Pattern separation, or the process by which highly similar stimuli or experiences in memory are r... more Pattern separation, or the process by which highly similar stimuli or experiences in memory are represented by non-overlapping neural ensembles, has typically been ascribed to processes supported by the hippocampus. Converging evidence from a wide range of studies, however, suggests that pattern separation is a multistage process supported by a network of brain regions. Based on this evidence, considered together with related findings from the interference resolution literature, we propose the ‘cortico-hippocampal pattern separation’ (CHiPS) framework, which asserts that brain regions involved in cognitive control play a significant role in pattern separation. Particularly, these regions may contribute to pattern separation by (1) resolving interference in sensory regions that project to the hippocampus, thus regulating its cortical input, or (2) directly modulating hippocampal processes in accordance with task demands. Considering recent interest in how hippocampal operations are m...
Current opinion in behavioral sciences, Oct 1, 2017
Our memory for the events we have personally experienced forms a crucial part of our consciousnes... more Our memory for the events we have personally experienced forms a crucial part of our consciousness, helps to define how we think about ourselves and guides our future decisions. Psychologists and neuroscientists have studied the nature and representation of these 'episodic' memories for decades and, while much progress has been made, there is still much to learn. Being able to 're-experience,' or at least reinstate, the spatiotemporal context of the event, that is where and when it occurred, has long been held to be a defining characteristic of episodic memory [1]. Equally, the hippocampus has long been identified as a key player in episodic memory [2]. While it is clear that hippocampal loss leads to an inability to remember not just spatial and temporal aspects of memory but also all manner of relational and/or associative aspects of memory [3], the mechanisms supporting episodic memory still remain elusive.
To address the memory functioning after medial temporal lobe (MTL) surgery for refractory epileps... more To address the memory functioning after medial temporal lobe (MTL) surgery for refractory epilepsy and relationships with the side of the hippocampal removal, 22 patients with pharmaco‐resistant epilepsy who had undergone MTL resection (10 right/12 left) at the Salpêtrière Hospital were compared with 21 matched healthy controls. We designed a specific neuropsychological binding memory test that specifically addressed hippocampal cortex functioning, and left–right material‐specific lateralization. Our results showed that both left and right mesial temporal lobe removal cause a severe memory impairment, for both verbal and visual material. The removal of left medial temporal lobe causes worse memory impairment than the right removal regardless of the stimuli type (verbal or visual) questioning the theory of the hippocampal material‐specific lateralization. The present study provided new evidence for the role of both hippocampus and surrounding cortices in memory‐binding whatever the m...
Supplemental material, Gruber_Supplemental_Material_Table_S3 for The Future of Women in Psycholog... more Supplemental material, Gruber_Supplemental_Material_Table_S3 for The Future of Women in Psychological Science by June Gruber, Jane Mendle, Kristen A. Lindquist, Toni Schmader, Lee Anna Clark, Eliza Bliss-Moreau, Modupe Akinola, Lauren Atlas, Deanna M. Barch, Lisa Feldman Barrett, Jessica L. Borelli, Tiffany Brannon, Silvia A. Bunge, Belinda Campos, Jessica Cantlon, Rona Carter, Adrienne R. Carter-Sowell, Serena Chen, Michelle G. Craske, Amy J. C. Cuddy, Alia Crum, Lila Davachi, Angela L. Duckworth, Sunny J. Dutra, Naomi I. Eisenberger, Melissa Ferguson, Brett Q. Ford, Barbara L. Fredrickson, Sherryl H. Goodman, Alison Gopnik, Valerie Purdie Greenaway, Kate L. Harkness, Mikki Hebl, Wendy Heller, Jill Hooley, Lily Jampol, Sheri L. Johnson, Jutta Joormann, Katherine D. Kinzler, Hedy Kober, Ann M. Kring, Elizabeth Levy Paluck, Tania Lombrozo, Stella F. Lourenco, Kateri McRae, Joan K. Monin, Judith T. Moskowitz, Misaki N. Natsuaki, Gabriele Oettingen, Jennifer H. Pfeifer, Nicole Prause, ...
