Neuronal responses related to long-term recognition memory processes in prefrontal cortex

Much evidence indicates that prefrontal cortex plays an important role in long-term recognition memory processes. Here, we report primate prefrontal neuronal responses carrying information necessary for long-term visual recognition memory. The responses of many neurons signaled stimulus familiarity even when the period over which stimuli had to be remembered extended to 24 hr. Such responses occurred frequently in ventromedial, orbitofrontal, and anterior cingulate but not dorsolateral prefrontal cortex. Prefrontal information processing, as indicated by the response latencies, started after that in inferior temporal cortex and might be related to retrieval processes, as responses were typically larger for familiar than for novel stimuli.     

Working memory in primate sensory systems

Sensory working memory consists of the short-term storage of sensory stimuli to guide behaviour. There is increasing evidence that elemental sensory dimensions - such as object motion in the visual system or the frequency of a sound in the auditory system - are stored by segregated feature-selective systems that include not only the prefrontal and parietal cortex, but also areas of sensory cortex that carry out relatively early stages of processing. These circuits seem to have a dual function: precise sensory encoding and short-term storage of this information. New results provide insights into how activity in these circuits represents the remembered sensory stimuli.     

Human dorsal and ventral auditory streams subserve rehearsal-based and echoic processes during verbal working memory

To hear a sequence of words and repeat them requires sensory-motor processing and something more-temporary storage. We investigated neural mechanisms of verbal memory by using fMRI and a task designed to tease apart perceptually based ("echoic") memory from phonological-articulatory memory. Sets of two- or three-word pairs were presented bimodally, followed by a cue indicating from which modality (auditory or visual) items were to be retrieved and rehearsed over a delay. Although delay-period activation in the planum temporale (PT) was insensible to the source modality and showed sustained delay-period activity, the superior temporal gyrus (STG) activated more vigorously when the retrieved items had arrived to the auditory modality and showed transient delay-period activity. Functional connectivity analysis revealed two topographically distinct fronto-temporal circuits, with STG co-activating more strongly with ventrolateral prefrontal cortex and PT co-activating more strongly with dorsolateral prefrontal cortex. These argue for separate contributions of ventral and dorsal auditory streams in verbal working memory.     

Shifting attention within memory representations involves early visual areas

Prior studies have shown that spatial attention modulates early visual cortex retinotopically, resulting in enhanced processing of external perceptual representations. However, it is not clear whether the same visual areas are modulated when attention is focused on, and shifted within a working memory representation. In the current fMRI study participants were asked to memorize an array containing four stimuli. After a delay, participants were presented with a verbal cue instructing them to actively maintain the location of one of the stimuli in working memory. Additionally, on a number of trials a second verbal cue instructed participants to switch attention to the location of another stimulus within the memorized representation. Results of the study showed that changes in the BOLD pattern closely followed the locus of attention within the working memory representation. A decrease in BOLD-activity (V1-V3) was observed at ROIs coding a memory location when participants switched away from this location, whereas an increase was observed when participants switched towards this location. Continuous increased activity was obtained at the memorized location when participants did not switch. This study shows that shifting attention within memory representations activates the earliest parts of visual cortex (including V1) in a retinotopic fashion. We conclude that even in the absence of visual stimulation, early visual areas support shifting of attention within memorized representations, similar to when attention is shifted in the outside world. The relationship between visual working memory and visual mental imagery is discussed in light of the current findings.     

Content-specific working memory modulation of the attentional blink

Three experiments were conducted to investigate the effects of working memory content on temporal attention in a rapid serial visual presentation attentional blink paradigm. It was shown that categorical similarity between working memory content and the target stimuli pertaining to the attentional task (both digits) increased attentional blink magnitude compared to a condition in which this similarity was absent (colors and digits, respectively). This effect was only observed when the items in working memory were not presented as conjunctions of the involved categories (i.e., colored digits). This suggested that storage and retrieval from working memory was at least preferentially conjunctive in this case. It was furthermore shown that the content of working memory enhanced the identification rate of the second target, by means of repetition priming, when inter-target lag was short and the attentional blink was in effect. The results are incompatible with theories of temporal attention that assume working memory has no causal role in the attentional blink and support theories that do.     

