Amygdala and “emotional” modulation of the relative use of multiple memory systems

The basolateral amygdala modulates the cognitive and habit memory processes mediated by the hippocampus and caudate nucleus, respectively. The present experiments used a plus-maze task that can be acquired using either hippocampus-dependent “place” learning or caudate-dependent “response” learning to examine whether peripheral or intra-basolateral amygdala injection of anxiogenic drugs would bias rats towards the use of a particular memory system. In Experiment 1, adult male Long–Evans rats were trained to swim from the same start point to an escape platform located in a consistent goal arm, and received pre-training peripheral injections of the α₂-adrenoceptor antagonists yohimbine (2.5 or 5.0 mg/kg), RS 79948-197 (0.05, 0.1, or 0.2 mg/kg), or vehicle. On a drug-free probe trial from a novel start point administered 24 h following acquisition, vehicle treated rats predominantly displayed hippocampus-dependent place learning, whereas rats previously treated with yohimbine (2.5, 5.0 mg/kg) or RS 79948-197 (0.1 mg/kg) predominantly displayed caudate-dependent response learning. In Experiment 2, rats receiving pre-training intra-basolateral amygdala infusions of RS 79948-197 (0.1 μg/0.5 μl) also predominantly displayed response learning on a drug-free probe trial. The findings indicate (1) peripheral injections of anxiogenic drugs can influence the relative use of multiple memory systems in a manner that favors caudate-dependent habit learning over hippocampus-dependent cognitive learning, and (2) intra-basolateral amygdala infusion of anxiogenic drugs is sufficient to produce this modulatory influence of emotional state on the use of multiple memory systems.     

Amygdala modulation of memory consolidation: interaction with other brain systems

There is a strong consensus that the amygdala is involved in mediating influences of emotional arousal and stress on learning and memory. There is extensive evidence that the basolateral amygdala (BLA) is a critical locus of integration of neuromodulatory influences regulating the consolidation of several forms of memory. Many drug and stress hormone influences converge in activating the release of norepinephrine (NE) within the BLA. Evidence from studies using in vivo microdialysis and high-performance liquid chromatography indicates that increases in amygdala NE levels assessed following inhibitory avoidance training correlate highly with subsequent retention. Other evidence indicates that NE influences on memory consolidation require muscarinic cholinergic activation within the BLA provided by projections from the nucleus basalis magnocellularis (NB). Evidence from several experiments indicates that activation of the BLA plays an essential role in modulating memory consolidation processes involving other brain regions. These findings provide strong support for the hypothesis that the BLA plays a critical role in regulating the consolidation of lasting memories of significant experiences.     

Cocaine self-administration alters the relative effectiveness of multiple memory systems during extinction