All in-text references underlined in blue are linked to publications on ResearchGate, letting you... more All in-text references underlined in blue are linked to publications on ResearchGate, letting you access and read them immediately.
Page 267. 8 Functional Neuroimaging of Episodic Memory John DE Gabriel! INTRODUCTION People gain ... more Page 267. 8 Functional Neuroimaging of Episodic Memory John DE Gabriel! INTRODUCTION People gain knowledge and skills through experiences that are recorded, retained, and retrieved by memory systems of the human brain. ...
It has long been known that the medial temporal lobe is crucial for the formation and retrieval o... more It has long been known that the medial temporal lobe is crucial for the formation and retrieval of episodic memories. This region includes the hippocampal formation (the hippocampus proper and subiculum) and the underlying entorhinal, perirhinal, and parahippocampal cortices, all of which receive a unique complement of cortical inputs. How best to characterize the precise roles of these different brain regions and their interactions is of central concern in understanding the medial temporal lobe contributions to episodic memory. Using functional magnetic resonance imaging (fMRI) to assess brain activity while subjects performed an episodic retrieval task, Giovanello et al. (2004) have contributed two important pieces to this puzzle. First, their findings show that the hippocampal formation is differentially recruited when subjects are asked to make memory decisions about the conjunctive relationship (in this case, the co-occurrence) of two stimuli compared to decisions about each st...
Over 40 years of accumulated research has detailed associations between neuroimaging signals meas... more Over 40 years of accumulated research has detailed associations between neuroimaging signals measured during a memory encoding task and later memory performance, across a variety of brain regions, measurement tools, statistical approaches and behavioral tasks. But the interpretation of these Subsequent Memory Effects (SMEs) remains unclear: if the identified signals reflect cognitive and neural mechanisms of memory encoding then the underlying neural activity must be causally related to future memory. However, almost all previous SME analyses do not control for potential confounders of this causal interpretation, such as serial position and item effects. We collect a large fMRI dataset and use a novel experimental design and analysis approach that allows us to statistically adjust for all exogenous confounding variables. We find that, using standard approaches without adjustment, we replicate several univariate and multivariate subsequent memory effects and are able to predict memor...
When our experience violates our predictions, it is adaptive to update our knowledge to promote a... more When our experience violates our predictions, it is adaptive to update our knowledge to promote a more accurate representation of the world and facilitate future predictions. Theoretical models propose that these mnemonic prediction errors should be encoded into a distinct memory trace to prevent interference with previous, conflicting memories. We investigated this proposal by repeatedly exposing participants to pairs of sequentially presented objects (A->B), thus evoking expectations. Then, we violated participants’ expectations by replacing the second object in the pairs with a novel object (A->C). The following item memory test required participants to discriminate between identical old items and similar lures, thus testing detailed and distinctive item memory representations. In two experiments, mnemonic prediction errors enhanced item memory: participants correctly identified more old items as old when those items violated expectations during learning, compared to items ...
Interictal epileptiform discharges (IEDs) can impair memory. The properties of IEDs most detrimen... more Interictal epileptiform discharges (IEDs) can impair memory. The properties of IEDs most detrimental to memory, however, are undefined. We studied the impact of temporal and spatial characteristics of IEDs on list learning. Subjects completed a memory task during intracranial EEG recordings including hippocampal depth and temporal neocortical subdural electrodes. Subjects viewed a series of objects, and after a distracting task, recalled the objects from the list. The impacts of IED presence, duration, and propagation to neocortex during encoding of individual stimuli were assessed. The effects of IED total number and duration during maintenance and recall periods on delayed recall performance were also determined. The influence of IEDs during recall was further investigated by comparing the likelihood of IEDs preceding correctly recalled items vs. periods of no verbal response. Across 6 subjects, we analyzed 28 hippocampal and 139 lateral temporal contacts. Recall performance was poor, with a median of 17.2% correct responses (range 10.4-21.9%). Interictal epileptiform discharges during encoding, maintenance, and recall did not significantly impact task performance, and there was no significant difference between the likelihood of IEDs during correct recall vs. periods of no response. No significant effects of discharge duration during encoding, maintenance, or recall were observed. Interictal epileptiform discharges with spread to lateral temporal cortex during encoding did not adversely impact recall. A post hoc analysis refining model assumptions indicated a negative impact of IED count during the maintenance period, but otherwise confirmed the above results. Our findings suggest no major effect of hippocampal IEDs on list learning, but study limitations, such as baseline hippocampal dysfunction, should be considered. The impact of IEDs during the maintenance period may be a focus of future research.
