Publications by authors named "Michael J Kahana"

151 Publications

Biomarkers of memory variability in traumatic brain injury.

Brain Commun 2021 15;3(1):fcaa202. Epub 2020 Dec 15.

Department of Psychology, University of Pennsylvania, Philadelphia, PA 19104, USA.

Traumatic brain injury is a leading cause of cognitive disability and is often associated with significant impairment in episodic memory. In traumatic brain injury survivors, as in healthy controls, there is marked variability between individuals in memory ability. Using recordings from indwelling electrodes, we characterized and compared the oscillatory biomarkers of mnemonic variability in two cohorts of epilepsy patients: a group with a history of moderate-to-severe traumatic brain injury ( = 37) and a group of controls without traumatic brain injury ( = 111) closely matched for demographics and electrode coverage. Analysis of these recordings demonstrated that increased high-frequency power and decreased theta power across a broad set of brain regions mark periods of successful memory formation in both groups. As features in a logistic-regression classifier, spectral power biomarkers effectively predicted recall probability, with little difference between traumatic brain injury patients and controls. The two groups also displayed similar patterns of theta-frequency connectivity during successful encoding periods. These biomarkers of successful memory, highly conserved between traumatic brain injury patients and controls, could serve as the basis for novel therapies that target disordered memory across diverse forms of neurological disease.
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http://dx.doi.org/10.1093/braincomms/fcaa202DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7850041PMC
December 2020

Factors correlated with intracranial interictal epileptiform discharges in refractory epilepsy.

Epilepsia 2021 Feb 17;62(2):481-491. Epub 2020 Dec 17.

Department of Neurology, Geisel School of Medicine at Dartmouth, Hanover, New Hampshire, USA.

Objective: This study was undertaken to evaluate the influence that subject-specific factors have on intracranial interictal epileptiform discharge (IED) rates in persons with refractory epilepsy.

Methods: One hundred fifty subjects with intracranial electrodes performed multiple sessions of a free recall memory task; this standardized task controlled for subject attention levels. We utilized a dominance analysis to rank the importance of subject-specific factors based on their relative influence on IED rates. Linear mixed-effects models were employed to comprehensively examine factors with highly ranked importance.

Results: Antiseizure medication (ASM) status, time of testing, and seizure onset zone (SOZ) location were the highest-ranking factors in terms of their impact on IED rates. The average IED rate of electrodes in SOZs was 34% higher than the average IED rate of electrodes outside of SOZs (non-SOZ; p < .001). However, non-SOZ electrodes had similar IED rates regardless of the subject's SOZ location (p = .99). Subjects on older generation (p < .001) and combined generation (p < .001) ASM regimens had significantly lower IED rates relative to the group taking no ASMs; newer generation ASM regimens demonstrated a nonsignificant association with IED rates (p = .13). Of the ASMs included in this study, the following ASMs were associated with significant reductions in IED rates: levetiracetam (p < .001), carbamazepine (p < .001), lacosamide (p = .03), zonisamide (p = .01), lamotrigine (p = .03), phenytoin (p = .03), and topiramate (p = .01). We observed a nonsignificant association between time of testing and IED rates (morning-afternoon p = .15, morning-evening p = .85, afternoon-evening p = .26).

Significance: The current study ranks the relative influence that subject-specific factors have on IED rates and highlights the importance of considering certain factors, such as SOZ location and ASM status, when analyzing IEDs for clinical or research purposes.
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http://dx.doi.org/10.1111/epi.16792DOI Listing
February 2021

Modeling Retest Effects in a Longitudinal Measurement Burst Study of Memory.

Comput Brain Behav 2020 Jun 14;3(2):200-207. Epub 2019 Aug 14.

Michigan State University.

Longitudinal designs must deal with the confound between increasing age and increasing task experience (i.e., retest effects). Most existing methods for disentangling these factors rely on large sample sizes and are impractical for smaller scale projects. Here, we show that a measurement burst design combined with a model of retest effects can be used to study age-related change with modest sample sizes. A combined model of age-related change and retest-related effects was developed. In a simulation experiment, we show that with sample sizes as small as = 8, the model can reliably detect age effects of the size reported in the longitudinal literature while avoiding false positives when there is no age effect. We applied the model to data from a measurement burst study in which eight subjects completed a burst of seven sessions of free recall every year for five years. Six additional subjects completed a burst only in years 1 and 5. They should, therefore, have smaller retest effects but equal age effects. The raw data suggested slight improvement in memory over five years. However, applying the model to the yearly-testing group revealed that a substantial positive retest effect was obscuring stability in memory performance. Supporting this finding, the control group showed a smaller retest effect but an equal age effect. Measurement burst designs combined with models of retest effects allow researchers to employ longitudinal designs in areas where previously only cross-sectional designs were feasible.
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http://dx.doi.org/10.1007/s42113-019-00047-wDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7717555PMC
June 2020

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

J Exp Psychol Learn Mem Cogn 2020 Nov 5. Epub 2020 Nov 5.