Subitization and attentional engagement by transient stimuli

A series of experiments investigated the visual selection of moving and static items during enumeration. Small numbers of visual targets can be enumerated with little increase in reaction time and error with set size, a process referred to as 'subitization'. The number of items that can be subitized' is typically between one and four and known as the subitization range. This study looked for evidence of subitizing of subsets of items presented on a computer display. Fast and accurate enumeration was found for random configurations of moving targets even when presented among static distracters. This was not the case for static targets presented among moving or transient distracters. RTs to these targets were longer and showed a steady increase in RT with target number, even in the subitization range. However, when static targets and moving distracters were presented foveally, fast enumeration/subitization of the static targets was again possible. This was not due to reduced inter-item spacing, since linear effects of the number of targets still emerged when stimuli were presented peripherally but the size-spacing ratio was matched to the foveal presentations. There was indication that instead performance reflected perceived differences in movement speed for stimuli presented in parafoveal and more peripheral retinal regions. In support of this, subitization of static items improved as the movement speed of the distracters increased. The data suggest that the processes supporting subitization are highly sensitive to dynamic stimuli and depend on the ease of segmentation between static and moving arrays.     

See me, hear me, touch me: multisensory integration in lateral occipital-temporal cortex

Our understanding of multisensory integration has advanced because of recent functional neuroimaging studies of three areas in human lateral occipito-temporal cortex: superior temporal sulcus, area LO and area MT (V5). Superior temporal sulcus is activated strongly in response to meaningful auditory and visual stimuli, but responses to tactile stimuli have not been well studied. Area LO shows strong activation in response to both visual and tactile shape information, but not to auditory representations of objects. Area MT, an important region for processing visual motion, also shows weak activation in response to tactile motion, and a signal that drops below resting baseline in response to auditory motion. Within superior temporal sulcus, a patchy organization of regions is activated in response to auditory, visual and multisensory stimuli. This organization appears similar to that observed in polysensory areas in macaque superior temporal sulcus, suggesting that it is an anatomical substrate for multisensory integration. A patchy organization might also be a neural mechanism for integrating disparate representations within individual sensory modalities, such as representations of visual form and visual motion.     

Eye movements predict recollective experience

Previously encountered stimuli can bring to mind a vivid memory of the episodic context in which the stimulus was first experienced ("remembered" stimuli), or can simply seem familiar ("known" stimuli). Past studies suggest that more attentional resources are required to encode stimuli that are subsequently remembered than known. However, it is unclear if the attentional resources are distributed differently during encoding and recognition of remembered and known stimuli. Here, we record eye movements while participants encode photos, and later while indicating whether the photos are remembered, known or new. Eye fixations were more clustered during both encoding and recognition of remembered photos relative to known photos. Thus, recognition of photos that bring to mind a vivid memory for the episodic context in which they were experienced is associated with less distributed overt attention during encoding and recognition. The results suggest that remembering is related to encoding of a few distinct details of a photo rather than the photo as a whole. In turn, during recognition remembering may be trigged by enhanced memory for the salient details of the photos.     

Acoustic facilitation of object movement detection during self-motion

In humans, as well as most animal species, perception of object motion is critical to successful interaction with the surrounding environment. Yet, as the observer also moves, the retinal projections of the various motion components add to each other and extracting accurate object motion becomes computationally challenging. Recent psychophysical studies have demonstrated that observers use a flow-parsing mechanism to estimate and subtract self-motion from the optic flow field. We investigated whether concurrent acoustic cues for motion can facilitate visual flow parsing, thereby enhancing the detection of moving objects during simulated self-motion. Participants identified an object (the target) that moved either forward or backward within a visual scene containing nine identical textured objects simulating forward observer translation. We found that spatially co-localized, directionally congruent, moving auditory stimuli enhanced object motion detection. Interestingly, subjects who performed poorly on the visual-only task benefited more from the addition of moving auditory stimuli. When auditory stimuli were not co-localized to the visual target, improvements in detection rates were weak. Taken together, these results suggest that parsing object motion from self-motion-induced optic flow can operate on multisensory object representations.     

