, 2010), yet others have reported no impairments (Winters et al. 2004; Good et al. 2007). Differences in hippocampal lesion size and behavioral procedures among the different studies have been implicated as the source of discrepancy in these findings (Ainge et al. 2006), but previous studies have not examined the consequences of environment familiarity on the hippocampus dependence of object recognition memory.Previous studies addressing the role of the hippocampus in recognition memory relied on permanent, pre-training lesions (Clark et al. 2000; Broadbent et al. 2004; Winters et al. 2004; Good et al. 2007). Permanent lesions inactivate the hippocampus not only during the consolidation phase, but also during habituation, acquisition, and memory retrieval, potentially confounding interpretation of the results. Furthermore, permanent lesion studies require long surgery recovery times during which extrahippocampal changes may emerge to mask or compensate for the loss of hippocampal function. To overcome these problems, we reversibly inactivated the dorsal hippocampus after training mice in two versions of the object recognition task. We infused muscimol, a γ-aminobutyric acid (GABA) receptor type A agonist, into the dorsal hippocampus immediately after training in an object-place recognition task or immediately following training in a NOR task. Consistent with previous studies (Save et al. 1992; Galani et al. 1998; Mumby et al. 2002; Stupien et al. 2003; Aggleton and Brown 2005), we observed that hippocampal inactivation impairs object-place recognition memory. Interestingly, we observed that the degree of contextual familiarity can influence NOR memory formation. We found that when shorter periods of habituation to the experimental environment were used, hippocampal inactivation enhances long-term NOR memory. In contrast, after extended periods of contextual habituation, long-term recognition memory was unaltered by hippocampal inactivation. Together these results suggest that if familiarization with objects occurs at a stage in which the contextual environment is relatively novel, the hippocampus plays an inhibitory role on the consolidation of object recognition memory. Supporting this view, we observed that object recognition memory is unaffected by hippocampal inactivation when initial exploration of the objects occurred in a familiar environment.     

Sleep enhances memory consolidation in the hippocampus-dependent object-place recognition task in rats

The positive impact of sleep on memory consolidation has been shown for human subjects in numerous studies, but there is still sparse knowledge on this topic in rats, one of the most prominent model species in neuroscience research. Here, we examined the role of sleep in the object-place recognition task, a task closely comparable to tasks typically applied for testing human declarative memory: It is a one-trial task, hippocampus-dependent, not stressful and can be repeated within the same animal. A test session consisted of the Sample trial, followed by a 2-h retention interval and a Test trial, the latter examining the memory the rat had for the places of two objects presented at the Sample trial. In Experiment 1, each rat was tested twice, with the retention interval taking place either in the morning or evening, i.e., in the inactive or active phase, respectively. Rats showed significantly (p<0.01) better memory for object place after the Morning session. To control for confounding circadian factors, in Experiment 2 rats were tested four times, i.e., in the morning or in the evening while sleep was or was not deprived. Sleep during the retention interval was recorded polysomnographically. Rats only showed significant memory for the target object place in the Test trial after the Morning retention interval in the absence of sleep deprivation, and recognition performance in this condition was significantly superior to that in the three other conditions (p<0.05). EEG recordings during spontaneous morning sleep revealed increased slow oscillation (0.85-2.0 Hz) and upper delta (2.0-4.0 Hz), but reduced spindle band (10.5-13.5 Hz) activity, as compared to evening sleep. However, spindle band power was increased in the Morning retention interval in comparison to a Morning Baseline period (p<0.05). We conclude that consolidation of object-place memory depends on sleep, and presumably requires NonREM sleep rich in both slow wave and spindle activity.     

New behavioral protocols to extend our knowledge of rodent object recognition memory