Department of Psychology.

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) 2020 APA, all rights reserved).
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http://dx.doi.org/10.1037/xlm0000966DOI Listing
November 2020

Predicting recall of words and lists.

J Exp Psychol Learn Mem Cogn 2020 Oct 22. Epub 2020 Oct 22.

University of Pennsylvania.

For more than a half-century, lists of words have served as the memoranda of choice in studies of human memory. To better understand why some words and lists are easier to recall than others, we estimated multivariate models of word and list recall. In each of the 23 sessions, subjects ( = 98) studied and recalled the same set of 576 words, presented in 24 study-test lists. Fitting a statistical model to these data revealed positive effects of animacy, contextual diversity, valence, arousal, concreteness, and semantic structure on recall of individual words. We next asked whether a similar approach would allow us to account for list-level variability in recall performance. Here we hypothesized that semantically coherent lists would be most memorable. Consistent with this prediction, we found that semantic similarity, weighted by temporal distance, was a strong positive predictor of list-level recall. Additionally, we found significant effects of average contextual diversity, valence, animacy, and concreteness on list-level recall. Our findings extend previous models of item-level recall and show that aggregate measures of item recallability also account for variability in list-level performance. (PsycInfo Database Record (c) 2020 APA, all rights reserved).
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http://dx.doi.org/10.1037/xlm0000964DOI Listing
October 2020

The effects of direct brain stimulation in humans depend on frequency, amplitude, and white-matter proximity.

Brain Stimul 2020 Sep - Oct;13(5):1183-1195. Epub 2020 May 21.

Department of Biomedical Engineering, Columbia University, New York, 10027, USA. Electronic address:

Background: Researchers have used direct electrical brain stimulation to treat a range of neurological and psychiatric disorders. However, for brain stimulation to be maximally effective, clinicians and researchers should optimize stimulation parameters according to desired outcomes.

Objective: The goal of our large-scale study was to comprehensively evaluate the effects of stimulation at different parameters and locations on neuronal activity across the human brain.

Methods: To examine how different kinds of stimulation affect human brain activity, we compared the changes in neuronal activity that resulted from stimulation at a range of frequencies, amplitudes, and locations with direct human brain recordings. We recorded human brain activity directly with electrodes that were implanted in widespread regions across 106 neurosurgical epilepsy patients while systematically stimulating across a range of parameters and locations.

Results: Overall, stimulation most often had an inhibitory effect on neuronal activity, consistent with earlier work. When stimulation excited neuronal activity, it most often occurred from high-frequency stimulation. These effects were modulated by the location of the stimulating electrode, with stimulation sites near white matter more likely to cause excitation and sites near gray matter more likely to inhibit neuronal activity.

Conclusion: By characterizing how different stimulation parameters produced specific neuronal activity patterns on a large scale, our results provide an electrophysiological framework that clinicians and researchers may consider when designing stimulation protocols to cause precisely targeted changes in human brain activity.
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http://dx.doi.org/10.1016/j.brs.2020.05.009DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7494653PMC
May 2020

Neural fatigue influences memory encoding in the human hippocampus.

Neuropsychologia 2020 06 22;143:107471. Epub 2020 Apr 22.

Department of Psychology, University of Pennsylvania, 425 South University Avenue, Philadelphia, PA, 19104, USA.

Here we examine the variability underlying successful memory encoding. Successful encoding of successive study items may fatigue encoding resources, thus decreasing the ability to encode subsequent items (Tulving and Rosenbaum, 2006); alternatively, successful encoding may be persistent, leading to more successful encoding (Kahana, Aggarwal, and Phan, 2018). Analyzing intracranial electroencephalographic activity while subjects studied lists of words for subsequent free recall, we examined high-frequency activity (HFA) in hippocampus and dorsolateral prefrontal cortex (DLPFC), as HFA was greater for subsequently recalled than non-recalled items in these regions. We compared non-recalled items with good encoding history (i.e. one of the two preceding items was recalled) with non-recalled items with poor encoding history (i.e. neither prior item was recalled). In the hippocampus, good encoding history led to reduced HFA, whereas in the DLPFC, good encoding history led to enhanced HFA. Hippocampal findings appear consistent with the neural fatigue hypothesis, whereas the DLPFC results appear consistent with persistent encoding states.
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http://dx.doi.org/10.1016/j.neuropsychologia.2020.107471DOI Listing
June 2020

Theta Oscillations in Human Memory.

Trends Cogn Sci 2020 03 3;24(3):208-227. Epub 2020 Feb 3.

