Mnemonic Encoding Research Articles

Memory-specific encoding activities of the ventral tegmental area dopamine and GABA neurons.

Although the midbrain dopamine (DA) system plays a crucial role in higher cognitive functions, including updating and maintaining short-term memory, the encoding properties of the somatic spiking activity of ventral tegmental area (VTA) DA neurons for short-term memory computations have not yet been identified. Here, we probed and analyzed the activity of optogenetically identified DA and GABA neurons while mice engaged in short-term memory-dependent behavior in a T-maze task. Single-neuron analysis revealed that significant subpopulations of DA and GABA neurons responded differently between left and right trials in the memory delay. With a series of control behavioral tasks and regression analysis tools, we show that firing rate differences are linked to short-term memory-dependent decisions and cannot be explained by reward-related processes, motivated behavior, or motor-related activities. This evidence provides novel insights into the mnemonic encoding activities of midbrain DA and GABA neurons.

Memory-specific encoding activities of the ventral tegmental area dopamine and GABA neurons

Although the midbrain dopamine (DA) system plays a crucial role in higher cognitive functions, including updating and maintaining short-term memory, the encoding properties of the somatic spiking activity of ventral tegmental area (VTA) DA neurons for short-term memory computations have not yet been identified. Here, we probed and analyzed the activity of optogenetically identified DA and GABA neurons while mice engaged in short-term memory-dependent behavior in a T-maze task. Single-neuron analysis revealed that significant subpopulations of DA and GABA neurons responded differently between left and right trials in the memory delay. With a series of control behavioral tasks and regression analysis tools, we show that firing rate differences are linked to short-term memory-dependent decisions and cannot be explained by reward-related processes, motivated behavior, or motor-related activities. This evidence provides novel insights into the mnemonic encoding activities of midbrain DA and GABA neurons.

Instructing Use of an Effective Strategy Improves Recognition Memory in Healthy Adults.

Age-related memory decrements correlate with metacognitive declines, including knowledge and deployment of effective mnemonic encoding strategies. However, whether imparting such strategy suffices for mitigating memory differences is unclear. In a longitudinal study of 276 healthy adults aged 18-79 years, we tested associative and working memory, and assessed beliefs regarding mnemonic strategies. Testing was repeated every 2 years, 5 times. Starting with the third occasion, we instructed participants to use an effective mnemonic strategy (sentence generation). Using continuous-time dynamic modeling, we assessed changes in the item and associative recognition, intervention effects, and their relations with age, sex, meta-memory beliefs, working memory, and metabolic health. Younger age, better working memory, and stronger belief in effective mnemonic strategies predicted better recognition, whereas instructional intervention attenuated associative memory deficits, with some persistence over time. The present findings show merely imparting effective strategies holds promise for mitigating age-related associative memory deficits.

Exploring the interaction between approach-avoidance conflict and memory processing

ABSTRACTThe medial temporal lobe (MTL) has been implicated in approach-avoidance (AA) conflict processing, which arises when a stimulus is imbued with both positive and negative valences. Notably, since the MTL has been traditionally viewed as a mnemonic brain region, a pertinent question is how AA conflict and memory processing interact with each other behaviourally. We conducted two behavioural experiments to examine whether increased AA conflict processing has a significant impact on incidental mnemonic encoding and inferential reasoning. In Experiment 1, participants first completed a reward and punishment AA task and were subsequently administered a surprise recognition memory test for stimuli that were presented during high and no AA conflict trials. In Experiment 2, participants completed a reward and punishment task in which they learned the valences of objects presented in pairs (AB, BC pairs). Next, we assessed their ability to integrate information across these pairs (infer A-C relationships) and examined whether inferential reasoning was more challenging across objects with conflicting compared to non-conflicting incentive values. We observed that increased motivational conflict did not significantly impact encoding or inferential reasoning. Potential explanations for these findings are considered, including the possibility that AA conflict and memory processing are not necessarily intertwined behaviourally.

