Neural representations in human spatial memory

Ekstrom et al. report the responses of single neurons recorded from the brains of human subjects performing a spatial navigation task in virtual reality. They found cells encoding the subject's current location, view and destination. These data, and related findings in animals, directly reveal some of the representations underlying spatial cognition. They highlight the potential for cognitive psychology and systems neuroscience to combine to provide a neuronal-level understanding of human behaviour.     

Direct retrieval from elaborated memory traces

Four experiments were performed to investigate the beneficial effects of elaborative processing on recall performance. Specifically, the experiments investigated J. R. Anderson's (1983) claim that increasing the number of associative pathways between propositions in a memory trace improves recall performance through direct retrieval. In this study, procedures were used that allowed the amount of elaboration to be systematically varied while the use of inferential reconstruction to aid recall was eliminated, thus providing a test of J. R. Anderson's model. Across all experiments, the results showed that recall of a name was better when it had been stored in a less elaborated memory trace. The results suggest that when reconstructive processes are eliminated, elaboration decreases rather than increases recall performance.     

From sensory to long-term memory: evidence from auditory memory reactivation studies

Everyday experience tells us that some types of auditory sensory information are retained for long periods of time. For example, we are able to recognize friends by their voice alone or identify the source of familiar noises even years after we last heard the sounds. It is thus somewhat surprising that the results of most studies of auditory sensory memory show that acoustic details, such as the pitch of a tone, fade from memory in ca. 10-15 s. One should, therefore, ask (1) what types of acoustic information can be retained for a longer term, (2) what circumstances allow or help the formation of durable memory records for acoustic details, and (3) how such memory records can be accessed. The present review discusses the results of experiments that used a model of auditory recognition, the auditory memory reactivation paradigm. Results obtained with this paradigm suggest that the brain stores features of individual sounds embedded within representations of acoustic regularities that have been detected for the sound patterns and sequences in which the sounds appeared. Thus, sounds closely linked with their auditory context are more likely to be remembered. The representations of acoustic regularities are automatically activated by matching sounds, enabling object recognition.     

Retrieval from semantic memory during a night without sleep

It has been demonstrated that retrieval performance from semantic memory varies during the day. Specifically, the retrieval of low- relative to high-dominance category members is slower in the morning compared to later in the day. It has been suggested that the effect is related to a circadian arousal rhythm, which steadily rises during the day and rapidly declines at night. This study examines retrieval from semantic memory during the night. Sixteen subjects performed a semantic classification task once every hour throughout one night without sleep. Classification latencies became progressively slower, and the time taken to retrieve low- relative to high-dominance category members increased from midnight to 4 a.m. The trend reversed between 4 and 7 a.m. The pattern of results closely parallels the hypothesised circadian arousal rhythm. It is suggested that the variation in retrieval performance as a function of time of day may be related to fluctuations in a circadian arousal rhythm.     

The basolateral amygdala modulates specific sensory memory representations in the cerebral cortex

Stress hormones released by an experience can modulate memory strength via the basolateral amygdala, which in turn acts on sites of memory storage such as the cerebral cortex [McGaugh, J. L. (2004). The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annual Review of Neuroscience, 27, 1–28]. Stimuli that acquire behavioral importance gain increased representation in the cortex. For example, learning shifts the tuning of neurons in the primary auditory cortex (A1) to the frequency of a conditioned stimulus (CS), and the greater the level of CS importance, the larger the area of representational gain [Weinberger, N. M. (2007). Associative representational plasticity in the auditory cortex: A synthesis of two disciplines. Learning & Memory, 14(1–2), 1–16]. The two lines of research suggest that BLA strengthening of memory might be accomplished in part by increasing the representation of an environmental stimulus. The present study investigated whether stimulation of the BLA can affect cortical memory representations. In male Sprague–Dawley rats studied under urethane general anesthesia, frequency receptive fields were obtained from A1 before and up to 75 min after the pairing of a tone with BLA stimulation (BLAstm: 100 trials, 400 ms, 100 Hz, 400 μA [±16.54]). Tone started before and continued after BLAstm. Group BLA/1.0 (n = 16) had a 1 s CS–BLAstm interval while Group BLA/1.6 (n = 5) has a 1.6 s interval. The BLA/1.0 group did develop specific tuning shifts toward and to the CS, which could change frequency tuning by as much as two octaves. Moreover, its shifts increased over time and were enduring, lasting 75 min. However, group BLA/1.6 did not develop tuning shifts, indicating that precise CS–BLAstm timing is important in the anesthetized animal. Further, training in the BLA/1.0 paradigm but stimulating outside of the BLA did not produce tuning shifts. These findings demonstrate that the BLA is capable of exerting highly specific, enduring, learning-related modifications of stimulus representation in the cerebral cortex. These findings suggest that the ability of the BLA to alter specific cortical representations may underlie, at least in part, the modulatory influence of BLA activity on strengthening long-term memory.     