Department of Psychology, University of Pennsylvania, Philadelphia, PA, USA. Electronic address:

Theta frequency (4-8 Hz) fluctuations of the local field potential have long been implicated in learning and memory. Human studies of episodic memory, however, have provided mixed evidence for theta's role in successful learning and remembering. Re-evaluating these conflicting findings leads us to conclude that: (i) successful memory is associated both with increased narrow-band theta oscillations and a broad-band tilt of the power spectrum; (ii) theta oscillations specifically support associative memory, whereas the spectral tilt reflects a general index of activation; and (iii) different cognitive contrasts (generalized versus specific to memory), recording techniques (invasive versus noninvasive), and referencing schemes (local versus global) alter the balance between the two phenomena to make one or the other more easily detectable.
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http://dx.doi.org/10.1016/j.tics.2019.12.006DOI Listing
March 2020

Reactivated Spatial Context Guides Episodic Recall.

J Neurosci 2020 03 23;40(10):2119-2128. Epub 2020 Jan 23.

Computational Memory Laboratory, Department of Psychology, University of Pennsylvania, Philadelphia, Pennsylvania 19104,

The medial temporal lobe (MTL) is known as the locus of spatial coding and episodic memory, but the interaction between these cognitive domains as well as the extent to which they rely on common neurophysiological mechanisms is poorly understood. Here, we use intracranial electroencephalography and a hybrid spatial-episodic memory task (29 subjects, 15 female) to determine how spatial information is dynamically reactivated in subregions of the human MTL and how this reactivation guides recall of episodic information. Our results implicate theta oscillations across the MTL as a common neurophysiological substrate for spatial coding in navigation and episodic recall. We further show that our index of retrieved spatial context is high in the hippocampus (HC) in an early time window preceding recall. Closer to recall, it decreases in the HC and increases in the parahippocampal gyrus. Finally, we demonstrate that hippocampal theta phase modulates parahippocampal gamma amplitude during retrieval of spatial context, suggesting a role for cross-frequency coupling in coding and transmitting retrieved spatial information. By recording from the human medial temporal lobe (MTL) while subjects recall items experienced in a virtual environment, we establish a direct relation between the strength of theta activity during memory search and the extent to which memories are organized by their spatial locations. We thereby pinpoint a role for theta oscillations in accessing the "cognitive map" during episodic retrieval and further highlight the dynamic interplay of hippocampus and extrahippocampal MTL in representing retrieved spatial context. Our results provide an important step toward a unified theory of MTL function encompassing its role in spatial navigation and episodic memory.
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http://dx.doi.org/10.1523/JNEUROSCI.1640-19.2019DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7055128PMC
March 2020

Age-related differences in the temporal dynamics of spectral power during memory encoding.

PLoS One 2020 16;15(1):e0227274. Epub 2020 Jan 16.

Department of Psychology, University of Pennsylvania, Philadelphia, PA, United States of America.

We examined oscillatory power in electroencephalographic recordings obtained while younger (18-30 years) and older (60+ years) adults studied lists of words for later recall. Power changed in a highly consistent way from word-to-word across the study period. Above 14 Hz, there were virtually no age differences in these neural gradients. But gradients below 14 Hz reliably discriminated between age groups. Older adults with the best memory performance showed the largest departures from the younger adult pattern of neural activity. These results suggest that age differences in the dynamics of neural activity across an encoding period reflect changes in cognitive processing that may compensate for age-related decline.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0227274PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6964832PMC
May 2020

Hippocampal theta codes for distances in semantic and temporal spaces.

Proc Natl Acad Sci U S A 2019 11 13;116(48):24343-24352. Epub 2019 Nov 13.

Department of Psychology, University of Pennsylvania, Philadelphia, PA 19104

The medial temporal lobe (MTL) is known to support episodic memory and spatial navigation, raising the possibility that its true function is to form "cognitive maps" of any kind of information. Studies in humans and animals support the idea that the hippocampal theta rhythm (4 to 8 Hz) is key to this mapping function, as it has been repeatedly observed during spatial navigation tasks. If episodic memory and spatial navigation are 2 sides of the same coin, we hypothesized that theta oscillations might reflect relations between explicitly nonspatial items, such as words. We asked 189 neurosurgical patients to perform a verbal free-recall task, of which 96 had indwelling electrodes placed in the MTL. Subjects were instructed to remember short lists of sequentially presented nouns. We found that hippocampal theta power and connectivity during item retrieval coded for semantic distances between words, as measured using word2vec-derived subspaces. Additionally, hippocampal theta indexed temporal distances between words after filtering lists on recall performance, to ensure adequate dynamic range in time. Theta effects were noted only for semantic subspaces of 1 dimension, indicating a substantial compression of the possible semantic feature space. These results lend further support to our growing confidence that the MTL forms cognitive maps of arbitrary representational spaces, helping to reconcile longstanding differences between the spatial and episodic memory literatures.
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http://dx.doi.org/10.1073/pnas.1906729116DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6883851PMC
November 2019

Computational Models of Memory Search.