Rats were trained to run a straight-alley maze for an oral cocaine or sucrose vehicle solution reward, followed by either response or latent extinction training procedures that engage neuroanatomically dissociable “habit” and “cognitive” memory systems, respectively. In the response extinction condition, rats performed a runway approach response to an empty fluid well. In the latent extinction condition, rats were placed at the empty fluid well without performing a runway approach response. Rats trained with the sucrose solution displayed normal extinction behavior in both conditions. In contrast, rats trained with the cocaine solution showed normal response extinction but impaired latent extinction. The selective impairment of latent extinction indicates that oral cocaine self-administration alters the relative effectiveness of multiple memory systems during subsequent extinction training.Understanding the psychological and neural mechanisms underlying the acquisition and extinction of drug-seeking behavior has important implications for therapies targeting drug addiction. A better understanding of the neurobiology of extinction can potentially allow for the development of treatments to produce more effective and persistent extinction learning. Dissociable hippocampus-dependent “cognitive” and dorsal striatal-dependent “habit” memory systems are engaged during the initial acquisition of learned behavior (for reviews, see Packard and Knowlton 2002; White and McDonald 2002; Squire 2004). Interestingly, recent evidence indicates that multiple memory systems can also be engaged during the new learning that occurs during behavioral extinction (Gabriele and Packard 2006). For example, the behavior of a rat trained to traverse a straight-alley runway for a food reward can be extinguished using either habit/response or cognitive/latent extinction training procedures. During response extinction, rats are allowed to perform the runway approach response to an empty food cup. In contrast, during latent extinction, rats are placed at the empty food cup without performing the runway approach response. Consistent with evidence indicating a selective role for the hippocampus in cognitive memory, neural inactivation of this brain structure impairs latent extinction and spares response extinction (Gabriele and Packard 2006). Moreover, consistent with evidence that the dorsal striatum selectively mediates habit memory (for review, see Packard and Knowlton 2002), neural inactivation of this brain region impairs response extinction and spares latent extinction (A. Gabriele and M.G. Packard, unpubl.).The transition from initial drug use to eventual addiction may involve, at least in part, the development of compulsive drug-seeking and drug-taking behaviors that are increasingly guided by dorsal striatal-dependent habit learning mechanisms (for reviews, see White 1996; Everitt et al. 2001; Everitt and Robbins 2005; Belin et al. 2008). This hypothesis raises the possibility that once “habit-like” drug-seeking behaviors are firmly acquired, the extinction of such behaviors may be differentially influenced by engaging habit and cognitive memory systems. In the present study, we examined this idea by comparing the relative effectiveness of response and latent extinction training procedures in rats trained to run a straight-alley maze for an oral cocaine reward. Consistent with criteria considered important for demonstrating drug dependence, oral cocaine self-administration produces withdrawal following forced abstinence (Barros and Miczek 1996) and additionally is resistant to reinforcer devaluation (Miles et al. 2003), indicating that this behavior becomes divorced from its consequences in a manner similar to the dorsal striatum-mediated compulsive drug-seeking behavior that may characterize addiction (for reviews, see White 1996; Everitt et al. 2001; Everitt and Robbins 2005; Belin et al. 2008).The apparatus was an elevated (86.4 cm) straight-alley maze with a black Plexiglas floor and clear Plexiglas sides (117.8 cm long, 11.4 cm wide, and 20.3 cm tall). A fluid cup (2.5-cm diameter) was located at the goal end of the maze. The maze was located in a room containing several extra-maze cues.Subjects were 32 adult male Long-Evans rats (275–300 g). Rats were individually housed on a 12:12-h light–dark cycle, with lights on from 8:00 a.m.–8:00 p.m. All animals received food ad libitum.During all behavioral procedures, water bottles were removed from home cages 24 h prior to training, and animals received 15 min/day access to water following each day''s procedures. Training began with 3 d of habituation to the solution to be used during training (cocaine–sucrose [0.1% cocaine HCl/20% sucrose in ddH₂0] or sucrose [20% in ddH₂0] alone). Each habituation day involved presentations of 0.5 mL of the solution in a novel environment consisting of a half-white, half-black box (41.9 cm long, 31.8 cm wide, 35.6 tall) with the fluid cup located in the center of the black side. The number of presentations increased with each habituation day (1, 2, and 4). Each individual presentation had a maximum time of 20 min, and rats were removed when the solution was consumed. Volume consumed and amount of time to consume the solution were recorded for each rat. Each sucrose rat was matched to a cocaine rat to ensure that there were no differences between groups in terms of volume of solution consumed prior to training. For each matched pair, the volume consumed by the rat receiving the cocaine solution during each presentation was measured, and an identical amount was made available to the matched sucrose animal. If, during any given presentation, the cocaine animal did not consume any solution, then the matched sucrose animal received 20 min in the habituation environment with no solution present.Behavioral procedures were similar to those of our previous study using food