Information processing during sleep onset and sleep.

This Special Section examines the extent of information processing during sleep onset and sleep itself. It is generally agreed that, stimulus input is markedly inhibited during sleep, thus preventing conscious awareness of the external environment. Overt behavioural responses are rarely made within sleep. Two neurophysiological measures are therefore often used. The electrical activity of the brain (the EEG) can be employed to distinguish waking (conscious) from sleeping (unconscious) states. It is also possible to quantify the EEG prior to and following a detection (or a failure of a detection) of a stimulus. Such measures can thus be used to predict conscious awareness. A second measure that frequently has been employed is the brain's response to an external stimulus (the evoked potential). Different components of the evoked potential can be used to trace the extent of information processing during the different states of consciousness. Some are associated with a preconscious detection while others are associated with conscious awareness. Other evoked potentials may be unique to sleep.     

Accessing long-term memory representations during visual change detection

In visual change detection tasks, providing a cue to the change location concurrent with the test image (post-cue) can improve performance, suggesting that, without a cue, not all encoded representations are automatically accessed. Our studies examined the possibility that post-cues can encourage the retrieval of representations stored in long-term memory (LTM). Participants detected changes in images composed of familiar objects. Performance was better when the cue directed attention to the post-change object. Supporting the role of LTM in the cue effect, the effect was similar regardless of whether the cue was presented during the inter-stimulus interval, concurrent with the onset of the test image, or after the onset of the test image. Furthermore, the post-cue effect and LTM performance were similarly influenced by encoding time. These findings demonstrate that monitoring the visual world for changes does not automatically engage LTM retrieval.     

System consolidation of memory during sleep

Over the past two decades, research has accumulated compelling evidence that sleep supports the formation of long-term memory. The standard two-stage memory model that has been originally elaborated for declarative memory assumes that new memories are transiently encoded into a temporary store (represented by the hippocampus in the declarative memory system) before they are gradually transferred into a long-term store (mainly represented by the neocortex), or are forgotten. Based on this model, we propose that sleep, as an offline mode of brain processing, serves the ‘active system consolidation’ of memory, i.e. the process in which newly encoded memory representations become redistributed to other neuron networks serving as long-term store. System consolidation takes place during slow-wave sleep (SWS) rather than rapid eye movement (REM) sleep. The concept of active system consolidation during sleep implicates that (a) memories are reactivated during sleep to be consolidated, (b) the consolidation process during sleep is selective inasmuch as it does not enhance every memory, and (c) memories, when transferred to the long-term store undergo qualitative changes. Experimental evidence for these three central implications is provided: It has been shown that reactivation of memories during SWS plays a causal role for consolidation, that sleep and specifically SWS consolidates preferentially memories with relevance for future plans, and that sleep produces qualitative changes in memory representations such that the extraction of explicit and conscious knowledge from implicitly learned materials is facilitated.     

Attention to memory: orienting attention to sound object representations

Despite a growing acceptance that attention and memory interact, and that attention can be focused on an active internal mental representation (i.e., reflective attention), there has been a paucity of work focusing on reflective attention to ‘sound objects’ (i.e., mental representations of actual sound sources in the environment). Further research on the dynamic interactions between auditory attention and memory, as well as its degree of neuroplasticity, is important for understanding how sound objects are represented, maintained, and accessed in the brain. This knowledge can then guide the development of training programs to help individuals with attention and memory problems. This review article focuses on attention to memory with an emphasis on behavioral and neuroimaging studies that have begun to explore the mechanisms that mediate reflective attentional orienting in vision and more recently, in audition. Reflective attention refers to situations in which attention is oriented toward internal representations rather than focused on external stimuli. We propose four general principles underlying attention to short-term memory. Furthermore, we suggest that mechanisms involved in orienting attention to visual object representations may also apply for orienting attention to sound object representations.     