Reward motivation enhances memory through interactions between mesolimbic, hippocampal, and corti... more Reward motivation enhances memory through interactions between mesolimbic, hippocampal, and cortical systems — both during and after encoding. Developmental changes in these distributed neural circuits may lead to age-related differences in reward-motivated memory and the underlying neural mechanisms. Converging evidence from cross-species studies suggests that subcortical dopamine signaling is increased during adolescence, which may lead to stronger memory representations of rewarding, relative to mundane, events and changes in the contributions of underlying subcortical and cortical brain mechanisms across age. Here, we used fMRI to examine how reward motivation influences the “online” encoding and “offline” post-encoding brain mechanisms that support long-term associative memory from childhood to adulthood in human participants of both sexes. We found that reward motivation led to both age-invariant enhancements and nonlinear age-related differences in associative memory after 24...
In this issue, we, the editors of Neuron, are publishing the Correction from Alexa Tompary and Li... more In this issue, we, the editors of Neuron, are publishing the Correction from Alexa Tompary and Lila Davachi. The correction outlines three errors in the analyses of their original Neuron paper (Tompary and Davachi, 2017, Neuron 96, 228-241). The authors describe the nature of the errors, which all occurred at the pre-processing stages of fMRI analysis, and the effects on their results and conclusions. The errors included the utilization of incorrect motion regressors, the use of different smoothing kernels for the similarity analyses, and, finally, the improper definition of regions of interest. The authors have corrected and re-analyzed the reported data. The main novel claim of the paper remains consistent with what was originally reported. The main conclusion of the paper was that patterns in medial prefrontal cortex and hippocampus represent featural overlap across remote memories. This finding did not change. The second finding that post-encoding connectivity between anterior hippocampus and medial prefrontal cortex is related to the overlap in retrieval similarity at remote, but not recent, time points also did not change. The authors originally reported that episodic reinstatement in anterior and posterior hippocampus was negatively related to the emergence of a common schema representation. The corrected data indicate that this effect is now marginal in posterior hippocampus and not reliable in anterior hippocampus. The errors and their effects on the originally reported findings have been discussed among the Neuron editorial team, with expert reviewers, and the Cell Press Editorial Department leadership team. We appreciate and respect the fact that the authors came forward and expressed the need to correct their published report. More generally, we recognize that these types of errors, especially the combination of multiple errors, may or may not have had a stronger effect on the reported results and that proper data and methods reporting is fundamental for increasing reproducibility in scientific research. Therefore, we would like to take this opportunity to remind the neuroscience community of the importance of proper reporting of experimental design, analysis workflows, and quality control checks before submission and publication of their study. Errors in scripts or elsewhere and their cascading effects could thus be minimized by appropriate controls and, wherever possible, replication of the experiments or analyses. Useful recommendations were issued by the Committee on Best Practices in Data Analysis and Sharing (COBIDAS), set up by the Organization for Human Brain Mapping.