reward (Gabriele and Packard 2006). During maze training, animals received either the cocaine–sucrose solution or sucrose vehicle solution reward. On days 1–10 of solution-rewarded maze training (six trials per day), rats were placed in the start end and allowed to traverse the maze and drink the available reward solution (0.5 mL). Upon consuming the solution, rats were removed from the maze and placed in an opaque holding box adjacent to the maze for a 30-sec intertrial interval. On each trial, the latency (in seconds) to reach the fluid cup was recorded and used as the measure of task acquisition. If a rat failed to reach the fluid cup within 60 sec, it was removed for the intertrial interval and a latency of 60 sec was recorded.Twenty-four hours following the completion of training (i.e., day 11), rats were assigned to one of two extinction conditions; latent extinction (n = 18, 10 cocaine and eight sucrose) or response extinction (n = 14, seven cocaine and seven sucrose). For both the latent and response conditions, extinction training was administered over 3 d (six trials per day, 30-sec intertrial interval) with no reward solution present. In the latent extinction condition, rats were placed facing the empty fluid cup in the goal end of the maze and were confined for 60 sec by placement of a clear Plexiglas barrier 20 cm from the rear wall of the goal end of the maze. Following confinement, rats were removed from the maze and placed in the holding box for the 30-sec intertrial interval. In the response extinction condition, rats were placed into the start end of the maze as during training and allowed to run to an empty fluid cup at the goal end of the maze. Upon reaching the empty fluid cup and being allowed to discover its emptiness (or after 60 sec if the rat did not reach the reward cup), rats were removed from the maze and placed in the holding box for the 30-sec intertrial interval. Latency to reach the fluid cup was recorded and used as the measure of extinction behavior. On day 3 of extinction, 90 min following the sixth daily extinction trial, all rats were given an additional four extinction “probe” trials in which they were placed in the start end of the maze and latency to reach the empty fluid cup was recorded. These four trials allowed for an assessment of the effectiveness of each extinction procedure.Data from the runway acquisition sessions are presented in Figure 1. A two-way one-repeated-measure ANOVA (Group [cocaine vs. sucrose] × Session) comparing the latencies to reach the fluid cup during acquisition in rats that subsequently received latent extinction revealed a significant effect of Session (F_(9,16) = 61.03, P < 0.001), indicating that latency to reach the fluid cup during acquisition decreased across sessions. However, the absence of a main effect of Group (F_(1,16) = 1.94, n.s.) or interaction between Group and Session (F_(9,16) = 0.53, n.s.) indicates that rats trained to run for cocaine and sucrose acquired the task at similar rates (Fig. 1A). Similar results were observed in rats that subsequently received response extinction (Fig. 1B) in that there was a main effect of Session (F_(9,12) = 13.11, P < 0.001) but no main effect (F_(1,12) = 0.44, n.s.) or interaction (F_(9,12) = 1.50, n.s.) involving drug Group.Open in a separate windowFigure 1.Acquisition of maze runway behavior. (A) Acquisition of maze runway behavior by rats that subsequently received latent extinction. (B) Acquisition of maze runway behavior by rats that subsequently received response extinction. Mean ± SEM of latency (in seconds) to reach the solution cup over training days. For both extinction conditions, there were no group differences in the initial acquisition of runway behavior.The effects of oral cocaine self-administration on latent and response extinction are shown in Figure 2. A two-way ANOVA (Group × Extinction condition) comparing mean runway latencies (collapsed across the four probe trials) for each group revealed a significant main effect of Extinction condition (F_(1,28) = 32.440, P < 0.001), indicating that the response extinction procedures produced greater extinction of the runway response, and a significant interaction effect between Extinction condition and Group (F_(1,28) = 4.813, P < 0.05) but no effect of Group (F_(1,28) = 0.96, n.s.). Simple effects tests showed a significant effect of Group within the latent extinction condition (F_(1,16) = 5.688, P < 0.05) but not the response extinction condition (F_(1,12) = 0.663, n.s.), indicating that oral cocaine self-administration selectively impaired latent but not response extinction. Additionally, a two-way one-repeated-measure ANOVA (Group × Trial) computed on the latencies to reach the fluid cup during response extinction training revealed a main effect of Trial (F_(2,12) = 16.44, P < 0.001), but no significant main effect (F_(1,12) = 2.27, n.s.) or interaction (F_(2,12) = 0.88, n.s.) involving Group, further indicating that oral cocaine did not impair response extinction.Open in a separate windowFigure 2.Effects of oral cocaine self-administration on extinction. The effect of oral cocaine self-administration on runway latent and response extinction. Mean ± SEM latency (in seconds) to reach the fluid cup is shown over the four extinction probe trials. Oral cocaine self-administration impaired latent extinction, but did not impair response extinction.The present experiments investigated the effect of oral cocaine self-administration on response and latent extinction in a straight-alley maze. Following training, rats in the response extinction condition performed the approach response to an empty goal box, whereas rats in the latent extinction condition were placed in the goal box with no reward present. Consistent with previous studies using food reward (e.g., Seward and Levy 1949; Gabriele and Packard 2006), rats rewarded with a sucrose solution