Abstract versus modality-specific memory representations in processing auditory and visual speech

Serial recall of lip-read, auditory, and audiovisual memory lists with and without a verbal suffix was examined. Recency effects were the same in the three presentation modalities. The disrupting effect of a suffix was largest when it was presented in the same modality as the list items. The results suggest that abstract linguistic as well as modality-specific codes play a role in memory for auditory and visual speech.     

Declarative memory consolidation: mechanisms acting during human sleep

Of late, an increasing number of studies have shown a strong relationship between sleep and memory. Here we summarize a series of our own studies in humans supporting a beneficial influence of slow-wave sleep (SWS) on declarative memory formation, and try to identify some mechanisms that might underlie this influence. Specifically, these experiments show that declarative memory benefits mainly from sleep periods dominated by SWS, whereas there is no consistent benefit of this memory from periods rich in rapid eye movement (REM) sleep. A main mechanism of declarative memory formation is believed to be the reactivation of newly acquired memory representations in hippocampal networks that stimulates a transfer and integration of these representations into neocortical neuronal networks. Consistent with this model, spindle activity and slow oscillation-related EEG coherence increase during early sleep after intense declarative learning in humans, signs that together point toward a neocortical reprocessing of the learned material. In addition, sleep seems to provide an optimal milieu for declarative memory reprocessing and consolidation by reducing cholinergic activation and the cortisol feedback to the hippocampus during SWS.     

Pseudocontingencies derived from categorically organized memory representations

Pseudocontingencies (PCs) allow for inferences about the contingency between two variables X and Y when the conditions for genuine contingency assessment are not met. Even when joint observations X _i and Y _i about the same reference objects i are not available or are detached in time or space, the correlation r(X _i ,Y _i ) is readily inferred from base rates. Inferred correlations are positive (negative) if X and Y base rates are skewed in the same (different) directions. Such PC inferences afford useful proxies for actually existing contingencies. While previous studies have focused on PCs due to environmental base rates, the present research highlights memory organization as a natural source of PC effects. When information about two attributes X and Y is represented in a hierarchically organized categorical memory code, as category-wise base rates p(X) and p(Y), the reconstruction of item-level information from category base rates will naturally produce PC effects. Three experiments support this contention. When the yes base rates of two respondents in four questionnaire subscales (categories) were correlated, recalled and predicted item-level responses were correlated in the same direction, even when the original responses to specific items within categories were correlated in the opposite direction.     

Neural processing associated with true and false memory retrieval

We investigated the neural bases for false memory with fMRI by examining neural activity during retrieval processes that yielded true or false memories. We used a reality monitoring paradigm in which participants saw or imagined pictures of concrete objects. (A subsequent misinformation task was also used to increase false memory rates.) At test, fMRI data were collected as the participants determined whether they had seen or had only imagined the object at study. True memories were of seen pictures accurately endorsed as seen, and for false memories were of imagined pictures falsely endorsed as seen. Three distinct patterns of activity were observed: Left frontal and parietal activity was not different for true and for false memories, whereas activity was greater for true than for false memories in occipital visual regions and posterior portions of the parahippocampal gyrus, and activity was greater for false than for true memories in right anterior cingulate gyrus. Possible interpretations are discussed.     

Age-related changes in processing auditory stimuli during visual attention: evidence for deficits in inhibitory control and sensory memory.

Age-related declines in attention and cognition have been associated with a difficulty in inhibiting the processing of task-irrelevant information (i.e., the inhibitory deficit hypothesis). However, evidence supporting the inhibitory deficit hypothesis remains equivocal, in part because of complexities in examining the processing of irrelevant stimuli using purely behavioral techniques. The effects of age on the processing of task-irrelevant stimuli were examined using scalp-recorded event-related brain potentials. Participants performed a visual discrimination task while standard and deviant auditory stimuli were presented in the background. Deviant auditory stimuli generated a mismatch negativity (MMN) wave that decreased with age, in part because of an age-related enhancement in sensory-evoked responses. The age-related changes in processing task-irrelevant auditory stimuli are consistent with the inhibitory deficit hypothesis and suggest that impaired inhibitory control of sensory input may play a role in the age-related declines in performance during selective attention tasks.     