Authors:
Michael J Kahana

Annu Rev Psychol 2020 01 30;71:107-138. Epub 2019 Sep 30.

Department of Psychology, University of Pennsylvania, Philadelphia, Pennsylvania 19104, USA; email:

The capacity to search memory for events learned in a particular context stands as one of the most remarkable feats of the human brain. How is memory search accomplished? First, I review the central ideas investigated by theorists developing models of memory. Then, I review select benchmark findings concerning memory search and analyze two influential computational approaches to modeling memory search: dual-store theory and retrieved context theory. Finally, I discuss the key theoretical ideas that have emerged from these modeling studies and the open questions that need to be answered by future research.
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http://dx.doi.org/10.1146/annurev-psych-010418-103358DOI Listing
January 2020

Does data cleaning improve brain state classification?

J Neurosci Methods 2019 12 18;328:108421. Epub 2019 Sep 18.

Dept. of Psychology, University of Pennsylvania, Philadelphia, PA 19104, USA. Electronic address:

Background: Neuroscientists routinely seek to identify and remove noisy or artifactual observations from their data. They do so with the belief that removing such data improves power to detect relations between neural activity and behavior, which are often subtle and can be overwhelmed by noise. Whereas standard methods can exclude certain well-defined noise sources (e.g., 50/60 Hz electrical noise), in many situations there is not a clear difference between noise and signals so it is not obvious how to separate the two. Here we ask whether methods routinely used to "clean" human electrophysiological recordings lead to greater power to detect brain-behavior relations.

New Method: This, to the authors' knowledge, is the first large-scale simultaneous evaluation of multiple commonly used methods for removing noise from intracranial EEG recordings.

Results: We find that several commonly used data cleaning methods (automated methods based on statistical signal properties and manual methods based on expert review) do not increase the power to detect univariate and multivariate electrophysiological biomarkers of successful episodic memory encoding, a well-characterized broadband pattern of neural activity observed across the brain.

Comparison With Existing Methods: Researchers may be more likely to increase statistical power to detect physiological phenomena of interest by allocating resources away from cleaning noisy data and toward collecting more within-patient observations.

Conclusions: These findings highlight the challenge of partitioning signal and noise in the analysis of brain-behavior relations, and suggest increasing sample size and numbers of observations, rather than data cleaning, as the best approach to improving statistical power.
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http://dx.doi.org/10.1016/j.jneumeth.2019.108421DOI Listing
December 2019

Risk of seizures induced by intracranial research stimulation: analysis of 770 stimulation sessions.

J Neural Eng 2019 11 11;16(6):066039. Epub 2019 Nov 11.

Department of Neurological Surgery, Columbia University, New York, NY, United States of America.

Objective: Patients with medically refractory epilepsy often undergo intracranial electroencephalography (iEEG) monitoring to identify a seizure focus and determine their candidacy for surgical intervention. This clinically necessary monitoring period provides an increasingly utilized research opportunity to study human neurophysiology, however ethical concerns demand a thorough appreciation of the associated risks. We measured the incidence of research stimulation-associated seizures in a large multi-institutional dataset in order to determine whether brain stimulation was statistically associated with seizure incidence and identify potential risk factors for stimulation-associated seizures.

Approach: 188 subjects undergoing iEEG monitoring across ten institutions participated in 770 research stimulation sessions over 3.5 yr. Seizures within 30 min of a stimulation session were included in our retrospective analysis. We analyzed stimulation parameters, seizure incidence, and typical seizure patterns, to assess the likelihood that recorded seizures were stimulation-induced, rather than events that occurred by chance in epilepsy patients prone to seizing.

Main Results: In total, 14 seizures were included in our analysis. All events were single seizures, and no adverse events occurred. The mean amplitude of seizure-associated stimulation did not differ significantly from the mean amplitude delivered in sessions without seizures. In order to determine the likelihood that seizures were stimulation induced, we used three sets of analyses: visual iEEG analysis, statistical frequency, and power analyses. We determined that three of the 14 seizures were likely stimulation-induced, five were possibly stimulation-induced, and six were unlikely stimulation-induced. Overall, we estimate a rate of stimulation-induced seizures between 0.39% and 1.82% of sessions.

Significance: The rarity of stimulation-associated seizures and the fact that none added morbidity or affected the clinical course of any patient are important findings for understanding the feasibility and safety of intracranial stimulation for research purposes.
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http://dx.doi.org/10.1088/1741-2552/ab4365DOI Listing
November 2019

Functional control of electrophysiological network architecture using direct neurostimulation in humans.

