The Penn Electrophysiology of Encoding and Retrieval Study.

The Penn Electrophysiology of Encoding and Retrieval Study (PEERS) aimed to characterize the behavioral and electrophysiological (EEG) correlates of memory encoding and retrieval in highly practiced individuals. Across five PEERS experiments, 300+ subjects contributed more than 7,000 memory testing sessions with recorded EEG data. Here we tell the story of PEERS: its genesis, evolution, major findings, and the lessons it taught us about taking a big scientific approach in studying memory and the human brain. (PsycInfo Database Record (c) 2024 APA, all rights reserved).

Direct brain recordings suggest a causal subsequent-memory effect.

Endogenous variation in brain state and stimulus-specific evoked activity can both contribute to successful encoding. Previous studies, however, have not clearly distinguished among these components. We address this question by analysing intracranial EEG recorded from epilepsy patients as they studied and subsequently recalled lists of words. We first trained classifiers to predict recall of either single items or entire lists and found that both classifiers exhibited similar performance. We found that list-level classifier output-a biomarker of successful encoding-tracked item presentation and recall events, despite having no information about the trial structure. Across widespread brain regions, decreased low- and increased high-frequency activity (HFA) marked successful encoding of both items and lists. We found regional differences in the hippocampus and prefrontal cortex, where in the hippocampus HFA correlated more strongly with item recall, whereas, in the prefrontal cortex, HFA correlated more strongly with list performance. Despite subtle differences in item- and list-level features, the similarity in overall classification performance, spectral signatures of successful recall and fluctuations of spectral activity across the encoding period argue for a shared endogenous process that causally impacts the brain's ability to learn new information.

A neural code for egocentric spatial maps in the human medial temporal lobe.

Spatial navigation and memory rely on neural systems that encode places, distances, and directions in relation to the external world or relative to the navigating organism. Place, grid, and head-direction cells form key units of world-referenced, allocentric cognitive maps, but the neural basis of self-centered, egocentric representations remains poorly understood. Here, we used human single-neuron recordings during virtual spatial navigation tasks to identify neurons providing a neural code for egocentric spatial maps in the human brain. Consistent with previous observations in rodents, these neurons represented egocentric bearings toward reference points positioned throughout the environment. Egocentric bearing cells were abundant in the parahippocampal cortex and supported vectorial representations of egocentric space by also encoding distances toward reference points. Beyond navigation, the observed neurons showed activity increases during spatial and episodic memory recall, suggesting that egocentric bearing cells are not only relevant for navigation but also play a role in human memory.

Neural measures of subsequent memory reflect endogenous variability in cognitive function.

Human cognition exhibits a striking degree of variability: Sometimes we rapidly forge new associations whereas at other times new information simply does not stick. Correlations between neural activity during encoding and subsequent retrieval performance have implicated such "subsequent memory effects" (SMEs) as important for understanding the neural basis of memory formation. Uncontrolled variability in external factors that also predict memory performance, however, confounds the interpretation of these effects. By controlling for a comprehensive set of external variables, we investigated the extent to which neural correlates of successful memory encoding reflect variability in endogenous brain states. We show that external variables that reliably predict memory performance have relatively small effects on electroencephalographic (EEG) correlates of successful memory encoding. Instead, the brain activity that is diagnostic of successful encoding primarily reflects fluctuations in endogenous neural activity. These findings link neural activity during learning to endogenous states that drive variability in human cognition. (PsycInfo Database Record (c) 2021 APA, all rights reserved).

Splitting time: Sound-induced illusory visual temporal fission and fusion.

Auditory stimuli have been shown to alter visual temporal perception. For example, illusory temporal order is perceived when an auditory tone cues one side of space prior to the onset of simultaneously presented visual stimuli. Competing accounts attempt to explain such effects. The spatial gradient account of attention suggests speeded processing of visual stimuli in the cued space, whereas the impletion account suggests a Gestalt-like process where an attempt is made to arrive at a "realistic" representation of an event given ambiguous conditions. Temporal ventriloquism-where visual temporal order judgment performance is enhanced when a spatially uninformative tone is presented prior to, and after, visual stimuli onset-argues that the temporal relationship of the auditory stimuli to visual stimuli, as well as the number of auditory stimuli equaling the visual stimuli, drives the mechanisms underlying these and related effects. Results from a series of experiments highlight putative inconsistencies in both the spatial gradient account of attention and the classical temporal ventriloquism account. We present novel behavioral effects-illusory temporal order via spatially uninformative tones, and illusory simultaneity via a single tone prior to visual stimuli onset-that can be accounted for by an expanded version of the impletion account. (PsycINFO Database Record (c) 2020 APA, all rights reserved).

Neural activity reveals interactions between episodic and semantic memory systems during retrieval.