were able to extinguish the approach response following both response and latent extinction procedures. In contrast, rats rewarded with a cocaine solution displayed normal response extinction (see also Schoenbaum and Setlow 2005) but impaired latent extinction. The selective impairing effect of oral cocaine self-administration on latent extinction indicates that the drug does not impair processes that contribute to general maze behavior (e.g., motivational, motor, or sensory processes), as any such influence would also likely produce a deficit in response extinction.Previous findings indicate that latent extinction of runway behavior is hippocampus dependent, whereas response extinction is dorsal striatal dependent (Gabriele and Packard 2006; A. Gabriele and M.G. Packard, unpubl.). In view of evidence that the hippocampus and dorsal striatum mediate cognitive and habit learning mechanisms, respectively (for reviews, see Packard and Knowlton 2002; White and McDonald 2002; Squire 2004), the findings suggest that oral cocaine self-administration can affect the relative use of multiple memory systems during extinction learning. The medial prefrontal cortex and basolateral amygdala have been implicated in extinction of several forms of learned behavior, and prior cocaine exposure can impair some forms of extinction learning (Burke et al. 2006; Peters et al. 2008; Quirk and Mueller 2008). However, neural inactivation of medial prefrontal cortex or basolateral amygdala does not affect latent extinction of maze runway behavior (A. Gabriele and M.G. Packard, unpubl.), suggesting that cocaine-induced dysfunction of these structures does not account for the results observed here.One explanation of the cocaine-induced impairment of latent extinction is that the approach response acquired during task acquisition is guided by a supra-normal stimulus-response habit, thereby rendering cognitive learning mechanisms ineffectual during latent extinction training. Consistent with this possibility, drug-seeking behaviors underlying addiction may involve, at least in part, a transition from goal-directed behaviors to habitual behaviors that characterize the function of the dorsal striatal memory system (e.g., Tiffany 1990; White 1996; Packard 1999; Everitt et al. 2001; Porrino et al. 2004; Everitt and Robbins 2005; Belin et al. 2008). Indeed, recent evidence implicates the dorsal striatum in habitual drug-seeking behaviors. For example, intradorsal striatum administration of dopamine antagonists impairs cocaine seeking (Vanderschuren et al. 2005), and inactivation of the dorsal striatum attenuates drug seeking, following both abstinence and extinction (Fuchs et al. 2006; See et al. 2007). Interestingly, disconnection between the ventral and dorsolateral striatum impairs cocaine-seeking behavior (Belin and Everitt 2008), and extended cocaine use enhanced cue-selective firing in the dorsal striatum and reduced cue-selective firing in the ventral striatum in go/no go discrimination learning, indicating an accelerated shift to dorsolateral striatal control (Takahashi et al. 2007). In addition, dopamine release increases in the dorsal striatum of rats following presentation of a response-contingent cue associated with cocaine (Ito et al. 2002). Similar results from fMRI and PET studies of human cocaine addicts showed increased activation in the dorsal striatum (Garavan et al. 2000) and an increase in dopamine release within the dorsal striatum (Volkow et al. 2006) following cue-induced cravings.A second explanation of the cocaine-induced impairment in latent extinction is that drug intake during task acquisition may have affected hippocampal physiology in a manner that negatively impacted the hippocampus-dependent learning that subsequently mediates latent extinction. Consistent with this possibility, chronic cocaine exposure impairs subsequent performance of hippocampus-dependent tasks such as the Morris water maze and the win-shift radial arm maze task (Melnick et al. 2001; Quirk et al. 2001; Mendez et al. 2008). However, it should be noted that the impairments observed in the latter studies were observed following exposure to cocaine doses considerably higher than those used in the present oral self-administration study. Since the current experiments do not explicitly examine the potential neurobiological progression underlying the acquisition of runway responding, further research is necessary to determine whether the cocaine-induced impairment of latent extinction involves the interfering effect of a supra-normal response habit, or a direct impairing effect on hippocampal physiology. It should also be noted that both oral cocaine self-administration and a passive cocaine administration regimen produce results analogous to those presented here, in that they impair “cognitive” representations of rewards (Miles et al. 2003; Schoenbaum and Setlow 2005). However, the relationship between this type of cognitive reward representation (mediated by interactions between basolateral amygdala and orbitofrontal cortex) (Pickens et al. 2003) and cognitive representations in latent extinction mediated by the hippocampus (Gabriele and Packard 2006) is currently unclear.Finally, the selective impairing effect of cocaine self-administration on latent extinction may have implications for understanding the persistent ability of drug-predictive cues and contexts to compel drug-seeking behavior and relapse. Specifically, if the ability to use cognitive learning mechanisms to extinguish drug-seeking behaviors is impaired following the transition from initial to habitual and compulsive drug use, then contextual/relational cues might be expected to maintain greater control over behavior following extinction training. This in turn might suggest that incorporation of response extinction procedures into treatment strategies might provide greater therapeutic efficacy.     