Everyday life unfolds continuously, yet we tend to remember past experiences as discrete event se... more Everyday life unfolds continuously, yet we tend to remember past experiences as discrete event sequences or episodes. Although this phenomenon has been well documented, the brain mechanisms that support the transformation of continuous experience into memorable episodes remain unknown. Here we show that a sudden change in context, or ‘event boundary’, elicits a burst of autonomic arousal, as indexed by pupil dilation. These boundaries during dynamic experience also led to the segmentation of adjacent episodes in later memory, evidenced by changes in memory for the timing, order, and perceptual details of recent event sequences. Critically, we find that distinct cognitive components of this pupil response were associated with both subjective (temporal distance judgements) and objective (temporal order discrimination) measures of episodic memory, suggesting that multiple arousal-mediated cognitive processes help construct meaningful mnemonic events. Together, these findings reveal tha...
ABSTRACTSome patients with medically refractory focal epilepsy are chronically implanted with a b... more ABSTRACTSome patients with medically refractory focal epilepsy are chronically implanted with a brain-responsive neurostimulation device (the RNS® System), permitting neurophysiological measurements at millisecond resolution. This clinical device can be adapted to measure hippocampal dynamics time-locked to cognitive tasks. We illustrate the technique with a proof of concept in three patients previously implanted with the RNS System as they engage in an associative memory task, measured months apart. Hippocampal activity measured in successful encoding in RNS System patients mirrors that in surgical patients during intracranial electroencephalography (iEEG), suggesting that chronic iEEG allows sensitive measurements of hippocampal physiology over prolonged timescales.
Direct recordings from the human brain have historically involved epilepsy patients undergoing in... more Direct recordings from the human brain have historically involved epilepsy patients undergoing invasive electroencephalography (iEEG) for surgery. However, these measurements are temporally limited and affected by clinical variables. The RNS System (NeuroPace, Inc.) is a chronic, closed-loop electrographic seizure detection and stimulation system. When adapted by investigators for research, it facilitates cognitive testing in a controlled ambulatory setting, with measurements collected over months to years. We utilized an associative learning paradigm in 5 patients with traditional iEEG and 3 patients with chronic iEEG, and found increased hippocampal gamma (60–100 Hz) sustained at 1.3–1.5 seconds during encoding in successful versus failed trials in surgical patients, with similar results in our RNS System patients (1.4–1.6 seconds). Our findings replicate other studies demonstrating that sustained hippocampal gamma supports encoding. Importantly, we have validated the RNS System t...
The ability to generalize from and distinguish between aversive memories and novel experiences is... more The ability to generalize from and distinguish between aversive memories and novel experiences is critical to survival. Previous research has revealed mechanisms underlying generalization of threat-conditioned defensive responses, but little is known about generalization of episodic memory for threatening events. Here we tested if aversive learning influences generalization of episodic memory for threatening events in human adults. Subjects underwent Pavlovian threat-conditioning in which objects from one category were paired with a shock and objects from a different category were unpaired. The next day, subjects underwent a recognition memory test that included old, highly similar, and entirely novel items from the shock-paired and shock-unpaired object categories. Results showed that items highly similar to those from the object category previously paired with shock were mistaken for old items more often than items from the shock-unpaired category. This finding indicates that threat learning promotes generalization of episodic memory, and is consistent with the idea that threat generalization is an active process that may be adaptive for avoiding a myriad of potential threats following an emotional experience. Enhanced generalization of aversive episodic memories may be maladaptive, however, when old threat memories are inappropriately reactivated in harmless situations, exemplified in a number of stress- and anxiety-related disorders. (PsycINFO Database Record (c) 2019 APA, all rights reserved).