How acute stress may enhance subsequent memory for threat stimuli outside the focus of attention: DLPFC-amygdala decoupling

Stress-related disorders, e.g., anxiety and depression, are characterized by decreased top-down control for distracting information, as well as a memory bias for threatening information. However, it is unclear how acute stress biases mnemonic encoding and leads to prioritized storage of threat-related information even if outside the focus of attention. In the current study, healthy adults (N = 53, all male) were randomly assigned to stress induction using the socially evaluated cold-pressor test (SECPT) or a control condition. Participants performed a task in which they were required to identify a target letter within a string of letters that were either identical to the target and thereby facilitating detection (low distractor load) or mixed with other letters to complicate the search (high load). Either a fearful or neutral face was presented on the background, outside the focus of attention. Twenty-four hours later, participants were asked to perform a surprise recognition memory test for those background faces. Stress induction resulted in increased cortisol and negative subjective mood ratings. Stress did not affect visual search performance, however, participants in the stress group showed stronger memory compared to the control group for fearful faces in the low attentional load condition. Critically, the stress induced memory bias was accompanied by decoupling between amygdala and DLFPC during encoding, which may represent a mechanism for decreased ability to filter task-irrelevant threatening background information. The current study provides a potential neural account for how stress can produce a negative memory bias for threatening information even if presented outside the focus of attention. Despite of an adaptive advantage for survival, such tendencies may ultimately also lead to generalized fear, a possibility requiring additional investigation.

Saccades are phase-locked to alpha oscillations in the occipital and medial temporal lobe during successful memory encoding.

Efficient sampling of visual information requires a coordination of eye movements and ongoing brain oscillations. Using intracranial and magnetoencephalography (MEG) recordings, we show that saccades are locked to the phase of visual alpha oscillations and that this coordination is related to successful mnemonic encoding of visual scenes. Furthermore, parahippocampal and retrosplenial cortex involvement in this coordination reflects effective vision-to-memory mapping, highlighting the importance of neural oscillations for the interaction between visual and memory domains.

Mnemonic Encoding and Cortical Organization in Parietal and Prefrontal Cortices.

Persistent activity within the frontoparietal network is consistently observed during tasks that require working memory. However, the neural circuit mechanisms underlying persistent neuronal encoding within this network remain unresolved. Here, we ask how neural circuits support persistent activity by examining population recordings from posterior parietal (PPC) and prefrontal (PFC) cortices in two male monkeys that performed spatial and motion direction-based tasks that required working memory. While spatially selective persistent activity was observed in both areas, robust selective persistent activity for motion direction was only observed in PFC. Crucially, we find that this difference between mnemonic encoding in PPC and PFC is associated with the presence of functional clustering: PPC and PFC neurons up to ∼700 μm apart preferred similar spatial locations, and PFC neurons up to ∼700 μm apart preferred similar motion directions. In contrast, motion-direction tuning similarity between nearby PPC neurons was much weaker and decayed rapidly beyond ∼200 μm. We also observed a similar association between persistent activity and functional clustering in trained recurrent neural network models embedded with a columnar topology. These results suggest that functional clustering facilitates mnemonic encoding of sensory information.SIGNIFICANCE STATEMENT Working memory refers to our ability to temporarily store and manipulate information. Numerous studies have observed that, during working memory, neurons in higher cortical areas, such as the parietal and prefrontal cortices, mnemonically encode the remembered stimulus. However, several recent studies have failed to observe mnemonic encoding during working memory, raising the question as to why mnemonic encoding is observed during some, but not all, conditions. In this study, we show that mnemonic encoding occurs when a cortical area is organized such that nearby neurons preferentially respond to the same stimulus. This result provides plausible neuronal conditions that allow for mnemonic encoding, and gives us further understanding of the brain's mechanisms that support working memory.

