Short-term Memory Trace Research Articles

A short-term memory trace persists for days in the mouse hippocampus

Active recall of short-term memory (STM) is known to last for a few hours, but whether STM has long-term functions is unknown. Here we show that STM can be optogenetically retrieved at a time point during which natural recall is not possible, uncovering the long-term existence of an STM engram. Moreover, re-training within 3 days led to natural long-term recall, indicating facilitated consolidation. Inhibiting offline CA1 activity during non-rapid eye movement (NREM) sleep, N-methyl-D-aspartate receptor (NMDAR) activity, or protein synthesis after first exposure to the STM-forming event impaired the future re-exposure-facilitated consolidation, which highlights a role of protein synthesis, NMDAR and NREM sleep in the long-term storage of an STM trace. These results provide evidence that STM is not completely lost within hours and demonstrates a possible two-step STM consolidation, first long-term storage as a behaviorally inactive engram, then transformation into an active state by recurrence within 3 days.

Astrocytes mediate analogous memory in a multi-layer neuron–astrocyte network

Modeling the neuronal processes underlying short-term working memory remains the focus of many theoretical studies in neuroscience. In this paper, we propose a mathematical model of a spiking neural network (SNN) which simulates the way a fragment of information is maintained as a robust activity pattern for several seconds and the way it completely disappears if no other stimuli are fed to the system. Such short-term memory traces are preserved due to the activation of astrocytes accompanying the SNN. The astrocytes exhibit calcium transients at a time scale of seconds. These transients further modulate the efficiency of synaptic transmission and, hence, the firing rate of neighboring neurons at diverse timescales through gliotransmitter release. We demonstrate how such transients continuously encode frequencies of neuronal discharges and provide robust short-term storage of analogous information. This kind of short-term memory can store relevant information for seconds and then completely forget it to avoid overlapping with forthcoming patterns. The SNN is inter-connected with the astrocytic layer by local inter-cellular diffusive connections. The astrocytes are activated only when the neighboring neurons fire synchronously, e.g., when an information pattern is loaded. For illustration, we took grayscale photographs of people’s faces where the shades of gray correspond to the level of applied current which stimulates the neurons. The astrocyte feedback modulates (facilitates) synaptic transmission by varying the frequency of neuronal firing. We show how arbitrary patterns can be loaded, then stored for a certain interval of time, and retrieved if the appropriate clue pattern is applied to the input.

Temporal dynamics of implicit memory underlying serial dependence.

Serial dependence is the effect in which the immediately preceding trial influences participants' responses to the current stimulus. But for how long does this bias last in the absence of interference from other stimuli? Here, we had 20 healthy young adult participants (12 women) perform a coincident timing task using different inter-trial intervals to characterize the serial dependence effect as the time between trials increases. Our results show that serial dependence abruptly decreases from 0.1 s to 1 s inter-trial interval, but it remains pronounced after that for up to 8 s. In addition, participants' response variability slightly decreases over longer intervals. We discuss these results in light of recent models suggesting that serial dependence might rely on a short-term memory trace kept through changes in synaptic weights, which might explain its long duration and apparent stability over time.

Learning Invariant Object and Spatial View Representations in the Brain Using Slow Unsupervised Learning.

First, neurophysiological evidence for the learning of invariant representations in the inferior temporal visual cortex is described. This includes object and face representations with invariance for position, size, lighting, view and morphological transforms in the temporal lobe visual cortex; global object motion in the cortex in the superior temporal sulcus; and spatial view representations in the hippocampus that are invariant with respect to eye position, head direction, and place. Second, computational mechanisms that enable the brain to learn these invariant representations are proposed. For the ventral visual system, one key adaptation is the use of information available in the statistics of the environment in slow unsupervised learning to learn transform-invariant representations of objects. This contrasts with deep supervised learning in artificial neural networks, which uses training with thousands of exemplars forced into different categories by neuronal teachers. Similar slow learning principles apply to the learning of global object motion in the dorsal visual system leading to the cortex in the superior temporal sulcus. The learning rule that has been explored in VisNet is an associative rule with a short-term memory trace. The feed-forward architecture has four stages, with convergence from stage to stage. This type of slow learning is implemented in the brain in hierarchically organized competitive neuronal networks with convergence from stage to stage, with only 4-5 stages in the hierarchy. Slow learning is also shown to help the learning of coordinate transforms using gain modulation in the dorsal visual system extending into the parietal cortex and retrosplenial cortex. Representations are learned that are in allocentric spatial view coordinates of locations in the world and that are independent of eye position, head direction, and the place where the individual is located. This enables hippocampal spatial view cells to use idiothetic, self-motion, signals for navigation when the view details are obscured for short periods.