On recency and echoic memory

In short-term memory, the tendency for the last few (recency) items from a verbal sequence to be increasingly well recalled is more pronounced if the items are spoken rather than written. This auditory recency advantage has been quite generally attributed to echoic memory, on the grounds that in the auditory, but not the visual, mode, sensory memory persists just long enough to supplement recall of the most recent items. This view no longer seems tenable. There are now several studies showing that an auditory recency advantage occurs not only in long-term memory, but under conditions in which it cannot possibly be attributed to echoic memory. Also, similar recency phenomena have been discovered in short-term memory when the items are lip-read, or presented in sign-language, rather than heard. This article provides a partial review of these studies, taking a broad theoretical position from which these particular recency phenomena are approached as possible exceptions, to a general theory according to which recency is due to temporal distinctiveness. Much of the fresh evidence reviewed is of a somewhat preliminary nature and it is as yet unexplained by any theory of memory. The need for additional, converging experimental tests is obvious; so too is the need for further theoretical development. Several alternative theoretical resolutions are mentioned, including the possibility that enhanced recency may reflect movement, from sequentially occurring stimulus features, and the suggestion that it may be associated with the primary linguistic mode of the individuals concerned. But special weight is attached to the conjecture that all these recency phenomena might be accounted for in terms of distinctiveness or discriminability. On this view, the enhanced recency effects observed with certain modes, including the auditory mode, are attributed to items possessing greater temporal discriminability in those modes.     

Attention and available long-term memory in an activation-based model

The influence of attention on memorizing related items and on available long-term memory (ALTM) was explored, showing that N400 of no-memory items was more negative than that of the memory item. The results of the category comparison task indicated that information processing under attention-driven in WM determined the availability of related long-term memory, i.e., specific content, which was formerly concerned or ignored, yielding different indirect semantic priming effects. These indicate that the orientation of conceptual attention leads the related representations of LTM to diverse activation patterns, supporting the activation-based model.     

Modelling neural informational propagation and functional auditory sensory memory with temporal multi-scale operators

In this paper we prove that both diffusion and the leaky integrators cascade based transport mechanisms have as their inherent property the effect of temporal multi-scaling. The two transport mechanisms are modeled not as convolution based algorithms but as causal physical processes. This implies that propagation of information through a neural map may act as a mechanism for achieving temporal multi-scale analysis in the auditory system. Specifically, we are interested in the effects of such a transport process on the formation and the dynamics of auditory sensory memory. Two temporal models of information propagation are discussed and compared in terms of their ability to model auditory sensory memory effects and the biological plausibility of their structure: the causal diffusion based operator (CD) and the leaky integrator cascade based operator (LINC). We show that temporal multi-scale representations achieved by both models exhibit the effects similar to those of auditory sensory memory (filtering, time delay and binding of information). As regards higher-level functions of auditory sensory memory such as change detection, the LINC operator seems to be a biologically more plausible solution for modeling temporal cortical processing.     

Uncovering camouflage: amygdala activation predicts long-term memory of induced perceptual insight

What brain mechanisms underlie learning of new knowledge from single events? We studied encoding in long-term memory of a unique type of one-shot experience, induced perceptual insight. While undergoing an fMRI brain scan, participants viewed degraded images of real-world pictures where the underlying objects were hard to recognize ("camouflage"), followed by brief exposures to the original images ("solution"), which led to induced insight ("Aha!"). A week later, the participants' memory was tested; a solution image was classified as "remembered" if detailed perceptual knowledge was elicited from the camouflage image alone. During encoding, subsequently remembered images were associated with higher activity in midlevel visual cortex and medial frontal cortex, but most pronouncedly, in the amygdala, whose activity could be used to predict which solutions will remain in long-term memory. Our findings extend the known roles of amygdala in memory to include promotion of long-term memory of the sudden reorganization of internal representations.     