Spatial Mnemonic Encoding: Theta Power Decreases and Medial Temporal Lobe BOLD Increases Co-Occur during the Usage of the Method of Loci.

The method of loci is one, if not the most, efficient mnemonic encoding strategy. This spatial mnemonic combines the core cognitive processes commonly linked to medial temporal lobe (MTL) activity: spatial and associative memory processes. During such processes, fMRI studies consistently demonstrate MTL activity, while electrophysiological studies have emphasized the important role of theta oscillations (3–8 Hz) in the MTL. However, it is still unknown whether increases or decreases in theta power co-occur with increased BOLD signal in the MTL during memory encoding. To investigate this question, we recorded EEG and fMRI separately, while human participants used the spatial method of loci or the pegword method, a similarly associative but nonspatial mnemonic. The more effective spatial mnemonic induced a pronounced theta power decrease source localized to the left MTL compared with the nonspatial associative mnemonic strategy. This effect was mirrored by BOLD signal increases in the MTL. Successful encoding, irrespective of the strategy used, elicited decreases in left temporal theta power and increases in MTL BOLD activity. This pattern of results suggests a negative relationship between theta power and BOLD signal changes in the MTL during memory encoding and spatial processing. The findings extend the well known negative relation of alpha/beta oscillations and BOLD signals in the cortex to theta oscillations in the MTL.

Categorical Decision Making and Category Learning in Parietal and Prefrontal Cortices

We have a remarkable ability to recognize the behavioral significance, or category membership of incoming sensory stimuli. In the visual system, much is known about how simple visual features (such as color, orientation and direction of motion) are processed in early stages of the visual system. However, much less is known about how the brain learns and recognizes categorical information that gives meaning to incoming stimuli. This talk will discuss neurophysiological and behavioral experiments aimed at understanding the mechanisms underlying visual categorization and decision making, with a focus on the impact of category learning on underlying neuronal representations in the posterior parietal cortex (PPC) and prefrontal cortex (PFC). We recorded from PPC both before and after training on a visual categorization task. This revealed that categorization training influenced both visual and cognitive encoding in PPC, with a marked enhancement of memory-related delay-period encoding during the categorization task which was not observed during a motion discrimination task prior to categorization training. In contrast, the PFC exhibited strong delay-period encoding during both discrimination and categorization tasks. This reveals a dissociation between PFCs and PPCs roles in decision making and short term memory, with generalized engagement of PFC across a wider range of tasks, in contrast with more task-specific and training dependent mnemonic encoding in PPC. Meeting abstract presented at VSS 2016

Distinct medial temporal networks encode surprise during motivation by reward versus punishment

Adaptive motivated behavior requires predictive internal representations of the environment, and surprising events are indications for encoding new representations of the environment. The medial temporal lobe memory system, including the hippocampus and surrounding cortex, encodes surprising events and is influenced by motivational state. Because behavior reflects the goals of an individual, we investigated whether motivational valence (i.e., pursuing rewards versus avoiding punishments) also impacts neural and mnemonic encoding of surprising events. During functional magnetic resonance imaging (fMRI), participants encountered perceptually unexpected events either during the pursuit of rewards or avoidance of punishments. Despite similar levels of motivation across groups, reward and punishment facilitated the processing of surprising events in different medial temporal lobe regions. Whereas during reward motivation, perceptual surprises enhanced activation in the hippocampus, during punishment motivation surprises instead enhanced activation in parahippocampal cortex. Further, we found that reward motivation facilitated hippocampal coupling with ventromedial PFC, whereas punishment motivation facilitated parahippocampal cortical coupling with orbitofrontal cortex. Behaviorally, post-scan testing revealed that reward, but not punishment, motivation resulted in greater memory selectivity for surprising events encountered during goal pursuit. Together these findings demonstrate that neuromodulatory systems engaged by anticipation of reward and punishment target separate components of the medial temporal lobe, modulating medial temporal lobe sensitivity and connectivity. Thus, reward and punishment motivation yield distinct neural contexts for learning, with distinct consequences for how surprises are incorporated into predictive mnemonic models of the environment.