Whereas numerous findings support a distinction between episodic and semantic memory, it is now widely acknowledged that these two forms of memory interact during both encoding and retrieval. The precise nature of this interaction, however, remains poorly understood. To examine the role of semantic organization during episodic encoding and retrieval, we recorded intracranial encephalographic signals as 69 neurosurgical patients studied and subsequently recalled categorized and unrelated word lists. Applying multivariate classifiers to neural recordings, we were able to reliably predict encoding success, retrieval success, and temporal and categorical clustering during recall. By assessing how these classifiers generalized across list types, we identified specific retrieval processes that predicted recall of categorized lists and distinguished between recall transitions within and between category clusters. These results particularly implicate retrieval (rather than encoding) processes in the categorical organization of episodic memories. (PsycINFO Database Record (c) 2018 APA, all rights reserved).

Dynamics of brain activity reveal a unitary recognition signal.

Dual-process models of recognition memory typically assume that independent familiarity and recollection signals with distinct temporal profiles can each lead to recognition (enabling 2 routes to recognition), whereas single-process models posit a unitary "memory strength" signal. Using multivariate classifiers trained on spectral electroencephalogram (EEG) features, we quantified neural evidence for recognition decisions as a function of time. Classifiers trained on a small portion of the decision period performed similarly to those also incorporating information from previous time points indicating that neural activity reflects an integrated evidence signal. We propose a single-route account of recognition memory that is compatible with contributions from familiarity and recollection signals, but relies on a unitary evidence signal that integrates all available evidence. (PsycINFO Database Record (c) 2019 APA, all rights reserved).

Intact word processing in developmental prosopagnosia.

A wealth of evidence from behavioural, neuropsychological and neuroimaging research supports the view that face recognition is reliant upon a domain-specific network that does not process words. In contrast, the recent many-to-many model of visual recognition posits that brain areas involved in word and face recognition are functionally integrated. Developmental prosopagnosia (DP) is characterised by severe deficits in the recognition of faces, which the many-to-many model predicts should negatively affect word recognition. Alternatively, domain-specific accounts suggest that impairments in face and word processing need not go hand in hand. To test these possibilities, we ran a battery of 7 tasks examining word processing in a group of DP cases and controls. One of our prosopagnosia cases exhibited a severe reading impairment with delayed response times during reading aloud tasks, but not lexical decision tasks. Overall, however, we found no evidence of global word processing deficits in DP, consistent with a dissociation account for face and word processing.

Localized component filtering for electroencephalogram artifact rejection.

Blind source separation (BSS) based artifact rejection systems have been extensively studied in the electroencephalogram (EEG) literature. Although there have been advances in the development of techniques capable of dissociating neural and artifactual activity, these are still not perfect. As a result, a compromise between reduction of noise and leakage of neural activity has to be found. Here, we propose a new methodology to enhance the performance of existing BSS systems: Localized component filtering (LCF). In essence, LCF identifies the artifactual time segments within each component extracted by BSS and restricts the processing of components to these segments, therefore reducing neural leakage. We show that LCF can substantially reduce the neural leakage, increasing the true acceptance rate by 22 percentage points while worsening the false acceptance rate by less than 2 percentage points in a dataset consisting of simulated EEG data (4% improvement of the correlation between original and cleaned signals). Evaluated on real EEG data, we observed a significant increase of the signal-to-noise ratio of up to 9%.

Cathodal tDCS improves task performance in participants high in Coldheartedness.

OBJECTIVE: It is investigated whether personality-related inter-individual differences modulate tDCS effects on response inhibition. Psychopathic personality traits have been associated with a reduced ability to inhibit prepotent responses and as such it is likely that these traits may modulate the effect tDCS has on response inhibition. This study represents the first investigation into the effect of psychopathic traits on tDCS effects in the context of response inhibition, and based on previous research, the psychopathic traits Blame Externalization and Coldheartedness were elected as potential candidates for modulating tDCS effects to right dorsolateral prefrontal cortex. METHODS: Eighteen healthy participants underwent tDCS stimulation (sham, anodal, cathodal) before completing a response inhibition task, the parametric Go/No-go task. This task measures response inhibition under conditions of low and high cognitive load. TDCS stimulation was applied to F4 (international 10-20 system), corresponding to right dorsolateral prefrontal cortex, for 20min with an intensity of 1.5mA. Analysis of covariance was performed to assess how changes in response inhibition performance across difficulty level and stimulation condition were related to individual differences in psychopathy scores as measured via the Psychopathic Personality Inventory-Revised questionnaire. RESULTS: A positive relationship was found between greater scores on the Psychopathic Personality Inventory-Revised subscale of Coldheartedness and improvement in Go/No-go task performance after application of cathodal tDCS. This effect specifically related to the high load condition of the Go/No-go task. CONCLUSION: The psychopathic personality trait Coldheartedness may represent an imbalance of excitatory and inhibitory inputs to dlPFC. Improvement in functioning on inhibitory tasks after cathodal tDCS may be a result of a shift of excitatory glutamate levels to a more optimal level. SIGNIFICANCE: The current results demonstrate the utility of tDCS as a tool to assess how differences in cortical responsivity are associated with specific personality traits. Additionally, this study represents the first investigation into the influence of psychopathic traits on tDCS effects on dlPFC, and we observed beneficial changes in response inhibition as a result of, especially, cathodal stimulation in participants scoring high on Coldheartedness.