Neurophysiological Correlates of Asymmetries in Vowel Perception: An English-French Cross-Linguistic Event-Related Potential Study.

Behavioral studies examining vowel perception in infancy indicate that, for many vowel contrasts, the ease of discrimination changes depending on the order of stimulus presentation, regardless of the language from which the contrast is drawn and the ambient language that infants have experienced. By adulthood, linguistic experience has altered vowel perception; analogous asymmetries are observed for non−native contrasts but are mitigated for native contrasts. Although these directional effects are well documented behaviorally, the brain mechanisms underlying them are poorly understood. In the present study we begin to address this gap. We first review recent behavioral work which shows that vowel perception asymmetries derive from phonetic encoding strategies, rather than general auditory processes. Two existing theoretical models–the Natural Referent Vowel framework and the Native Language Magnet model–are invoked as a means of interpreting these findings. Then we present the results of a neurophysiological study which builds on this prior work. Using event-related brain potentials, we first measured and assessed the mismatch negativity response (MMN, a passive neurophysiological index of auditory change detection) in English and French native-speaking adults to synthetic vowels that either spanned two different phonetic categories (/y/vs./u/) or fell within the same category (/u/). Stimulus presentation was organized such that each vowel was presented as standard and as deviant in different blocks. The vowels were presented with a long (1,600-ms) inter-stimulus interval to restrict access to short-term memory traces and tap into a “phonetic mode” of processing. MMN analyses revealed weak asymmetry effects regardless of the (i) vowel contrast, (ii) language group, and (iii) MMN time window. Then, we conducted time-frequency analyses of the standard epochs for each vowel. In contrast to the MMN analysis, time-frequency analysis revealed significant differences in brain oscillations in the theta band (4–8 Hz), which have been linked to attention and processing efficiency. Collectively, these findings suggest that early-latency (pre-attentive) mismatch responses may not be a strong neurophysiological correlate of asymmetric behavioral vowel discrimination. Rather, asymmetries may reflect differences in neural processing efficiency for vowels with certain inherent acoustic-phonetic properties, as revealed by theta oscillatory activity.

A Path Toward Explainable AI and Autonomous Adaptive Intelligence: Deep Learning, Adaptive Resonance, and Models of Perception, Emotion, and Action.

Biological neural network models whereby brains make minds help to understand autonomous adaptive intelligence. This article summarizes why the dynamics and emergent properties of such models for perception, cognition, emotion, and action are explainable, and thus amenable to being confidently implemented in large-scale applications. Key to their explainability is how these models combine fast activations, or short-term memory (STM) traces, and learned weights, or long-term memory (LTM) traces. Visual and auditory perceptual models have explainable conscious STM representations of visual surfaces and auditory streams in surface-shroud resonances and stream-shroud resonances, respectively. Deep Learning is often used to classify data. However, Deep Learning can experience catastrophic forgetting: At any stage of learning, an unpredictable part of its memory can collapse. Even if it makes some accurate classifications, they are not explainable and thus cannot be used with confidence. Deep Learning shares these problems with the back propagation algorithm, whose computational problems due to non-local weight transport during mismatch learning were described in the 1980s. Deep Learning became popular after very fast computers and huge online databases became available that enabled new applications despite these problems. Adaptive Resonance Theory, or ART, algorithms overcome the computational problems of back propagation and Deep Learning. ART is a self-organizing production system that incrementally learns, using arbitrary combinations of unsupervised and supervised learning and only locally computable quantities, to rapidly classify large non-stationary databases without experiencing catastrophic forgetting. ART classifications and predictions are explainable using the attended critical feature patterns in STM on which they build. The LTM adaptive weights of the fuzzy ARTMAP algorithm induce fuzzy IF-THEN rules that explain what feature combinations predict successful outcomes. ART has been successfully used in multiple large-scale real world applications, including remote sensing, medical database prediction, and social media data clustering. Also explainable are the MOTIVATOR model of reinforcement learning and cognitive-emotional interactions, and the VITE, DIRECT, DIVA, and SOVEREIGN models for reaching, speech production, spatial navigation, and autonomous adaptive intelligence. These biological models exemplify complementary computing, and use local laws for match learning and mismatch learning that avoid the problems of Deep Learning.