Amygdala oscillations and the consolidation of emotional memories

The amygdala receives multi-modal sensory inputs and projects to virtually all levels of the central nervous system. Via these widespread projections, the amygdala facilitates consolidation of emotionally arousing memories. How the amygdala promotes synaptic plasticity elsewhere in the brain remains unknown, however. Recent work indicates that amygdala neurons show theta activity during emotional arousal, and various types of oscillations during sleep. These synchronized neuronal events could promote synaptic plasticity by facilitating interactions between neocortical storage sites and temporal lobe structures involved in declarative memory.     

Effects of emotional arousal on multiple memory systems: evidence from declarative and procedural learning

Extensive evidence documents emotional modulation of hippocampus-dependent declarative memory in humans. However, little is known about the emotional modulation of striatum-dependent procedural memory. To address how emotional arousal influences declarative and procedural memory, the current study utilized (1) a picture recognition and (2) a weather prediction (WP) task (a probabilistic classification learning task), which have been shown to rely on hippocampal- and striatum-based memory systems, respectively. Observers viewed arousing or neutral pictures after (Experiment 1) or during (Experiment 2) WP training trials. A 1-wk delayed picture recognition memory test revealed enhanced declarative memory for arousing compared with neutral pictures. Arousal during encoding impaired initial WP acquisition but did not influence retention when tested after a 1-wk delay. Data from a subsequent 3-mo delayed test, however, suggested that arousal during acquisition may enhance remote WP retention. These results suggest a potential dissociation between how readily emotional arousal influences hippocampus-dependent and striatum-dependent memory systems in humans.     

Coordination of multiple memory systems

On the basis of lesions of different brain areas, several neural systems appear to be important for processing information regarding different types of learning and memory. This paper examines the development of pharmacological and neurochemical approaches to multiple memory systems from past studies of modulation of memory formation. The findings suggest that peripheral neuroendocrine mechanisms that regulate memory processing may target their actions toward those neural systems most engaged in the processing of learning and memory. In addition, measurements of acetylcholine release in different memory systems reveals extensive interactions between memory systems, some cooperative and some competitive. These results imply that many neural systems, often characterized as relatively independent, may in fact interact extensively, blurring the dependencies of different memory tasks on specific neural systems.     

Category learning and multiple memory systems

Categorization is a vitally important skill that people use every day. Early theories of category learning assumed a single learning system, but recent evidence suggests that human category learning may depend on many of the major memory systems that have been hypothesized by memory researchers. As different memory systems flourish under different conditions, an understanding of how categorization uses available memory systems will improve our understanding of a basic human skill, lead to better insights into the cognitive changes that result from a variety of neurological disorders, and suggest improvements in training procedures for complex categorization tasks.     

Decisions and the evolution of memory: multiple systems, multiple functions

Memory evolved to supply useful, timely information to the organism's decision-making systems. Therefore, decision rules, multiple memory systems, and the search engines that link them should have coevolved to mesh in a coadapted, functionally interlocking way. This adaptationist perspective suggested the scope hypothesis: When a generalization is retrieved from semantic memory, episodic memories that are inconsistent with it should be retrieved in tandem to place boundary conditions on the scope of the generalization. Using a priming paradigm and a decision task involving person memory, the authors tested and confirmed this hypothesis. The results support the view that priming is an evolved adaptation. They further show that dissociations between memory systems are not--and should not be--absolute: Independence exists for some tasks but not others.     