Task-specific versus generalized mnemonic representations in parietal and prefrontal cortices.

Our ability to learn a wide range of behavioral tasks is essential for responding appropriately to sensory stimuli according to behavioral demands, but the underlying neural mechanism has been rarely examined by neurophysiological recordings in the same subjects across learning. To understand how learning new behavioral tasks affects neuronal representations, we recorded from posterior parietal cortex (PPC) before and after training on a visual motion categorization task. We found that categorization training influenced cognitive encoding in PPC, with a marked enhancement of memory-related delay-period encoding during the categorization task that was absent during a motion discrimination task before categorization training. In contrast, the prefrontal cortex (PFC) exhibited strong delay-period encoding during both discrimination and categorization tasks. This reveals a dissociation between PFC's and PPC's roles in working memory, with general engagement of PFC across multiple tasks, in contrast with more task-specific mnemonic encoding in PPC.

Spatial and temporal dynamics of cortical networks engaged in memory encoding and retrieval

Memory operations such as encoding and retrieval require the coordinated interplay of cortical regions with distinct functional contributions. The mechanistic nature of these interactions, however, remains unspecified. During the performance of a face memory task during fMRI scanning, we measured the magnitude (a measure of the strength of coupling between areas) and phase (a measure of the relative timing across areas) of coherence between regions of interest and the rest of the brain. The fusiform face area (FFA) showed robust coherence with a distributed network of subregions in the prefrontal cortex (PFC), posterior parietal cortex (PPC), precuneus, and hippocampus across both memory operations. While these findings reveal significant overlap in the cortical networks underlying mnemonic encoding and retrieval, coherence phase analyses revealed context-dependent differences in cortical dynamics. During both encoding and retrieval, PFC and PPC exhibited earlier activity than in the FFA and hippocampus. Also, during retrieval, PFC activity preceded PPC activity. These findings are consistent with prior physiology studies suggesting an early contribution of PFC and PPC in mnemonic control. Together, these findings contribute to the growing literature exploring the spatio-temporal dynamics of basic memory operations.

Superior self-paced memorization of digits in spite of a normal digit span: The structure of a memorist’s skill.

Over the last century many individuals with exceptional memory have been studied and tested in the laboratory. This article studies Chao Lu, who set a Guinness World Record by memorizing 67,890 decimals of pi. Chao Lu's superior self-paced memorization of digits is shown through analyses of study times and verbal reports to be mediated by mnemonic encoding and retrieval processes. Furthermore, Chao Lu's development of his superior memory for decimals of pi is consistent with his engagement in thousands of hours of memorization. In contrast to most other studied memorists, who have digit spans over 15 digits, Chao Lu exhibited a digit span in only the normal range. Implications for different types of memorization skills and associated practice activities are discussed.

Independent delta/theta rhythms in the human hippocampus and entorhinal cortex

Theta oscillations in the medial temporal lobe (MTL) of mammals are involved in various functions such as spatial navigation, sensorimotor integration, and cognitive processing. While the theta rhythm was originally assumed to originate in the medial septum, more recent studies suggest autonomous theta generation in the MTL. Although coherence between entorhinal and hippocampal theta activity has been found to influence memory formation, it remains unclear whether these two structures can generate theta independently. In this study we analyzed intracranial electroencephalographic (EEG) recordings from 22 patients with unilateral hippocampal sclerosis undergoing presurgical evaluation prior to resection of the epileptic focus. Using a wavelet-based, frequency-band-specific measure of phase synchronization, we quantified synchrony between 10 different recording sites along the longitudinal axis of the hippocampal formation in the non-epileptic brain hemisphere. We compared EEG synchrony between adjacent recording sites (i) within the entorhinal cortex, (ii) within the hippocampus, and (iii) between the hippocampus and entorhinal cortex. We observed a significant interregional gap in synchrony for the delta and theta band, indicating the existence of independent delta/theta rhythms in different subregions of the human MTL. The interaction of these rhythms could represent the temporal basis for the information processing required for mnemonic encoding and retrieval.