Retrieval Intention Modulates the Effects of Directed Forgetting Instructions on Recollection

The neurocognitive basis of memory retrieval is often examined by investigating brain potential old/new effects, which are differences in brain activity between successfully remembered repeated stimuli and correctly rejected new stimuli in a recognition test. In this study, we combined analyses of old/new effects for words with an item-method directed-forgetting manipulation in order to isolate differences between the retrieval processes elicited by words that participants were initially instructed to commit to memory and those that participants were initially instructed to forget. We compared old/new effects elicited by to-be-forgotten (TBF) words with those elicited by to-be-remembered (TBR) words in both an explicit-memory test (a recognition test) and an implicit-memory test (a lexical-decision test). Behavioral results showed clear directed forgetting effects in the recognition test, but not in the lexical decision test. Mirroring the behavioral findings, analyses of brain potentials showed evidence of directed forgetting only in the recognition test. In this test, potentials from 450–650 ms (P600 old/new effects) were more positive for TBR relative to TBF words. By contrast, P600 effects evident during the lexical-decision test did not differ in magnitude between TBR and TBF items. When taken in the context of prior studies that have linked similar parietal old/new effects to the recollection of episodic information, these data suggest that directed-forgetting effects manifest primarily in greater episodic retrieval by TBR than TBF items, and that retrieval intention may be important for these directed-forgetting effects to occur.     

Auditory event-related potentials dissociate early and late memory processes

Event-related potentials (ERPs) to environmental sounds were recorded from 15 young control subjects in an auditory recognition memory task. Subjects listened to a continuous string of binaurally presented sounds, 20% of which were presented once and 80% were repeated. Of the repeated sounds, some repeated immediately after the initial presentation (2 sec; short delay repetition) while others repeated after 2–6 intervening sounds (4–12 sec; long delay repetition). Subjects were instructed to indicate whether they had heard the sounds before by pressing a “yes” or “no” button.The initial stimulus presentation and long delay repetition stimuli generated both an N4 component and a prolonged latency P3 component while the short delay repetition stimuli elicited no N4 component and an earlier latency P3 component. Subjects' responses were faster and more accurate for short delay repetition. All stimuli generated a sustained frontal negative component (SFN). These data indicate that auditory recognition memory for environmental sounds may involve two processes. The P3 generated by both short and long delay repetition stimuli may index activation of a neocortical template matching system. The N4 generated by initial stimulus presentations and long delay repetition is proposed to measure additional activation of limbic memory systems at long retention intervals.     

Activity in both hippocampus and perirhinal cortex predicts the memory strength of subsequently remembered information

It has been suggested that hippocampal activity predicts subsequent recognition success when recognition decisions are based disproportionately on recollection, whereas perirhinal activity predicts recognition success when decisions are based primarily on familiarity. Another perspective is that both hippocampal and perirhinal activity are predictive of overall memory strength. We tested the relationship between brain activity during learning and subsequent memory strength. Activity in a number of cortical regions (including regions within the "default network") was negatively correlated with subsequent memory strength, suggesting that this activity reflects inattention or mind wandering (and, consequently, poor memory). In contrast, activity in both hippocampus and perirhinal cortex positively correlated with the subsequent memory strength of remembered items. This finding suggests that both structures cooperate during learning to determine the memory strength of what is being learned.     

Distinct Effects of Memory Retrieval and Articulatory Preparation when Learning and Accessing New Word Forms

Temporal and frontal activations have been implicated in learning of novel word forms, but their specific roles remain poorly understood. The present magnetoencephalography (MEG) study examines the roles of these areas in processing newly-established word form representations. The cortical effects related to acquiring new phonological word forms during incidental learning were localized. Participants listened to and repeated back new word form stimuli that adhered to native phonology (Finnish pseudowords) or were foreign (Korean words), with a subset of the stimuli recurring four times. Subsequently, a modified 1-back task and a recognition task addressed whether the activations modulated by learning were related to planning for overt articulation, while parametrically added noise probed reliance on developing memory representations during effortful perception. Learning resulted in decreased left superior temporal and increased bilateral frontal premotor activation for familiar compared to new items. The left temporal learning effect persisted in all tasks and was strongest when stimuli were embedded in intermediate noise. In the noisy conditions, native phonotactics evoked overall enhanced left temporal activation. In contrast, the frontal learning effects were present only in conditions requiring overt repetition and were more pronounced for the foreign language. The results indicate a functional dissociation between temporal and frontal activations in learning new phonological word forms: the left superior temporal responses reflect activation of newly-established word-form representations, also during degraded sensory input, whereas the frontal premotor effects are related to planning for articulation and are not preserved in noise.     