Alexithymia disrupts verbal short-term memory

ABSTRACT While some research has now started to suggest that there are long-term memory (LTM) deficits in alexithymia, short-term memory (STM) in alexithymia remained largely unexplored. This study investigated whether the STM trace for emotion and neutral words might also be disrupted by alexithymia. Forty-four participants were randomly assigned to Study 1 in which the to-be-memorised six-word lists were composed of words belonging to the same valence (i.e. pure lists condition, Study 1), and 44 other participants were randomly assigned to Study 2 in which six-word lists were composed of embedded neutral and emotional words (i.e. mixed lists condition). All the participants completed the Toronto-Alexithymia Scale (TAS-20) and a current mood states scale (PANAS). Results showed that the main effect of alexithymia was observed in the pure lists condition while no alexithymia groups effect emerged in the mixed lists condition. In the pure lists condition only correlation analyses confirmed that alexithymia significantly and negatively correlated with recall accuracy. The results are discussed with regard to the influence of alexithymia on the proposed role of (1) semantic organisation of LTM on STM performance in the pure lists condition and (2) attentional capture by emotional words in the mixed lists condition.

Visual short-term memory for coherent motion in video game players: evidence from a memory-masking paradigm

In this study, we investigated visual short-term memory for coherent motion in action video game players (AVGPs), non-action video game players (NAVGPs), and non-gamers (control group: CONs). Participants performed a visual memory-masking paradigm previously used with macaque monkeys and humans. In particular, we tested whether video game players form a more robust visual short-term memory trace for coherent moving stimuli during the encoding phase, and whether such memory traces are less affected by an intervening masking stimulus presented 0.2 s after the offset of the to-be-remembered sample. The results showed that task performance of all groups was affected by the masking stimulus, but video game players were affected to a lesser extent than controls. Modelling of performance values and reaction times revealed that video game players have a lower guessing rate than CONs, and higher drift rates than CONs, indicative of more efficient perceptual decisions. These results suggest that video game players exhibit a more robust VSTM trace for moving objects and this trace is less prone to external interference.

Blue is in the Eye of the Beholder: A Cross-Linguistic Study on Color Perception and Memory.

The linguistic relativity hypothesis states that the language one speaks affects how one thinks. Color categorization across languages has often been studied in order to examine the hypothesis. However, those studies often rely on uniform color stimuli or focus on one aspect of cognition. In experiment one, we examined how Russian- and English-speaking participants rated the color of blue/grey eyes perceptually and from memory. Russian-speakers are more likely to describe such eyes as grey, whereas English-speakers are more likely to describe them as blue. Participants were randomly assigned to one of three conditions. In the first condition (perception), participants saw the color scale and an eye picture simultaneously and then chose the color that best matched the picture. In the second condition (memory), participants matched the color of an eye to the color scale from memory. The third condition (label) was similar to the second, except participants labeled the eye orally before matching the color from memory. A Bayesian analysis showed that Russian-speakers rated the eyes greyer than did English-speakers in the memory and label conditions, but not perception conditions. In experiment two, we examined how short-term linguistic memory traces are related to color memory. Overall, results find nuanced support for the linguistic relativity hypothesis: language affects color memory more than color perception.

Regulators of Long-Term Memory Revealed by Mushroom Body-Specific Gene Expression Profiling in Drosophila melanogaster.