A Common System for the Comprehension and Production of Narrative Speech

Humans devote much time to the exchange of memories within the context of shared general and personal semantic knowledge. Our hypothesis was that functional imaging in normal subjects would demonstrate the convergence of speech comprehension and production on high-order heteromodal and amodal cortical areas implicated in declarative memory functions. Activity independent of speech phase (that is, comprehension and production) was most evident in the left and right lateral anterior temporal cortex. Significant activity was also observed in the posterior cortex, ventral to the angular gyri. The left and right hippocampus and adjacent inferior temporal cortex were active during speech comprehension, compatible with mnemonic encoding of narrative information, but activity was significantly less during the overt memory retrieval associated with speech production. Therefore, although clinical studies suggest that hippocampal function is necessary for the retrieval as well as the encoding of memories, the former appears to depend on much less net synaptic activity. In contrast, the retrosplenial/posterior cingulate cortex and the parahippocampal area, which are closely associated anatomically with the hippocampus, were equally active during both speech comprehension and production. The results demonstrate why a severe and persistent inability both to understand and produce meaningful speech in the absence of an impairment to process linguistic forms is usually only observed after bilateral, and particularly anterior, destruction of the temporal lobes, and emphasize the importance of retrosplenial/posterior cingulate cortex, an area known to be affected early in the course of Alzheimer's disease, in the processing of memories during communication.

Neuropharmacology of Verbal Perseveration

In this article we will review available evidence concerning the effects of forebrain catecholaminergic and cholinergic activity on verbal perseveration. The anatomy and physiology of these two major neuropharmacological systems make it likely that they influence speech and language functioning directly as well as the cognitive systems that have an indirect impact on speech and language functions. Both catecholaminergic and cholinergic agents have been shown to influence executive cognitive functions (ECFs) such as "resistance to interference" and "attentional switching" as well as mnemonic encoding and retrieval processes. The ECF effects are most likely mediated by prefrontal cortex; mnemonic processes are mediated by both prefrontal and temporal lobes. Although no full-scale clinical trials on the effects of pharmacological agents on verbal perseveration have been conducted as yet, existing preclinical trials suggest that both presynaptic and postsynaptic dopaminergic agents can reduce perseverative responding by increasing inhibitory control processes. Cholinesterase inhibitors and other cholinergic agents can reduce perseverative responding by reducing verbal intrusions.

Tracking the time-course of attentional involvement in spatial working memory: an event-related potential investigation

Spatial working memory is a cognitive brain mechanism that enables the temporary maintenance and manipulation of spatial information. Recent neuroimaging and behavioral studies have led to the proposal that directed spatial attention is the mechanism by which location information is maintained in spatial working memory. Yet it is unclear whether attentional involvement is required throughout the period of active maintenance or is only invoked during discrete task-phases such as mnemonic encoding. In the current study, we aimed to track the time-course of attentional involvement during spatial working memory by recording event-related brain potentials (ERPs) from healthy volunteers. In Experiment 1, subjects performed a delayed-recognition task. Each trial began with the presentation of a brief stimulus (S1) that indicated the relevant location that subjects were to maintain in working memory. A 4.8–5.3 sec delay interval followed during which a single task-irrelevant probe was presented. The delay interval concluded with a test item (S2) to which subjects made a response indicating whether the S2-location was the same as the S1-memory location. To determine if attention was differentially engaged during discrete phases of the trial, task-irrelevant probes were presented early (400–800 msec following S1-offset) or late (2600–3000 msec following S1-offset) during the delay interval. Sensory-evoked ERPs (P1 and N1) elicited by these irrelevant probes showed attention-like modulations with greater amplitude responses for probes occurring at the S1-memory locations in comparison to probes presented at other locations. This pattern was obtained for both early- and late-delay probes. Probe-evoked activity during delayed-recognition trials was similar to activity observed when spatial attention was explicitly focused on a location in visual space (Experiment 2). These results are consistent with a model of spatial working memory in which perceptual level selective attention is utilized throughout the entire period of active maintenance to keep relevant spatial information in mind.