Rhesus monkeys see who they hear: spontaneous cross-modal memory for familiar conspecifics

Rhesus monkeys gather much of their knowledge of the social world through visual input and may preferentially represent this knowledge in the visual modality. Recognition of familiar faces is clearly advantageous, and the flexibility and utility of primate social memory would be greatly enhanced if visual memories could be accessed cross-modally either by visual or auditory stimulation. Such cross-modal access to visual memory would facilitate flexible retrieval of the knowledge necessary for adaptive social behavior. We tested whether rhesus monkeys have cross-modal access to visual memory for familiar conspecifics using a delayed matching-to-sample procedure. Monkeys learned visual matching of video clips of familiar individuals to photographs of those individuals, and generalized performance to novel videos. In crossmodal probe trials, coo-calls were played during the memory interval. The calls were either from the monkey just seen in the sample video clip or from a different familiar monkey. Even though the monkeys were trained exclusively in visual matching, the calls influenced choice by causing an increase in the proportion of errors to the picture of the monkey whose voice was heard on incongruent trials. This result demonstrates spontaneous cross-modal recognition. It also shows that viewing videos of familiar monkeys activates naturally formed memories of real monkeys, validating the use of video stimuli in studies of social cognition in monkeys.     

Sleep-related hippocampo-cortical interplay during emotional memory recollection

Emotional events are usually better remembered than neutral ones. This effect is mediated in part by a modulation of the hippocampus by the amygdala. Sleep plays a role in the consolidation of declarative memory. We examined the impact of sleep and lack of sleep on the consolidation of emotional (negative and positive) memories at the macroscopic systems level. Using functional MRI (fMRI), we compared the neural correlates of successful recollection by humans of emotional and neutral stimuli, 72 h after encoding, with or without total sleep deprivation during the first post-encoding night. In contrast to recollection of neutral and positive stimuli, which was deteriorated by sleep deprivation, similar recollection levels were achieved for negative stimuli in both groups. Successful recollection of emotional stimuli elicited larger responses in the hippocampus and various cortical areas, including the medial prefrontal cortex, in the sleep group than in the sleep deprived group. This effect was consistent across subjects for negative items but depended linearly on individual memory performance for positive items. In addition, the hippocampus and medial prefrontal cortex were functionally more connected during recollection of either negative or positive than neutral items, and more so in sleeping than in sleep-deprived subjects. In the sleep-deprived group, recollection of negative items elicited larger responses in the amygdala and an occipital area than in the sleep group. In contrast, no such difference in brain responses between groups was associated with recollection of positive stimuli. The results suggest that the emotional significance of memories influences their sleep-dependent systems-level consolidation. The recruitment of hippocampo-neocortical networks during recollection is enhanced after sleep and is hindered by sleep deprivation. After sleep deprivation, recollection of negative, potentially dangerous, memories recruits an alternate amygdalo-cortical network, which would keep track of emotional information despite sleep deprivation.     

Learning-induced plasticity in animal and human auditory cortex

Recent data on learning-related changes in animal and human auditory cortex indicate functions beyond mere stimulus representation and simple recognition memory for stimuli. Rather, auditory cortex seems to process and represent stimuli in a task-dependent fashion. This implies plasticity in neural processing, which can be observed at the level of single neuron firing and the level of spatiotemporal activity patterns in cortical areas. Auditory cortex is a structure in which behaviorally relevant aspects of stimulus processing are highly developed because of the fugitive nature of auditory stimuli.