Netw Neurosci 2019 1;3(3):848-877. Epub 2019 Jul 1.

Department of Bioengineering, University of Pennsylvania, Philadelphia, PA, USA.

Chronically implantable neurostimulation devices are becoming a clinically viable option for treating patients with neurological disease and psychiatric disorders. Neurostimulation offers the ability to probe and manipulate distributed networks of interacting brain areas in dysfunctional circuits. Here, we use tools from network control theory to examine the dynamic reconfiguration of functionally interacting neuronal ensembles during targeted neurostimulation of cortical and subcortical brain structures. By integrating multimodal intracranial recordings and diffusion-weighted imaging from patients with drug-resistant epilepsy, we test hypothesized structural and functional rules that predict altered patterns of synchronized local field potentials. We demonstrate the ability to predictably reconfigure functional interactions depending on stimulation strength and location. Stimulation of areas with structurally weak connections largely modulates the functional hubness of downstream areas and concurrently propels the brain towards more difficult-to-reach dynamical states. By using focal perturbations to bridge large-scale structure, function, and markers of behavior, our findings suggest that stimulation may be tuned to influence different scales of network interactions driving cognition.
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http://dx.doi.org/10.1162/netn_a_00089DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6663306PMC
July 2019

Multivariate stochastic volatility modeling of neural data.

Elife 2019 08 1;8. Epub 2019 Aug 1.

University of Pennsylvania, Philadelphia, United States.

Because multivariate autoregressive models have failed to adequately account for the complexity of neural signals, researchers have predominantly relied on non-parametric methods when studying the relations between brain and behavior. Using medial temporal lobe (MTL) recordings from 96 neurosurgical patients, we show that time series models with volatility described by a multivariate stochastic latent-variable process and lagged interactions between signals in different brain regions provide new insights into the dynamics of brain function. The implied volatility inferred from our process positively correlates with high-frequency spectral activity, a signal that correlates with neuronal activity. We show that volatility features derived from our model can reliably decode memory states, and that this classifier performs as well as those using spectral features. Using the directional connections between brain regions during complex cognitive process provided by the model, we uncovered perirhinal-hippocampal desynchronization in the MTL regions that is associated with successful memory encoding.
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http://dx.doi.org/10.7554/eLife.42950DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6697415PMC
August 2019

Dynamic Theta Networks in the Human Medial Temporal Lobe Support Episodic Memory.

Curr Biol 2019 04 21;29(7):1100-1111.e4. Epub 2019 Mar 21.

Department of Psychology, University of Pennsylvania, Philadelphia, PA 19104, USA. Electronic address:

The medial temporal lobe (MTL) is a locus of episodic memory in the human brain. It is comprised of cytologically distinct subregions that, in concert, give rise to successful encoding and retrieval of context-dependent memories. However, the functional connections between these subregions are poorly understood. To determine functional connectivity among MTL subregions, we had 131 subjects fitted with indwelling electrodes perform a verbal memory task and asked how encoding or retrieval correlated with inter-regional synchronization. Using phase-based measures of connectivity, we found that synchronous theta (4-8 Hz) activity underlies successful episodic memory. During encoding, we observed a dynamic pattern of connections converging on the left entorhinal cortex, beginning with the perirhinal cortex and shifting through hippocampal subfields. Retrieval-associated networks demonstrated enhanced involvement of the subiculum and CA1, reflecting a substantial reorganization of the encoding network. We posit that coherent theta activity within the MTL marks periods of successful memory, but distinct patterns of connectivity dissociate key stages of memory processing.
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http://dx.doi.org/10.1016/j.cub.2019.02.020DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6445741PMC
April 2019

Human Verbal Memory Encoding Is Hierarchically Distributed in a Continuous Processing Stream.

eNeuro 2019 Jan-Feb;6(1). Epub 2019 Mar 4.

Department of Neurology, Mayo Clinic, Rochester, MN 55905.

Processing of memory is supported by coordinated activity in a network of sensory, association, and motor brain regions. It remains a major challenge to determine where memory is encoded for later retrieval. Here, we used direct intracranial brain recordings from epilepsy patients performing free recall tasks to determine the temporal pattern and anatomical distribution of verbal memory encoding across the entire human cortex. High γ frequency activity (65-115 Hz) showed consistent power responses during encoding of subsequently recalled and forgotten words on a subset of electrodes localized in 16 distinct cortical areas activated in the tasks. More of the high γ power during word encoding, and less power before and after the word presentation, was characteristic of successful recall and observed across multiple brain regions. Latencies of the induced power changes and this subsequent memory effect (SME) between the recalled and forgotten words followed an anatomical sequence from visual to prefrontal cortical areas. Finally, the magnitude of the memory effect was unexpectedly found to be the largest in selected brain regions both at the top and at the bottom of the processing stream. These included the language processing areas of the prefrontal cortex and the early visual areas at the junction of the occipital and temporal lobes. Our results provide evidence for distributed encoding of verbal memory organized along a hierarchical posterior-to-anterior processing stream.
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http://dx.doi.org/10.1523/ENEURO.0214-18.2018DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6402539PMC
May 2019

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

J Exp Psychol Gen 2019 Jan;148(1):1-12

Department of Psychology, University of Pennsylvania.