Differential effects of glucose on modulation of emotional and nonemotional spatial memory tasks

Research examining the memory-enhancing effects of glucose in humans has been limited to mnemonic tasks lacking affective components, even though glucose may be a mechanism for emotioninduced memory enhancement. This limitation does not permit analysis of interactions between the enhancing properties of emotional stimuli and glucose. Participants were administered either glucose or saccharin 15 min prior to completing a neutral or emotional spatial memory task. Performance under three glycemic conditions (100 mg/kg or 50 g glucose, or placebo) for the two sets of emotional stimuli revealed a significant interaction. Both 100-mg/kg and 50-g doses of glucose resulted in impaired performance for emotional stimuli. For neutral stimuli, a 100-mg/kg dose enhanced memory, whereas a 50-g dose showed no effect. Results indicate that the enhancing effects of emotional stimuli may be attenuated by the consumption of glucose and suggest that recent food consumption should be considered in paradigms examining memory.     

The use of acute ethanol administration as a tool to investigate multiple memory systems

The discovery of multiple memory systems supported by discrete brain regions has been one of the most important advances in behavioral neuroscience. A wealth of studies have investigated the role of the hippocampus and related structures in supporting various types of memory classifications. While the exact classification that best describes hippocampal function is often debated, a specific subset of cognitive function that is focused on the use of spatial information to form hippocampal cognitive maps has received extensive investigation. These studies frequently employ a variety of experimental manipulations including brain lesions, temporary neural blockade due to cooling or discrete injections of specific drugs. While these studies have provided important insights into the function of the hippocampus, they are limited due to the invasive nature of the manipulation. Ethanol is a drug that is easily administered in a non-invasive fashion, is rapidly absorbed and produces effects only in specific brain regions. The hippocampus is one brain region affected by acute ethanol administration. The following review summarizes research from the last 20 years investigating the effects of acute ethanol administration on one specific type of hippocampal cognitive function, namely spatial memory. It is proposed that among its many effects, one specific action of acute ethanol administration is to produce similar cognitive and neurophysiological effects as lesions of the hippocampus. Based on these similarities and the ease of its use, it is concluded that acute ethanol administration is a valuable tool in studying hippocampal function and multiple memory systems.     

Acetylcholine modulation of neural systems involved in learning and memory

Extensive evidence supports the view that cholinergic mechanisms modulate learning and memory formation. This paper reviews evidence for cholinergic regulation of multiple memory systems, noting that manipulations of cholinergic functions in many neural systems can enhance or impair memory for tasks generally associated with those neural systems. While parallel memory systems can be identified by combining lesions with carefully crafted tasks, most—if not all—tasks require the combinatorial participation of multiple neural systems. This paper offers the hypothesis that the magnitude of acetylcholine (ACh) release in different neural systems may regulate the relative contributions of these systems to learning. Recent studies of ACh release, obtained with in vivo microdialysis samples during training, together with direct injections of cholinergic drugs into different neural systems, provide evidence that release of ACh is important in engaging these systems during learning, and that the extent to which the systems are engaged is associated with individual differences in learning and memory.     

Evaluating the neuropsychological dissociation evidence for multiple memory systems

This article presents a critical evaluation of the logic and nature of the neuropsychological dissociation evidence that has provided one of the essential lines of support for claims of multiple memory systems--specifically, suggesting that amnesia selectively compromises, and an intact hippocampal system selectively supports, a particular form of memory. An analysis of the existing neuropsychological dissociation evidence is offered in which different classes of evidence--different dissociation approaches-are identified and characterized. The logic of these neuropsychological dissociation approaches is evaluated critically in terms of their ability to distinguish among alternative theoretical views. We conclude that although they support a multiple memory systems account, the findings from these types of neuropsychological dissociation, taken individually and without support from other converging lines of cognitive neuroscience evidence, cannot definitively rule out alternative formulations. A more powerful neuropsychological dissociation approach is then outlined, involving dissociation within condition, that, by more effectively limiting the critical domains of difference between the dissociated performances, can successfully rule out alternative accounts. Its application in Ryan, Althoff, Whitlow, and Cohen (2000) is described, providing strong support for the power of the dissociation within condition approach.     