Songs naturally bind lyrics and melody into a unified representation. Using a subsequent memory p... more Songs naturally bind lyrics and melody into a unified representation. Using a subsequent memory paradigm, we examined the neural processes associated with binding lyrics and melodies during song encoding. Participants were presented with songs in two conditions: a unified condition (melodies sung with lyrics), and a separate condition (melodies sung with the syllable "la"). In both cases, written lyrics were displayed and participants were instructed to memorize them by repeating them covertly or by generating mental images of the songs. We expected the unified condition to recruit the posterior superior temporal gyrus, known to be involved in perceptual integration of songs, as well as the left inferior frontal gyrus (IFG). Conversely, we hypothesized that the separate condition would engage a larger network including the hippocampus to bind lyrics and melodies of songs, and the basal ganglia and the cerebellum to ensure the correct sequence coupling of verbal and musical information in time. Binding lyrics and melodies in the unified condition revealed activation of the left IFG, bilateral middle temporal gyrus (MTG), and left motor cortex, suggesting a strong linguistic processing for this condition. Binding in the separate compared to the unified condition revealed greater activity in the right hippocampus as well as other areas including the left caudate, left cerebellum, and right IFG. This study provides novel evidence for the role of the right hippocampus in binding lyrics and melodies in songs. Results are discussed in light of studies of binding in the visual domain and highlight the role of regions involved in timing and synchronization such as the basal ganglia and the cerebellum.
Pattern separation, or the process by which highly similar stimuli or experiences in memory are r... more Pattern separation, or the process by which highly similar stimuli or experiences in memory are represented by non-overlapping neural ensembles, has typically been ascribed to processes supported by the hippocampus. Converging evidence from a wide range of studies, however, suggests that pattern separation is a multistage process supported by a network of brain regions. Based on this evidence, considered together with related findings from the interference resolution literature, we propose the ‘cortico-hippocampal pattern separation’ (CHiPS) framework, which asserts that brain regions involved in cognitive control play a significant role in pattern separation. Particularly, these regions may contribute to pattern separation by (1) resolving interference in sensory regions that project to the hippocampus, thus regulating its cortical input, or (2) directly modulating hippocampal processes in accordance with task demands. Considering recent interest in how hippocampal operations are m...
Current opinion in behavioral sciences, Oct 1, 2017
Our memory for the events we have personally experienced forms a crucial part of our consciousnes... more Our memory for the events we have personally experienced forms a crucial part of our consciousness, helps to define how we think about ourselves and guides our future decisions. Psychologists and neuroscientists have studied the nature and representation of these 'episodic' memories for decades and, while much progress has been made, there is still much to learn. Being able to 're-experience,' or at least reinstate, the spatiotemporal context of the event, that is where and when it occurred, has long been held to be a defining characteristic of episodic memory [1]. Equally, the hippocampus has long been identified as a key player in episodic memory [2]. While it is clear that hippocampal loss leads to an inability to remember not just spatial and temporal aspects of memory but also all manner of relational and/or associative aspects of memory [3], the mechanisms supporting episodic memory still remain elusive.
To address the memory functioning after medial temporal lobe (MTL) surgery for refractory epileps... more To address the memory functioning after medial temporal lobe (MTL) surgery for refractory epilepsy and relationships with the side of the hippocampal removal, 22 patients with pharmaco‐resistant epilepsy who had undergone MTL resection (10 right/12 left) at the Salpêtrière Hospital were compared with 21 matched healthy controls. We designed a specific neuropsychological binding memory test that specifically addressed hippocampal cortex functioning, and left–right material‐specific lateralization. Our results showed that both left and right mesial temporal lobe removal cause a severe memory impairment, for both verbal and visual material. The removal of left medial temporal lobe causes worse memory impairment than the right removal regardless of the stimuli type (verbal or visual) questioning the theory of the hippocampal material‐specific lateralization. The present study provided new evidence for the role of both hippocampus and surrounding cortices in memory‐binding whatever the m...