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).
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http://dx.doi.org/10.1037/xge0000480DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6419095PMC
January 2019

Contiguity in episodic memory.

Psychon Bull Rev 2019 Jun;26(3):699-720

University of Pennsylvania, Philadelphia, PA, USA.

Contiguity is one of the major predictors of recall dynamics in human episodic memory. But there are many competing theories of how the memory system gives rise to contiguity. Here we provide a set of benchmark findings for which any such theory should account. These benchmarks are drawn from a review of the existing literature as well as analyses of both new and archival data. They include 34 distinct findings on how various factors including individual and group differences, task parameters, and type of stimuli influence the magnitude of the contiguity effect. We will see that contiguity is observed in a range of tasks including recognition, paired associates, and autobiographical recall and across a range of time scales including minutes, days, weeks, and years. The broad pattern of data point toward a theory in which contiguity arises from fundamental memory mechanisms that encode and search an approximately time scale invariant representation of temporal distance.
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http://dx.doi.org/10.3758/s13423-018-1537-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6529295PMC
June 2019

Neuronal phase consistency tracks dynamic changes in acoustic spectral regularity.

Eur J Neurosci 2019 05 29;49(10):1268-1287. Epub 2018 Nov 29.

Neuroscience Graduate Group, University of Pennsylvania, Philadelphia, Pennsylvania.

The brain parses the auditory environment into distinct sounds by identifying those acoustic features in the environment that have common relationships (e.g., spectral regularities) with one another and then grouping together the neuronal representations of these features. Although there is a large literature that tests how the brain tracks spectral regularities that are predictable, it is not known how the auditory system tracks spectral regularities that are not predictable and that change dynamically over time. Furthermore, the contribution of brain regions downstream of the auditory cortex to the coding of spectral regularity is unknown. Here, we addressed these two issues by recording electrocorticographic activity, while human patients listened to tone-burst sequences with dynamically varying spectral regularities, and identified potential neuronal mechanisms of the analysis of spectral regularities throughout the brain. We found that the degree of oscillatory stimulus phase consistency (PC) in multiple neuronal-frequency bands tracked spectral regularity. In particular, PC in the delta-frequency band seemed to be the best indicator of spectral regularity. We also found that these regularity representations existed in multiple regions throughout cortex. This widespread reliable modulation in PC - both in neuronal-frequency space and in cortical space - suggests that phase-based modulations may be a general mechanism for tracking regularity in the auditory system specifically and other sensory systems more generally. Our findings also support a general role for the delta-frequency band in processing the regularity of auditory stimuli.
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http://dx.doi.org/10.1111/ejn.14263DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6520206PMC
May 2019

Hippocampal contributions to serial-order memory.

Hippocampus 2019 03 5;29(3):252-259. Epub 2018 Nov 5.

Department of Psychology, University of Pennsylvania, Philadelphia, PA.

Our memories form a record not only of our experiences, but also of their temporal structure. Although memory for the temporal structure of experience likely relies on multiple neural systems, numerous studies have implicated the hippocampus in the encoding and retrieval of temporal information. This review evaluates the literature on hippocampal contributions to human serial-order memory from the perspective of three cognitive theories: associative chaining theory, positional-coding theory and retrieved-context theory. Evaluating neural findings through the lens of cognitive theories enables us to draw more incisive conclusions about the relations between brain and behavior.
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http://dx.doi.org/10.1002/hipo.23025DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6608709PMC
March 2019

Spatial Representations in the Human Brain.

Front Hum Neurosci 2018 30;12:297. Epub 2018 Jul 30.

Computational Memory Lab, Department of Psychology, University of Pennsylvania, Philadelphia, PA, United States.