ERPs studies of cognitive processing during sleep

In the last few decades, several works on cognitive processing during sleep have emerged. The study of cognitive processing with event related potentials (ERPs) during sleep is a topic of great interest, since ERPs allow the study of stimulation with passive paradigms (without conscious response or behavioural response), opening multiple research possibilities during different sleep phases. We review ERPs modulated by cognitive processes during sleep: N1, Mismatch Negativity (MMN), P2, P3, N400-like, N300-N550, among others. The review shows that there are different cognitive discriminations during sleep related to the frequency, intensity, duration, saliency, novelty, proportion of appearance, meaning, and even sentential integration of stimuli. The fascinating results of cognitive processing during sleep imply serious challenges for cognitive models. The studies of ERPs, together with techniques of neuroimaging, have demonstrated the existence of cognitive processing during sleep. A fundamental question to be considered is if these cognitive phenomena are similar to processing that occurs during wakefulness. Based on this question we discussed the existence of possible mechanisms associated with sleep, as well as the specific cognitive and neurophysiologic differences of wakefulness and sleep. Much knowledge is still required to even understand the conjunction of dramatic changes in cerebral dynamics and the occurrence of cognitive processes. We propose some insights based on ERPs research for further construction of theoretical models for integrating both cognitive processing and specific brain sleep dynamics.     

Gender differences in memory processing: evidence from event-related potentials to faces

This study investigated gender differences on memory processing using event-related potentials (ERPs). Behavioral data and ERPs were recorded in 16 males and 10 females during a recognition memory task for faces. The behavioral data results showed that females performed better than males. Gender differences on ERPs were evidenced over anterior locations and involve the modulation of two spatially and temporally distinct components. These results are in general accordance with the view that males and females differ in the cognitive strategies they use to process information. Specifically, they could differ in their abilities to maintain information over interference and in the processing of the intrinsic contextual attributes of items, respectively, associated with the modulation of two anterior components. These interpretations lend support to the view that processing in females entails more detailed elaboration of information content than in males. Processing in males is more likely driven by schemas or overall information theme.     

Information processing during general anesthesia: Evidence for unconscious memory

Memory for words presented during general anesthesia was studied in two experiments. In Experiment 1, surgical patients (n=80) undergoing elective procedures under general anesthesia were presented shortly before and during surgery with words via headphones. At the earliest convenient time after surgery (within 5 h) and 24 h later, memory was tested by asking patients to complete auditorily presented word stems with the first word that came to mind and to leave out words they remembered having heard earlier (exclusion task). Moreover, patients were requested to perform a “yes/no” forcedchoice recognition task to assess recognition memory for both the pre- and intraoperative words. Memory for the material presented during anesthesia was demonstrated immediately after surgery and 24 h later by means of both tasks. In a second similar experiment (n=80), the results were replicated. These findings show that anesthetized patients can process information that was presented intraoperatively.     

Using selective interference to investigate spatial memory representations

Two experiments used a selective interference procedure in an attempt to determine whether nonverbal visual stimuli were represented in memory in a verbal or spatial format. A spatial representation was clearly implicated. In both experiments, Ss were required to remember either the positions or the identities of seven target items in a 25-item array. During the retention interval for that information, Ss attempted to recognize schematic face or airplane photograph stimuli in a same-different memory task. Memory performance on one or both tasks was greatly impaired when the recall task involved position or spatial information, but was either much less or not at all affected by an identity or verbal information recall task. Because of the selective nature of the interference and on the basis of certain correlational evidence, the experimental results were also interpreted as providing support for the notion that verbal and spatial information are stored and processed in separate information-processing systems.     

The role of auditory memory traces in attention to frequency

Three cued signal detection experiments demonstrated a role for auditory memory traces in frequency selectivity. The extent to which the cue predicted the signal frequency affected the size of the advantage for signals at the cue frequency over those at distant frequencies when the cue-signal gap was 10 sec but not when it was 1 sec. Detection of occasional signals presented at uncued frequencies was enhanced when they matched the frequency of cues from recent trials. With "relative" cues, which were usually followed by signals at the musical fifth above the cue frequency, performance on occasional signals at the cue frequency was enhanced relative to other unexpected frequencies. These results suggest that, regardless of the listener's expectations and intentions, the detectability of a signal is enhanced if its frequency matches an existing memory trace. One form of voluntary attention to frequency may involve maintaining traces that would otherwise slowly decay.