Memory formation is achieved by genetically tightly controlled molecular pathways that result in a change of synaptic strength and synapse organization. While for short-term memory traces, rapidly acting biochemical pathways are in place, the formation of long-lasting memories requires changes in the transcriptional program of a cell. Although many genes involved in learning and memory formation have been identified, little is known about the genetic mechanisms required for changing the transcriptional program during different phases of long-term memory (LTM) formation. With Drosophila melanogaster as a model system, we profiled transcriptomic changes in the mushroom body—a memory center in the fly brain—at distinct time intervals during appetitive olfactory LTM formation using the targeted DamID technique. We describe the gene expression profiles during these phases and tested 33 selected candidate genes for deficits in LTM formation using RNAi knockdown. We identified 10 genes that enhance or decrease memory when knocked-down in the mushroom body. For vajk-1 and hacd1—the two strongest hits—we gained further support for their crucial role in appetitive learning and forgetting. These findings show that profiling gene expression changes in specific cell-types harboring memory traces provides a powerful entry point to identify new genes involved in learning and memory. The presented transcriptomic data may further be used as resource to study genes acting at different memory phases.

Visual Working Memory Requires Permissive and Instructive NO/cGMP Signaling at Presynapses in the Drosophila Central Brain

The gaseous second messenger nitric oxide (NO) has been shown to regulate memory formation by activating retrograde signaling cascades from post- to presynapse that involve cyclic guanosine monophosphate (cGMP) production to induce synaptic plasticity and transcriptional changes. In this study, we analyzed the role of NO in the formation of a visual working memory that lasts only a few seconds. This memory is encoded in a subset of ring neurons that form the ellipsoid body in the Drosophila brain. Using genetic and pharmacological manipulations, we show that NO signaling is required for cGMP-mediated CREB activation, leading to the expression of competence factors like the synaptic homer protein. Interestingly, this cell-autonomous function can also be fulfilled by hydrogen sulfide (H2S) through a converging pathway, revealing for the first time that endogenously produced H2S has a role in memory processes. Notably, the NO synthase is strictly localized to the axonal output branches of the ring neurons, and this localization seems to be necessary for a second, phasic role of NO signaling. We provide evidence for a model where NO modulates the opening of cGMP-regulated cation channels to encode a short-term memory trace. Local production of NO/cGMP in restricted branches of ring neurons seems to represent the engram for objects, and comparing signal levels between individual ring neurons is used to orient the fly during search behavior. Due to its short half-life, NO seems to be a uniquely suited second messenger to encode working memories that have to be restricted in their duration.

Consolidation and restoration of memory traces in working memory.

Consolidation is the process through which ephemeral sensory traces are transformed into more stable short-term memory traces. It has been shown that consolidation plays a crucial role in working memory (WM) performance, by strengthening memory traces that then better resist interference and decay. In a recent study, Bayliss, Bogdanovs, and Jarrold (Journal of Memory and Language, 81, 34-50, 2015) argued that this process is separate from the processes known to restore WM traces after degradation, such as attentional refreshing and verbal rehearsal. In the present study, we investigated the relationship between the two types of processes in the context of WM span tasks. Participants were presented with series of letters for serial recall, each letter being followed by four digits for parity judgment. Consolidation opportunity was manipulated by varying the delay between each letter and the first digit to be processed, while opportunities for restoration were manipulated by varying the pace at which the parity task had to be performed (i.e., its cognitive load, or CL). Increasing the time available for either consolidation or restoration resulted in higher WM spans, with some substitutability between the two processes. Accordingly, when consolidation time was added to restoration time in the calculation of CL, the new resulting index, called extended CL, proved a very good predictor of recall performance, a finding also observed when verbal rehearsal was prevented by articulatory suppression. This substitutability between consolidation and restoration suggests that both processes may rely on the same mechanisms.

Short-term memory trace mediated by termination kinetics of olfactory receptor.

Odorants activate receptors in the peripheral olfactory neurons, which sends information to higher brain centers where behavioral valence is determined. Movement and airflow continuously change what odor plumes an animal encounters and little is known about the effect one plume has on the detection of another. Using the simple Drosophila melanogaster larval model to study this relationship we identify an unexpected phenomenon: response to an attractant can be selectively blocked by previous exposure to some odorants that activates the same receptor. At a mechanistic level, we find that exposure to this type of odorant causes prolonged tonic responses from a receptor (Or42b), which can block subsequent detection of a strong activator of that same receptor. We identify naturally occurring odorants with prolonged tonic responses for other odorant receptors (Ors) as well, suggesting that termination-kinetics is a factor for olfactory coding mechanisms. This mechanism has implications for odor-coding in any system and for designing applications to modify odor-driven behaviors.