While extensive research on the neurophysiology of spatial memory has been carried out in rodents, memory research in humans had traditionally focused on more abstract, language-based tasks. Recent studies have begun to address this gap using virtual navigation tasks in combination with electrophysiological recordings in humans. These studies suggest that the human medial temporal lobe (MTL) is equipped with a population of place and grid cells similar to that previously observed in the rodent brain. Furthermore, theta oscillations have been linked to spatial navigation and, more specifically, to the encoding and retrieval of spatial information. While some studies suggest a single navigational theta rhythm which is of lower frequency in humans than rodents, other studies advocate for the existence of two functionally distinct delta-theta frequency bands involved in both spatial and episodic memory. Despite the general consensus between rodent and human electrophysiology, behavioral work in humans does not unequivocally support the use of a metric Euclidean map for navigation. Formal models of navigational behavior, which specifically consider the spatial scale of the environment and complementary learning mechanisms, may help to better understand different navigational strategies and their neurophysiological mechanisms. Finally, the functional overlap of spatial and declarative memory in the MTL calls for a unified theory of MTL function. Such a theory will critically rely upon linking task-related phenomena at multiple temporal and spatial scales. Understanding how single cell responses relate to ongoing theta oscillations during both the encoding and retrieval of spatial and non-spatial associations appears to be key toward developing a more mechanistic understanding of memory processes in the MTL.
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http://dx.doi.org/10.3389/fnhum.2018.00297DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6078001PMC
July 2018

Dynamics of brain activity reveal a unitary recognition signal.

J Exp Psychol Learn Mem Cogn 2019 Mar 19;45(3):440-451. Epub 2018 Jul 19.

Department of Psychology.

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).
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http://dx.doi.org/10.1037/xlm0000593DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6339602PMC
March 2019

The variability puzzle in human memory.

J Exp Psychol Learn Mem Cogn 2018 Dec 26;44(12):1857-1863. Epub 2018 Apr 26.

Department of Psychology.

Memory performance exhibits a high level of variability from moment to moment. Much of this variability may reflect inadequately controlled experimental variables, such as word memorability, past practice and subject fatigue. Alternatively, stochastic variability in performance may largely reflect the efficiency of endogenous neural processes that govern memory function. To help adjudicate between these competing views, the authors conducted a multisession study in which subjects completed 552 trials of a delayed free-recall task. Applying a statistical model to predict variability in each subject's recall performance uncovered modest effects of word memorability, proactive interference, and other variables. In contrast to the limited explanatory power of these experimental variables, performance on the prior list strongly predicted current list recall. These findings suggest that endogenous factors underlying successful encoding and retrieval drive variability in performance. (PsycINFO Database Record (c) 2018 APA, all rights reserved).
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http://dx.doi.org/10.1037/xlm0000553DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6203681PMC
December 2018

A spacing account of negative recency in final free recall.

J Exp Psychol Learn Mem Cogn 2018 Aug 12;44(8):1180-1185. Epub 2018 Apr 12.

Department of Psychology, University of Pennsylvania.

The well-known recency effect in immediate free recall reverses when subjects attempt to recall items studied and tested on a series of prior lists, as in the final-free-recall procedure (Craik, 1970). In this case, the last few items on each list are actually remembered less well than are the midlist items. Because dual-store theories of recall naturally predict negative recency, this phenomenon has long been cited as evidence favoring these models. In a final-free-recall study, we replicate the negative-recency effect for the within-list serial position curve and the positive-recency effect for the between-list serial position curve. Whereas we find prominent negative recency for items recalled early in the initial recall period, this effect is markedly reduced for items recalled later in the recall period. When considering initial recall as a second presentation of studied items, we find that the probability of final free recall increases as the number of items between initial presentation and initial recall increases. These results suggest that negative recency may reflect the beneficial effects of spaced practice, in which end-of-list items recalled early constitute massed repetitions and end-of-list items recalled late are spaced repetitions. To help distinguish between the spacing account and the prevailing dual-store, rehearsal-based account, we examined negative recency in continual-distractor free recall. Contrary to the dual-store account, but in accord with the spacing account, we find robust negative recency in continual-distractor free recall, which is greater for those items recalled early in output. (PsycINFO Database Record
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http://dx.doi.org/10.1037/xlm0000491DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6066445PMC
August 2018

Closed-loop stimulation of temporal cortex rescues functional networks and improves memory.

Nat Commun 2018 02 6;9(1):365. Epub 2018 Feb 6.

Department of Psychology, University of Pennsylvania, 433 South University Avenue, Philadelphia, PA, 19104, USA.

Memory failures are frustrating and often the result of ineffective encoding. One approach to improving memory outcomes is through direct modulation of brain activity with electrical stimulation. Previous efforts, however, have reported inconsistent effects when using open-loop stimulation and often target the hippocampus and medial temporal lobes. Here we use a closed-loop system to monitor and decode neural activity from direct brain recordings in humans. We apply targeted stimulation to lateral temporal cortex and report that this stimulation rescues periods of poor memory encoding. This system also improves later recall, revealing that the lateral temporal cortex is a reliable target for memory enhancement. Taken together, our results suggest that such systems may provide a therapeutic approach for treating memory dysfunction.
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http://dx.doi.org/10.1038/s41467-017-02753-0DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5802791PMC
February 2018

Electrical Stimulation Modulates High γ Activity and Human Memory Performance.

eNeuro 2018 Jan-Feb;5(1). Epub 2018 Feb 2.