Supplemental material, Gruber_Supplemental_Material_Table_S3 for The Future of Women in Psycholog... more Supplemental material, Gruber_Supplemental_Material_Table_S3 for The Future of Women in Psychological Science by June Gruber, Jane Mendle, Kristen A. Lindquist, Toni Schmader, Lee Anna Clark, Eliza Bliss-Moreau, Modupe Akinola, Lauren Atlas, Deanna M. Barch, Lisa Feldman Barrett, Jessica L. Borelli, Tiffany Brannon, Silvia A. Bunge, Belinda Campos, Jessica Cantlon, Rona Carter, Adrienne R. Carter-Sowell, Serena Chen, Michelle G. Craske, Amy J. C. Cuddy, Alia Crum, Lila Davachi, Angela L. Duckworth, Sunny J. Dutra, Naomi I. Eisenberger, Melissa Ferguson, Brett Q. Ford, Barbara L. Fredrickson, Sherryl H. Goodman, Alison Gopnik, Valerie Purdie Greenaway, Kate L. Harkness, Mikki Hebl, Wendy Heller, Jill Hooley, Lily Jampol, Sheri L. Johnson, Jutta Joormann, Katherine D. Kinzler, Hedy Kober, Ann M. Kring, Elizabeth Levy Paluck, Tania Lombrozo, Stella F. Lourenco, Kateri McRae, Joan K. Monin, Judith T. Moskowitz, Misaki N. Natsuaki, Gabriele Oettingen, Jennifer H. Pfeifer, Nicole Prause, ...
All in-text references underlined in blue are linked to publications on ResearchGate, letting you... more All in-text references underlined in blue are linked to publications on ResearchGate, letting you access and read them immediately.
Page 267. 8 Functional Neuroimaging of Episodic Memory John DE Gabriel! INTRODUCTION People gain ... more Page 267. 8 Functional Neuroimaging of Episodic Memory John DE Gabriel! INTRODUCTION People gain knowledge and skills through experiences that are recorded, retained, and retrieved by memory systems of the human brain. ...
It has long been known that the medial temporal lobe is crucial for the formation and retrieval o... more It has long been known that the medial temporal lobe is crucial for the formation and retrieval of episodic memories. This region includes the hippocampal formation (the hippocampus proper and subiculum) and the underlying entorhinal, perirhinal, and parahippocampal cortices, all of which receive a unique complement of cortical inputs. How best to characterize the precise roles of these different brain regions and their interactions is of central concern in understanding the medial temporal lobe contributions to episodic memory. Using functional magnetic resonance imaging (fMRI) to assess brain activity while subjects performed an episodic retrieval task, Giovanello et al. (2004) have contributed two important pieces to this puzzle. First, their findings show that the hippocampal formation is differentially recruited when subjects are asked to make memory decisions about the conjunctive relationship (in this case, the co-occurrence) of two stimuli compared to decisions about each st...
Over 40 years of accumulated research has detailed associations between neuroimaging signals meas... more Over 40 years of accumulated research has detailed associations between neuroimaging signals measured during a memory encoding task and later memory performance, across a variety of brain regions, measurement tools, statistical approaches and behavioral tasks. But the interpretation of these Subsequent Memory Effects (SMEs) remains unclear: if the identified signals reflect cognitive and neural mechanisms of memory encoding then the underlying neural activity must be causally related to future memory. However, almost all previous SME analyses do not control for potential confounders of this causal interpretation, such as serial position and item effects. We collect a large fMRI dataset and use a novel experimental design and analysis approach that allows us to statistically adjust for all exogenous confounding variables. We find that, using standard approaches without adjustment, we replicate several univariate and multivariate subsequent memory effects and are able to predict memor...
When our experience violates our predictions, it is adaptive to update our knowledge to promote a... more When our experience violates our predictions, it is adaptive to update our knowledge to promote a more accurate representation of the world and facilitate future predictions. Theoretical models propose that these mnemonic prediction errors should be encoded into a distinct memory trace to prevent interference with previous, conflicting memories. We investigated this proposal by repeatedly exposing participants to pairs of sequentially presented objects (A->B), thus evoking expectations. Then, we violated participants’ expectations by replacing the second object in the pairs with a novel object (A->C). The following item memory test required participants to discriminate between identical old items and similar lures, thus testing detailed and distinctive item memory representations. In two experiments, mnemonic prediction errors enhanced item memory: participants correctly identified more old items as old when those items violated expectations during learning, compared to items ...