Personality and emotional memory: How regulating emotion impairs memory for emotional events

In everyday life, individuals actively regulate their emotions in a variety of ways. One common form of emotion regulation is expressive suppression, which entails inhibiting outward signs of emotion. Although expressive suppression is often undertaken with an eye to looking calm despite feeling emotional, an analysis of its self-regulatory demands suggests that this form of emotion regulation may come at a cognitive price. We tested this hypothesis in two studies. In Study 1, we measured spontaneously occurring expressive suppression during a film that depicted a surgical procedure, and then assessed memory for the film. Greater use of suppression predicted worse memory. In Study 2, we examined expressive suppression during a film that depicted a conflictual conversation, and we measured memory for what was said during the conversation. To gauge the magnitude of any cognitive costs, we compared expressive suppression with self-distraction, which entails intentionally trying not to think about something. Both spontaneously occurring and experimentally induced suppression were associated with worse memory. Strikingly, these effects were comparable to the effects of spontaneously occurring and experimentally induced distraction. These studies suggest that “simply” keeping a stiff upper lip during an emotional event exacts a cognitive toll that is as great as intentional cognitive avoidance. We argue that efforts to understand links between emotion and memory must consider emotion regulation.     

Motor action and emotional memory

Can simple motor actions affect how efficiently people retrieve emotional memories, and influence what they choose to remember? In Experiment 1, participants were prompted to retell autobiographical memories with either positive or negative valence, while moving marbles either upward or downward. They retrieved memories faster when the direction of movement was congruent with the valence of the memory (upward for positive, downward for negative memories). Given neutral-valence prompts in Experiment 2, participants retrieved more positive memories when instructed to move marbles up, and more negative memories when instructed to move them down, demonstrating a causal link from motion to emotion. Results suggest that positive and negative life experiences are implicitly associated with schematic representations of upward and downward motion, consistent with theories of metaphorical mental representation. Beyond influencing the efficiency of memory retrieval, the direction of irrelevant, repetitive motor actions can also partly determine the emotional content of the memories people retrieve: moving marbles upward (an ostensibly meaningless action) can cause people to think more positive thoughts.     

Long-term memory for the emotional gist and the emotional essence of an experience

We investigated accuracy in recalling past emotional behaviours and emotionality. Male couples discussed the history of their relationship, and coders rated the extent to which each partner engaged in behaviours such as complimenting or criticising. These ratings were combined into dimensions representing the deeper, emotional essence of that partner's discussion (expressions of We-ness, Fondness, Negativity, and Disappointment). Four years later, participants accurately recalled some of their own and some of their partner's emotional gist-level behaviours, but their answers indicated that they also remembered the emotional essence of the conversation. We conclude that individuals can retain the emotional essence of an experience for a long time, and that they may use this memory to infer, in part, gist-level details of the experience.     

Long-term memory for the emotional gist and the emotional essence of an experience

We investigated accuracy in recalling past emotional behaviours and emotionality. Male couples discussed the history of their relationship, and coders rated the extent to which each partner engaged in behaviours such as complimenting or criticising. These ratings were combined into dimensions representing the deeper, emotional essence of that partner's discussion (expressions of We-ness, Fondness, Negativity, and Disappointment). Four years later, participants accurately recalled some of their own and some of their partner's emotional gist-level behaviours, but their answers indicated that they also remembered the emotional essence of the conversation. We conclude that individuals can retain the emotional essence of an experience for a long time, and that they may use this memory to infer, in part, gist-level details of the experience.     

Modeling single versus multiple systems in implicit and explicit memory

It is currently controversial whether priming on implicit tasks and discrimination on explicit recognition tests are supported by a single memory system or by multiple, independent systems. In a Psychological Review article, Berry and colleagues used mathematical modeling to address this question and provide compelling evidence against the independent-systems approach.     

The use of avoidance training in studies of modulation of memory storage

Studies of the modulatory effects on memory of many treatments have relied in large part on the use of inhibitory (passive) avoidance training procedures. Recent critiques have questioned the validity of data obtained with the inhibitory avoidance task. This paper addresses these comments and describes many of the advantages of using the procedure in studies of processes which regulate the neurobiological mechanisms which store new information.