Department of Neurology, Mayo Clinic, Rochester, MN 55905.

Direct electrical stimulation of the brain has emerged as a powerful treatment for multiple neurological diseases, and as a potential technique to enhance human cognition. Despite its application in a range of brain disorders, it remains unclear how stimulation of discrete brain areas affects memory performance and the underlying electrophysiological activities. Here, we investigated the effect of direct electrical stimulation in four brain regions known to support declarative memory: hippocampus (HP), parahippocampal region (PH) neocortex, prefrontal cortex (PF), and lateral temporal cortex (TC). Intracranial EEG recordings with stimulation were collected from 22 patients during performance of verbal memory tasks. We found that high γ (62-118 Hz) activity induced by word presentation was modulated by electrical stimulation. This modulatory effect was greatest for trials with "poor" memory encoding. The high γ modulation correlated with the behavioral effect of stimulation in a given brain region: it was negative, i.e., the induced high γ activity was decreased, in the regions where stimulation decreased memory performance, and positive in the lateral TC where memory enhancement was observed. Our results suggest that the effect of electrical stimulation on high γ activity induced by word presentation may be a useful biomarker for mapping memory networks and guiding therapeutic brain stimulation.
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http://dx.doi.org/10.1523/ENEURO.0369-17.2018DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5797477PMC
January 2019

Evidence for verbal memory enhancement with electrical brain stimulation in the lateral temporal cortex.

Brain 2018 04;141(4):971-978

Mayo Clinic, Department of Neurology, Rochester MN, USA.

Direct electrical stimulation of the human brain can elicit sensory and motor perceptions as well as recall of memories. Stimulating higher order association areas of the lateral temporal cortex in particular was reported to activate visual and auditory memory representations of past experiences (Penfield and Perot, 1963). We hypothesized that this effect could be used to modulate memory processing. Recent attempts at memory enhancement in the human brain have been focused on the hippocampus and other mesial temporal lobe structures, with a few reports of memory improvement in small studies of individual brain regions. Here, we investigated the effect of stimulation in four brain regions known to support declarative memory: hippocampus, parahippocampal neocortex, prefrontal cortex and temporal cortex. Intracranial electrode recordings with stimulation were used to assess verbal memory performance in a group of 22 patients (nine males). We show enhanced performance with electrical stimulation in the lateral temporal cortex (paired t-test, P = 0.0067), but not in the other brain regions tested. This selective enhancement was observed both on the group level, and for two of the four individual subjects stimulated in the temporal cortex. This study shows that electrical stimulation in specific brain areas can enhance verbal memory performance in humans.awx373media15704855796001.
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http://dx.doi.org/10.1093/brain/awx373DOI Listing
April 2018

Theta band power increases in the posterior hippocampus predict successful episodic memory encoding in humans.

Hippocampus 2017 10 30;27(10):1040-1053. Epub 2017 Jun 30.

Department of Neurological Surgery, University of Texas, Southwestern Medical Center, Dallas, Texas, 75390.

Functional differences in the anterior and posterior hippocampus during episodic memory processing have not been examined in human electrophysiological data. This is in spite of strong evidence for such differences in rodent data, including greater place cell specificity in the dorsal hippocampus, greater sensitivity to the aversive or motivational content of memories in ventral regions, connectivity analyses identifying preferential ventral hippocampal connections with the amygdala, and gene expression analyses identifying a dorsal-ventral gradient. We asked if memory-related oscillatory patterns observed in human hippocampal recordings, including the gamma band and slow-theta (2.5-5 Hz) subsequent memory effects, would exhibit differences along the longitudinal axis and between hemispheres. We took advantage of a new dataset of stereo electroencephalography patients with simultaneous, robotically targeted anterior, and posterior hippocampal electrodes to directly compare oscillatory subsequent memory effects during item encoding. This same data set allowed us to examine left-right connectivity and hemispheric differences in hippocampal oscillatory patterns. Our data suggest that a power increase during successful item encoding in the 2.5-5 Hz slow-theta frequency range preferentially occurs in the posterior hippocampus during the first 1,000 ms after item presentation, while a gamma band power increase is stronger in the dominant hemisphere. This dominant-nondominant pattern in the gamma range appears to reverse during item retrieval, however. Intrahippocampal phase coherence was found to be stronger during successful item encoding. Our phase coherence data are also consistent with existing reports of a traveling wave for theta oscillations propagating along the septotemporal (longitudinal) axis of the human hippocampus. We examine how our findings fit with theories of functional specialization along the hippocampal axis.
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http://dx.doi.org/10.1002/hipo.22751DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6517838PMC
October 2017