Assessing recognition memory using confidence ratings and response times.

Classification of stimuli into categories (such as 'old' and 'new' in tests of recognition memory or 'present' versus 'absent' in signal detection tasks) requires the mapping of internal signals to discrete responses. Introspective judgements about a given choice response are regularly employed in research, legal and clinical settings in an effort to measure the signal that is thought to be the basis of the classification decision. Correlations between introspective judgements and task performance suggest that such ratings often do convey information about internal states that are relevant for a given task, but well-known limitations of introspection call the fidelity of this information into question. We investigated to what extent response times can reveal information usually assessed with explicit confidence ratings. We quantitatively compared response times to confidence ratings in their ability to qualify recognition memory decisions and found convergent results suggesting that much of the information from confidence ratings can be obtained from response times.

EEG biometric identification: a thorough exploration of the time-frequency domain.

OBJECTIVE: Although interest in using electroencephalogram (EEG) activity for subject identification has grown in recent years, the state of the art still lacks a comprehensive exploration of the discriminant information within it. This work aims to fill this gap, and in particular, it focuses on the time-frequency representation of the EEG. APPROACH: We executed qualitative and quantitative analyses of six publicly available data sets following a sequential experimentation approach. This approach was divided in three blocks analysing the configuration of the power spectrum density, the representation of the data and the properties of the discriminant information. A total of ten experiments were applied. MAIN RESULTS: Results show that EEG information below 40 Hz is unique enough to discriminate across subjects (a maximum of 100 subjects were evaluated here), regardless of the recorded cognitive task or the sensor location. Moreover, the discriminative power of rhythms follows a W-like shape between 1 and 40 Hz, with the central peak located at the posterior rhythm (around 10 Hz). This information is maximized with segments of around 2 s, and it proved to be moderately constant across montages and time. SIGNIFICANCE: Therefore, we characterize how EEG activity differs across individuals and detail the optimal conditions to detect subject-specific information. This work helps to clarify the results of previous studies and to solve some unanswered questions. Ultimately, it will serve as guide for the design of future biometric systems.

Recognition memory in developmental prosopagnosia: electrophysiological evidence for abnormal routes to face recognition.

DUAL PROCESS MODELS OF RECOGNITION MEMORY PROPOSE TWO DISTINCT ROUTES FOR RECOGNIZING A FACE: recollection and familiarity. Recollection is characterized by the remembering of some contextual detail from a previous encounter with a face whereas familiarity is the feeling of finding a face familiar without any contextual details. The Remember/Know (R/K) paradigm is thought to index the relative contributions of recollection and familiarity to recognition performance. Despite researchers measuring face recognition deficits in developmental prosopagnosia (DP) through a variety of methods, none have considered the distinct contributions of recollection and familiarity to recognition performance. The present study examined recognition memory for faces in eight individuals with DP and a group of controls using an R/K paradigm while recording electroencephalogram (EEG) data at the scalp. Those with DP were found to produce fewer correct "remember" responses and more false alarms than controls. EEG results showed that posterior "remember" old/new effects were delayed and restricted to the right posterior (RP) area in those with DP in comparison to the controls. A posterior "know" old/new effect commonly associated with familiarity for faces was only present in the controls whereas individuals with DP exhibited a frontal "know" old/new effect commonly associated with words, objects and pictures. These results suggest that individuals with DP do not utilize normal face-specific routes when making face recognition judgments but instead process faces using a pathway more commonly associated with objects.

Electrophysiological evidence for functionally distinct neuronal populations in the human substantia nigra.

The human substantia nigra (SN) is thought to consist of two functionally distinct neuronal populations-dopaminergic (DA) neurons in the pars compacta subregion and GABA-ergic neurons in the pars reticulata subregion. However, a functional dissociation between these neuronal populations has not previously been demonstrated in the awake human. Here we obtained microelectrode recordings from the SN of patients undergoing deep brain stimulation (DBS) surgery for Parkinson's disease as they performed a two-alternative reinforcement learning task. Following positive feedback presentation, we found that putative DA and GABA neurons demonstrated distinct temporal dynamics. DA neurons demonstrated phasic increases in activity (250-500 ms post-feedback) whereas putative GABA neurons demonstrated more delayed and sustained increases in activity (500-1000 ms post-feedback). These results provide the first electrophysiological evidence for a functional dissociation between DA and GABA neurons in the human SN. We discuss possible functions for these neuronal responses based on previous findings in human and animal studies.