Animals often show an innate preference for novelty. This preference facilitates spontaneous exploration tasks of novelty discrimination (recognition memory). In response to limitations with standard spontaneous object recognition procedures for rodents, a new task (“bow-tie maze”) was devised. This task combines features of delayed nonmatching-to-sample with spontaneous exploration. The present study explored aspects of object recognition in the bow-tie maze not amenable to standard procedures. Two rat strains (Lister Hooded, Dark Agouti) displayed very reliable object recognition in both the light and dark, with the Lister Hooded strain showing superior performance (Experiment 1). These findings reveal the potential contribution of tactile and odor cues in object recognition. As the bow-tie maze task permits multiple trials within a session, it was possible to derive forgetting curves both within-session and between-sessions (Experiment 1). In Experiment 2, rats with hippocampal or fornix lesions performed at normal levels on the basic version of the recognition task, contrasting with the marked deficits previously seen after perirhinal cortex lesions. Next, the training protocol was adapted (Experiment 3), and this modified version was used successfully with mice (Experiment 4). The overall findings demonstrate the efficacy of this new behavioral task and advance our understanding of object recognition.Understanding the neural basis of recognition memory, the ability to discriminate whether a stimulus is novel or familiar, is heavily reliant on animal research. Here, advances have been closely tied to the introduction of new behavioral tests. The preeminent example concerns one-trial tests of recognition memory for monkeys using delayed nonmatching-to-sample (Mishkin and Delacour 1975). These tasks reward the natural preference that monkeys have for selecting novel items and permit multiple recognition trials within a single session. These features make the task relatively easy to train and then maximize findings from small group sizes. Although rat tasks closely based on delayed nonmatching-to-sample have been devised (Aggleton 1985; Mumby et al. 1990; Steckler et al. 1998; Prusky et al. 2004), they are very rarely employed as they are difficult to train and performance levels are unreliable.Almost all studies of rodent recognition memory now employ the spontaneous object recognition test and its direct variants (Ennaceur and Delacour 1988; Dix and Aggleton 1999; Winters et al. 2008). These tasks again take advantage of an innate preference for novel items, but this preference is displayed by spending more time exploring novel than familiar stimuli. In the standard version of the task, a rodent (rat or mouse) is placed in an arena containing two identical objects and then freely allowed to explore these objects for several minutes (“sample” phase). After a delay, the rodent is placed back in the arena (“test” phase), which now contains one familiar object (a copy of the sample phase objects) and a novel object. Recognition is signified by greater exploration of the novel object. Because the task measures spontaneous behavior, it requires minimal pretraining, but for the same reason it is prone to considerable variance. Unlike delayed nonmatching-to-sample, each trial (sample plus test phase) takes many minutes, and so only one recognition trial is normally given per session. Advantages are that proactive interference between objects is minimized, and the one-trial design lends itself to episodic-like tests of memory (Dere et al. 2005; Good et al. 2007). Disadvantages include the fact that data accumulation, with appropriate counterbalancing, is slow.To address these limitations, a new object recognition test using a “bow-tie maze” (Fig. 1A) has been developed for rats (Albasser et al. 2010). This test combines features of delayed nonmatching-to-sample with spontaneous object preference: It permits multiple trials per session, but the measure of recognition comes from the preferential exploration of novelty. The rat is first placed in one end of a bow-tie–shaped maze that contains a single object (object A; Fig. 1B). After a minute, the rat is allowed to run to the other end of the maze where there are two dissimilar objects (A and B; Fig. 1B). Object A is familiar as it is identical to the object previously explored, while object B is novel. Consequently, a rat will typically prefer to explore object B. On the next trial, a minute later, the rat shuttles back to the initial start point, but this time encounters objects B and C. Object B is now familiar, while object C is novel. The next trial, 1 min later, is between object C (now familiar) and object D (novel), and so on. A food reward placed under every object promotes shuttling back and forth within the maze, and encourages interaction with the objects. Unlike delayed nonmatching-to-sample, the food reward is not contingent on first selecting the novel object.Open in a separate windowFigure 1.(A) Schematic of the bow-tie maze. A sliding door separates the two ends of the maze in which two objects are placed. (B) General procedure showing the presentation order of the objects in the standard object recognition task. All objects are rewarded (+). (Arrow) Rat movements. (Black print) Novel objects, (gray print) familiar objects.The present study used the bow-tie maze to explore recognition memory on four fronts. In Experiment 1, recognition in the light and recognition in the dark were compared to help determine the cues available to detect object familiarity. It is known that rats can perform recognition tasks when solely reliant on visual cues (Aggleton 1985; Bartko et al. 2007; Winters and Reid 2010), but object recognition based on other modalities remains largely unexplored (Winters and Reid 2010). Potential cues for recognition include odor differences and tactile information. It is known that rats can discriminate novel from familiar olfactory cues (Otto and Eichenbaum 1992; Kesner et al. 2002; Fortin et al. 2004; Wolff et al. 2006), while tactile (e.g., vibrissae) cues can be used to distinguish surfaces (e.g., Birrell and Brown 2000). The bow-tie maze is ideal for studying object recognition in the dark as the rats are rewarded for visiting items in set locations (to receive food rewards), and so should readily approach the objects. In contrast, running the standard spontaneous object recognition test (in an arena) in the dark would be problematic as it is not clear how the rats would first appreciate the presence of the to-be-discriminated objects.An additional goal of Experiment 1 was to determine how readily the bow-tie maze could be used to compile within-session and between-session forgetting curves. A limitation with the standard spontaneous object task is that with only one trial per session it can be very time consuming to create forgetting curves, while within-session forgetting curves for individual animals are not feasible. These shortcomings create limitations when examining manipulations thought to affect memory. The possibility of deriving within-session forgetting curves is particularly appealing as: (1) it minimized the impact of those factors that introduce variance when performance is compared across sessions, and (2) the animal need not be removed from the maze, which could additionally disrupt performance, e.g., by increasing stress. A further component of Experiment 1 manipulated object memory strength by presenting objects either once (“single”) or six times (“repeated”). Recognition was tested after a 3-h delay with the twin goals of determining whether repeated presentation would aid performance and whether these performance levels would be sufficiently above chance so that they could be used to examine factors involved in longer term memory.At the same time, Experiment 1 provided the opportunity to compare two rat strains, Dark Agouti (DA) and Lister Hooded (LH). Previous studies suggest that the Dark Agouti strain might be particularly good at visual recognition tasks (Aggleton 1996), though others have argued that this strain has aberrant behavioral properties, including higher anxiety and higher levels of inappropriate nonspatial behaviors in spatial learning tasks (Mechan et al. 2002; Harker and Whishaw 2004; but see Aggleton and Vann 2004).Experiment 2 examined the ability of rats with either hippocampal or fornix lesions to perform object recognition in the bow-tie maze. There is a longstanding debate over the impact of hippocampal damage on recognition memory, with mixed findings coming from spontaneous object recognition tests (Clark et al. 2000; Mumby 2001; Gaskin et al. 2003; Winters et al. 2008). The bow-tie maze should prove informative as numerous trials can be run to assess the impact of selective brain lesions. Although in this initial study only short retention delays were examined, these same delays and conditions are highly sensitive to perirhinal cortex lesions (Aggleton et al. 2010; Horne et al. 2010), a brain region regarded as vital for recognition memory (Brown and Aggleton 2001). In Experiment 3 the training protocol changed so that objects did not cover food rewards. Rather, a single food reward was always placed between the test objects. This modification was examined because: (1) it would preclude any exploration scores that were simply derived from attempts to move the test objects in order to uncover the food reward, and (2) it would introduce a task variant that might be amenable to small rodents not able to move objects. Accordingly, Experiment 4 examined the performance of mice (strain C57Bl/6) on a test of object recognition based on the modified version of the bow-tie maze from Experiment 3.     