Interictal epileptiform discharges (IEDs) can impair memory. The properties of IEDs most detrimen... more Interictal epileptiform discharges (IEDs) can impair memory. The properties of IEDs most detrimental to memory, however, are undefined. We studied the impact of temporal and spatial characteristics of IEDs on list learning. Subjects completed a memory task during intracranial EEG recordings including hippocampal depth and temporal neocortical subdural electrodes. Subjects viewed a series of objects, and after a distracting task, recalled the objects from the list. The impacts of IED presence, duration, and propagation to neocortex during encoding of individual stimuli were assessed. The effects of IED total number and duration during maintenance and recall periods on delayed recall performance were also determined. The influence of IEDs during recall was further investigated by comparing the likelihood of IEDs preceding correctly recalled items vs. periods of no verbal response. Across 6 subjects, we analyzed 28 hippocampal and 139 lateral temporal contacts. Recall performance was poor, with a median of 17.2% correct responses (range 10.4-21.9%). Interictal epileptiform discharges during encoding, maintenance, and recall did not significantly impact task performance, and there was no significant difference between the likelihood of IEDs during correct recall vs. periods of no response. No significant effects of discharge duration during encoding, maintenance, or recall were observed. Interictal epileptiform discharges with spread to lateral temporal cortex during encoding did not adversely impact recall. A post hoc analysis refining model assumptions indicated a negative impact of IED count during the maintenance period, but otherwise confirmed the above results. Our findings suggest no major effect of hippocampal IEDs on list learning, but study limitations, such as baseline hippocampal dysfunction, should be considered. The impact of IEDs during the maintenance period may be a focus of future research.
Reward motivation enhances memory through interactions between mesolimbic, hippocampal, and corti... more Reward motivation enhances memory through interactions between mesolimbic, hippocampal, and cortical systems — both during and after encoding. Developmental changes in these distributed neural circuits may lead to age-related differences in reward-motivated memory and the underlying neural mechanisms. Converging evidence from cross-species studies suggests that subcortical dopamine signaling is increased during adolescence, which may lead to stronger memory representations of rewarding, relative to mundane, events and changes in the contributions of underlying subcortical and cortical brain mechanisms across age. Here, we used fMRI to examine how reward motivation influences the “online” encoding and “offline” post-encoding brain mechanisms that support long-term associative memory from childhood to adulthood in human participants of both sexes. We found that reward motivation led to both age-invariant enhancements and nonlinear age-related differences in associative memory after 24...
In this issue, we, the editors of Neuron, are publishing the Correction from Alexa Tompary and Li... more In this issue, we, the editors of Neuron, are publishing the Correction from Alexa Tompary and Lila Davachi. The correction outlines three errors in the analyses of their original Neuron paper (Tompary and Davachi, 2017, Neuron 96, 228-241). The authors describe the nature of the errors, which all occurred at the pre-processing stages of fMRI analysis, and the effects on their results and conclusions. The errors included the utilization of incorrect motion regressors, the use of different smoothing kernels for the similarity analyses, and, finally, the improper definition of regions of interest. The authors have corrected and re-analyzed the reported data. The main novel claim of the paper remains consistent with what was originally reported. The main conclusion of the paper was that patterns in medial prefrontal cortex and hippocampus represent featural overlap across remote memories. This finding did not change. The second finding that post-encoding connectivity between anterior hippocampus and medial prefrontal cortex is related to the overlap in retrieval similarity at remote, but not recent, time points also did not change. The authors originally reported that episodic reinstatement in anterior and posterior hippocampus was negatively related to the emergence of a common schema representation. The corrected data indicate that this effect is now marginal in posterior hippocampus and not reliable in anterior hippocampus. The errors and their effects on the originally reported findings have been discussed among the Neuron editorial team, with expert reviewers, and the Cell Press Editorial Department leadership team. We appreciate and respect the fact that the authors came forward and expressed the need to correct their published report. More generally, we recognize that these types of errors, especially the combination of multiple errors, may or may not have had a stronger effect on the reported results and that proper data and methods reporting is fundamental for increasing reproducibility in scientific research. Therefore, we would like to take this opportunity to remind the neuroscience community of the importance of proper reporting of experimental design, analysis workflows, and quality control checks before submission and publication of their study. Errors in scripts or elsewhere and their cascading effects could thus be minimized by appropriate controls and, wherever possible, replication of the experiments or analyses. Useful recommendations were issued by the Committee on Best Practices in Data Analysis and Sharing (COBIDAS), set up by the Organization for Human Brain Mapping.