Direct recordings of grid-like neuronal activity in human spatial navigation.

Grid cells in the entorhinal cortex appear to represent spatial location via a triangular coordinate system. Such cells, which have been identified in rats, bats and monkeys, are believed to support a wide range of spatial behaviors. Recording neuronal activity from neurosurgical patients performing a virtual-navigation task, we identified cells exhibiting grid-like spiking patterns in the human brain, suggesting that humans and simpler animals rely on homologous spatial-coding schemes.

Association of salivary-assessed oxytocin and cortisol levels with time of night and sleep stage.

There have been proposals for REM to have a function of emotional memory consolidation, and also for REM sleep to be involved in the promotion of attachment behaviour. The hormones cortisol and oxytocin, respectively, may be involved in these proposed REM sleep functions. However, there are conflicting reports on whether levels of cortisol differ between sleep stages when time since sleep onset (SSO) is controlled, and virtually no literature on whether levels of oxytocin differ between sleep stages. This study thus investigated the changes in levels of oxytocin (OT) and cortisol (CT) across the night, and whether these levels differ between REM and N2 sleep when time SSO is controlled. 20 participants (10 males, 10 females, mean age = 20.45, SD = 2.01) were awakened 10 min into REM and N2 sleep periods in the sleep laboratory and gave saliva samples which were assayed for OT and CT. Levels of OT were relatively constant across the night, whereas CT increased significantly. REM and N2 did not differ significantly neither for OT nor for CT. The study has implications for models of sleep-dependent memory consolidation that incorporate the late sleep increase in cortisol as a functional component of memory consolidation, and also for the medical diagnostic assaying of OT during sleep.

Neuronal activity in the human subthalamic nucleus encodes decision conflict during action selection.

The subthalamic nucleus (STN), which receives excitatory inputs from the cortex and has direct connections with the inhibitory pathways of the basal ganglia, is well positioned to efficiently mediate action selection. Here, we use microelectrode recordings captured during deep brain stimulation surgery as participants engage in a decision task to examine the role of the human STN in action selection. We demonstrate that spiking activity in the STN increases when participants engage in a decision and that the level of spiking activity increases with the degree of decision conflict. These data implicate the STN as an important mediator of action selection during decision processes.

Recall termination in free recall.

Although much is known about the dynamics of memory search in the free recall task, relatively little is known about the factors related to recall termination. Reanalyzing individual trial data from 14 prior studies (1,079 participants in 28,015 trials) and defining termination as occurring when a final response is followed by a long nonresponse interval, we observed that termination probability increased throughout the recall period and that retrieval was more likely to terminate following an error than following a correct response. Among errors, termination probability was higher following prior-list intrusions and repetitions than following extralist intrusions. To verify that this pattern of results can be seen in a single study, we report a new experiment in which 80 participants contributed recall data from a total of 9,122 trials. This experiment replicated the pattern observed in the aggregate analysis of the prior studies.

Alphabetic letter identification: effects of perceivability, similarity, and bias.

The legibility of the letters in the Latin alphabet has been measured numerous times since the beginning of experimental psychology. To identify the theoretical mechanisms attributed to letter identification, we report a comprehensive review of literature, spanning more than a century. This review revealed that identification accuracy has frequently been attributed to a subset of three common sources: perceivability, bias, and similarity. However, simultaneous estimates of these values have rarely (if ever) been performed. We present the results of two new experiments which allow for the simultaneous estimation of these factors, and examine how the shape of a visual mask impacts each of them, as inferred through a new statistical model. Results showed that the shape and identity of the mask impacted the inferred perceivability, bias, and similarity space of a letter set, but that there were aspects of similarity that were robust to the choice of mask. The results illustrate how the psychological concepts of perceivability, bias, and similarity can be estimated simultaneously, and how each make powerful contributions to visual letter identification.

A habituation account of change detection in same/different judgments.

We investigated the basis of change detection in a short-term priming task. In two experiments, participants were asked to indicate whether or not a target word was the same as a previously presented cue. Data from an experiment measuring magnetoencephalography failed to find different patterns for "same" and "different" responses, consistent with the claim that both arise from a common neural source, with response magnitude defining the difference between immediate novelty versus familiarity. In a behavioral experiment, we tested and confirmed the predictions of a habituation account of these judgments by comparing conditions in which the target, the cue, or neither was primed by its presentation in the previous trial. As predicted, cue-primed trials had faster response times, and target-primed trials had slower response times relative to the neither-primed baseline. These results were obtained irrespective of response repetition and stimulus-response contingencies. The behavioral and brain activity data support the view that detection of change drives performance in these tasks and that the underlying mechanism is neuronal habituation.