Scopolamine infused into perirhinal cortex improves object recognition memory by blocking the acquisition of interfering object information

In a previous study, we reported apparently paradoxical facilitation of object recognition memory following infusions of the cholinergic muscarinic receptor antagonist scopolamine into the perirhinal cortex (PRh) of rats. We attributed these effects to the blockade by scopolamine of the acquisition of interfering information. The present study tested this possibility directly by modifying the spontaneous object recognition memory task to allow the presentation of a potentially interfering object either before the sample phase or in the retention delay between the sample and choice phases. Presentation of an object between the sample and choice phases disrupted subsequent recognition of the sample object (retroactive interference), and intra-PRh infusions of scopolamine prior to the presentation of the irrelevant object prevented this retroactive interference effect. Moreover, presentation of an irrelevant object prior to the sample phase interfered proactively with sample object recognition, and intra-PRh infusions of scopolamine prior to the presentation of the pre-sample object prevented this proactive interference effect. These results suggest that blocking muscarinic cholinergic receptors in PRh can disrupt the acquisition of potentially interfering object information, thereby facilitating object recognition memory. This finding provides further, strong evidence that acetylcholine is important for the acquisition of object information in PRh.     

Deletion of the GluA1 AMPA receptor subunit impairs recency-dependent object recognition memory

Deletion of the GluA1 AMPA receptor subunit impairs short-term spatial recognition memory. It has been suggested that short-term recognition depends upon memory caused by the recent presentation of a stimulus that is independent of contextual-retrieval processes. The aim of the present set of experiments was to test whether the role of GluA1 extends to nonspatial recognition memory. Wild-type and GluA1 knockout mice were tested on the standard object recognition task and a context-independent recognition task that required recency-dependent memory. In a first set of experiments it was found that GluA1 deletion failed to impair performance on either of the object recognition or recency-dependent tasks. However, GluA1 knockout mice displayed increased levels of exploration of the objects in both the sample and test phases compared to controls. In contrast, when the time that GluA1 knockout mice spent exploring the objects was yoked to control mice during the sample phase, it was found that GluA1 deletion now impaired performance on both the object recognition and the recency-dependent tasks. GluA1 deletion failed to impair performance on a context-dependent recognition task regardless of whether object exposure in knockout mice was yoked to controls or not. These results demonstrate that GluA1 is necessary for nonspatial as well as spatial recognition memory and plays an important role in recency-dependent memory processes.     

Contextual modulation of memory consolidation

We investigate olfactory memory consolidation in honeybees. Three experiments are reported that include 1024 animals in 28 experimental groups. After one pairing of odorant and sucrose reward, retention is typically nonmonotonic with a minimum 3 min after conditioning. This corresponds to the “Kamin effect” in vertebrates; the postminimum rise in retention is usually interpreted as reflecting memory consolidation. First, we test for the generality of this effect across four different odorants. The postminimum rise in retention was reproducibly observed for 1-hexanol but not for 1-octanol, limonene, or geraniol. Second, we investigate whether previous learning about the training context modulates subsequent memory consolidation. On the day before training, a reward was applied either upon placement into the future training context for 1 min, halfway during exposure or just before removal from the context. In the latter group, the 3-min minimum in retention was eliminated; thus, in that group, forward pairings of context and reward (i.e., context exposure begins before reward is applied) lead to an associative context memory that can modulate subsequent olfactory memory consolidation. Third, we found no evidence for a modulation of olfactory memory consolidation by pre-exposure to the odorant.