Distinct contributions of glutamate and dopamine receptors to temporal aspects of rodent working memory using a clinically relevant task.

Understanding the mechanistic basis of working memory, the capacity to hold representation "on line," is important for delineating the processes involved in higher cognitive functions and the pathophysiology of thought disorders. We compared the contribution of glutamate and dopamine receptor subtypes to temporal aspects of working memory using a modified rodent spatial working memory task that incorporates important elements of clinical working memory tasks. A discrete paired-trial variable-delay T-maze task was used. Initial characterization studies indicated that performance on this task is stable at seconds-long retention intervals, is sensitive to retention interval and proactive interference, and is dependent on the integrity of the medial prefrontal cortex. Consistent with clinical findings, low dose amphetamine (0.25 mg/kg) produced a delay-dependent improvement in performance, while higher doses impaired performance at all retention intervals. D1 receptor blockade produced the predicted dose- and delay-dependent impairment. D2 receptor blockade had no effect. Activation of metabotropic glutamate 2/3 (mGluR2/3) receptors, which in the prefrontal cortex inhibits the slow asynchronous phase of glutamate release, also produced a delay-dependent impairment. Low doses of an AMPA/kainate antagonist had effects similar to the mGluR2/3 agonist. In contrast, NMDA receptor antagonist-induced impairment was memory load-insensitive, resulting in chance-level performance at all retention intervals. These findings suggest that activation of NMDA receptors is necessary for the formation of mnemonic encoding while modulatory components involving slow asynchronous release of glutamate and phasic release of dopamine contribute to the active maintenance of information during the delay period.

ELABORATIVE MAPS FOR ENHANCED LEARNING OF HISTORICAL INFORMATION: UNITING SPATIAL, VERBAL, AND IMAGINAL INFORMATION

Map-like displays containing names of battles of the American Revolution and related battle information were presented to 72 middle school students with learning disabilities (LD). Students were randomly assigned to one of three map conditions that depicted information in a spatial organizational format but varied the symbols used to mark the map. Map symbols included (a) reconstructive elaborations of battle names and associated event information, (b) mnemonic keywords of battle names, and (c) realistic drawings of soldiers, buildings, and so forth. A 3 (organization) by 2 (recall) (location vs. event information) analysis of variance indicated that recall of locations was significantly greater than recall of event information in all conditions, mnemonic encoding resulted in greater recall of locations but not events, and elaborative encoding resulted in greater recall of event information relative to the mnemonic map but greater recall of locations and event information relative to the non-mnemonic map. Student reports of strategy use and implications for instruction of students with LD are discussed.

How do we perceive atonal music? Suggestions for a theoretical approach

In the discussion that follows, I will attempt to formulate some propositions for a model of the perception and mnemonic encoding of atonal music. These propositions aim to address the psychological paradox on which, at least at the outset, Schoenberg and his pupils founded their theoretical work, that of the suppression of hierarchical tonal functions at the heart of musical structure. It is a psychological paradox to the extent that today we know that there is no visual or auditory perception without there being a hierarchical organisation of the information, which at the same time allows for economical storage in memory regardless of the complexity of the information. We must then suppose that in the case of an atonal work the listener himself constructs new hierarchical rules which are substituted for tonal rules, and the coherence of the musical work depends on the listener's capacity to treat the musical information outside the conventions he has acquired by listening to tonal works. More exactly, i...