Neurophysiological modulation of rapid emotional face processing is associated with impulsivity traits.

BackgroundSensori-perceptual processing of emotional stimuli under attentive conditions effectively prevents response disinhibition. This is observed saliently in low-impulsive people, because of their high sensitivity to warning signals, such as emotional faces. Results from human neurophysiological studies have been used to develop a dual detector model for early sensori-perceptual processing. A transient detector mechanism is related to automatic neurophysiological arousal in response to warning signals, which is reflected by early frontal event-related potential effects. The memory-based detector mechanism is associated with subsequent mismatch negativity (MMN), which reflects a short-term memory trace of signals. Based on previous findings, we predicted that impulsivity affects functional associations among the dual detector mechanisms, and modulates early frontal and/or MMN activities. In the present study, we recorded electroencephalograms for twenty-one healthy adults using a visual oddball paradigm with neutral faces as frequent stimuli, and angry and happy faces as infrequent stimuli. We measured the impulsivity traits by a self-report scale (the Barratt Impulsiveness Scale, 11th version).ResultsMain findings were that only happy faces increased early frontal negativity and subsequent occipital visual MMN (vMMN) for emotional change, and these neurophysiological effects positively correlated with each other in a temporally causal manner. However, an impulsivity sub-trait positively correlated selectively with vMMN for the happy faces.ConclusionThese findings demonstrate that higher impulsivity is associated with attenuated vMMN for emotional change detection in healthy populations, potentially because of weakened fronto-occipital functional connection that is responsible for the dual detector mechanism.Electronic supplementary materialThe online version of this article (doi:10.1186/s12868-015-0223-x) contains supplementary material, which is available to authorized users.

Auditory short-term memory trace formation for nonspeech and speech in SLI and dyslexia as indexed by the N100 and mismatch negativity electrophysiological responses.

This study investigates nonspeech and speech processing in specific language impairment (SLI) and dyslexia. We used a passive mismatch negativity (MMN) task to tap automatic brain responses and an active behavioural task to tap attended discrimination of nonspeech and speech sounds. Using the roving standard MMN paradigm, we varied the number of standards ('few' vs. 'many') to investigate the effect of sound repetition on N100 and MMN responses. The results revealed that the SLI group needed more repetitions than dyslexics and controls to create a strong enough sensory trace to elicit MMN. In contrast, in the behavioural task, we observed good discrimination of speech and nonspeech in all groups. The findings indicate that auditory processing deficits in SLI and dyslexia are dissociable and that memory trace formation may be implicated in SLI.

Finding and recognizing objects in natural scenes: complementary computations in the dorsal and ventral visual systems.

Searching for and recognizing objects in complex natural scenes is implemented by multiple saccades until the eyes reach within the reduced receptive field sizes of inferior temporal cortex (IT) neurons. We analyze and model how the dorsal and ventral visual streams both contribute to this. Saliency detection in the dorsal visual system including area LIP is modeled by graph-based visual saliency, and allows the eyes to fixate potential objects within several degrees. Visual information at the fixated location subtending approximately 9° corresponding to the receptive fields of IT neurons is then passed through a four layer hierarchical model of the ventral cortical visual system, VisNet. We show that VisNet can be trained using a synaptic modification rule with a short-term memory trace of recent neuronal activity to capture both the required view and translation invariances to allow in the model approximately 90% correct object recognition for 4 objects shown in any view across a range of 135° anywhere in a scene. The model was able to generalize correctly within the four trained views and the 25 trained translations. This approach analyses the principles by which complementary computations in the dorsal and ventral visual cortical streams enable objects to be located and recognized in complex natural scenes.

The role of nitric oxide in memory is modulated by diurnal time.

Nitric oxide (NO) is thought to play an important neuromodulatory role in the olfactory system. This modulation has been suggested to be particularly important for olfactory learning and memory in the antennal lobe (the primary olfactory network in invertebrates). We are using the hawkmoth, Manduca sexta, to further investigate the role of NO in olfactory memory. Recent findings suggest that NO affects short-term memory traces and that NO concentration fluctuates with the light cycle. This gives rise to the hypothesis that NO may be involved in the connection between memory and circadian rhythms. In this study, we explore the role of diurnal time and NO in memory by altering the time of day when associative-olfactory conditioning is performed. We find a strong effect of NO on short-term memory, and two surprising effects of diurnal time. We find that (1) at certain time points, NO affects longer traces of memory in addition to short-term memory; and (2) when conditioning is performed close to the light cycle switches—both from light to dark and dark to light—NO does not significantly affect memory at all. These findings suggest an intriguing functional role for NO in olfactory conditioning that is modulated as a function of diurnal time.

Deformation-specific and deformation-invariant visual object recognition: pose vs. identity recognition of people and deforming objects.

When we see a human sitting down, standing up, or walking, we can recognize one of these poses independently of the individual, or we can recognize the individual person, independently of the pose. The same issues arise for deforming objects. For example, if we see a flag deformed by the wind, either blowing out or hanging languidly, we can usually recognize the flag, independently of its deformation; or we can recognize the deformation independently of the identity of the flag. We hypothesize that these types of recognition can be implemented by the primate visual system using temporo-spatial continuity as objects transform as a learning principle. In particular, we hypothesize that pose or deformation can be learned under conditions in which large numbers of different people are successively seen in the same pose, or objects in the same deformation. We also hypothesize that person-specific representations that are independent of pose, and object-specific representations that are independent of deformation and view, could be built, when individual people or objects are observed successively transforming from one pose or deformation and view to another. These hypotheses were tested in a simulation of the ventral visual system, VisNet, that uses temporal continuity, implemented in a synaptic learning rule with a short-term memory trace of previous neuronal activity, to learn invariant representations. It was found that depending on the statistics of the visual input, either pose-specific or deformation-specific representations could be built that were invariant with respect to individual and view; or that identity-specific representations could be built that were invariant with respect to pose or deformation and view. We propose that this is how pose-specific and pose-invariant, and deformation-specific and deformation-invariant, perceptual representations are built in the brain.

Olfactory memories are intensity specific in larval Drosophila

Learning can rely on stimulus quality, stimulus intensity, or a combination of these. Regarding olfaction, the coding of odour quality is often proposed to be combinatorial along the olfactory pathway, and working hypotheses are available concerning short-term associative memory trace formation of odour quality. However, it is less clear how odour intensity is coded, and whether olfactory memory traces include information about the intensity of the learnt odour. Using odour-sugar associative conditioning in larval Drosophila, we first describe the dose-effect curves of learnability across odour intensities for four different odours (n-amyl acetate, 3-octanol, 1-octen-3-ol and benzaldehyde). We then chose odour intensities such that larvae were trained at an intermediate odour intensity, but were tested for retention with either that trained intermediate odour intensity, or with respectively higher or lower intensities. We observed a specificity of retention for the trained intensity for all four odours used. This adds to the appreciation of the richness in 'content' of olfactory short-term memory traces, even in a system as simple as larval Drosophila, and to define the demands on computational models of associative olfactory memory trace formation. We suggest two kinds of circuit architecture that have the potential to accommodate intensity learning, and discuss how they may be implemented in the insect brain.

Aging impairs intermediate-term behavioral memory by disrupting the dorsal paired medial neuron memory trace

How the functional activity of the brain is altered during aging to cause age-related memory impairments is unknown. We used functional cellular imaging to monitor two different calcium-based memory traces that underlie olfactory classical conditioning in young and aged Drosophila. Functional imaging of neural activity in the processes of the dorsal paired medial (DPM) and mushroom body neurons revealed that the capacity to form an intermediate-term memory (ITM) trace in the DPM neurons after learning is lost with age, whereas the capacity to form a short-term memory trace in the α'/β' mushroom body neurons remains unaffected by age. Stimulation of the DPM neurons by activation of a temperature-sensitive cation channel between acquisition and retrieval enhanced ITM in aged but not young flies. These data indicate that the functional state of the DPM neurons is selectively altered with age to cause an age-related impairment of ITM, and demonstrate that altering the excitability of DPM neurons can restore age-related memory impairments.