Everyday life unfolds continuously, yet we tend to remember past experiences as discrete event se... more Everyday life unfolds continuously, yet we tend to remember past experiences as discrete event sequences or episodes. Although this phenomenon has been well documented, the brain mechanisms that support the transformation of continuous experience into memorable episodes remain unknown. Here we show that a sudden change in context, or ‘event boundary’, elicits a burst of autonomic arousal, as indexed by pupil dilation. These boundaries during dynamic experience also led to the segmentation of adjacent episodes in later memory, evidenced by changes in memory for the timing, order, and perceptual details of recent event sequences. Critically, we find that distinct cognitive components of this pupil response were associated with both subjective (temporal distance judgements) and objective (temporal order discrimination) measures of episodic memory, suggesting that multiple arousal-mediated cognitive processes help construct meaningful mnemonic events. Together, these findings reveal tha...
ABSTRACTSome patients with medically refractory focal epilepsy are chronically implanted with a b... more ABSTRACTSome patients with medically refractory focal epilepsy are chronically implanted with a brain-responsive neurostimulation device (the RNS® System), permitting neurophysiological measurements at millisecond resolution. This clinical device can be adapted to measure hippocampal dynamics time-locked to cognitive tasks. We illustrate the technique with a proof of concept in three patients previously implanted with the RNS System as they engage in an associative memory task, measured months apart. Hippocampal activity measured in successful encoding in RNS System patients mirrors that in surgical patients during intracranial electroencephalography (iEEG), suggesting that chronic iEEG allows sensitive measurements of hippocampal physiology over prolonged timescales.
Direct recordings from the human brain have historically involved epilepsy patients undergoing in... more Direct recordings from the human brain have historically involved epilepsy patients undergoing invasive electroencephalography (iEEG) for surgery. However, these measurements are temporally limited and affected by clinical variables. The RNS System (NeuroPace, Inc.) is a chronic, closed-loop electrographic seizure detection and stimulation system. When adapted by investigators for research, it facilitates cognitive testing in a controlled ambulatory setting, with measurements collected over months to years. We utilized an associative learning paradigm in 5 patients with traditional iEEG and 3 patients with chronic iEEG, and found increased hippocampal gamma (60–100 Hz) sustained at 1.3–1.5 seconds during encoding in successful versus failed trials in surgical patients, with similar results in our RNS System patients (1.4–1.6 seconds). Our findings replicate other studies demonstrating that sustained hippocampal gamma supports encoding. Importantly, we have validated the RNS System t...
The ability to generalize from and distinguish between aversive memories and novel experiences is... more The ability to generalize from and distinguish between aversive memories and novel experiences is critical to survival. Previous research has revealed mechanisms underlying generalization of threat-conditioned defensive responses, but little is known about generalization of episodic memory for threatening events. Here we tested if aversive learning influences generalization of episodic memory for threatening events in human adults. Subjects underwent Pavlovian threat-conditioning in which objects from one category were paired with a shock and objects from a different category were unpaired. The next day, subjects underwent a recognition memory test that included old, highly similar, and entirely novel items from the shock-paired and shock-unpaired object categories. Results showed that items highly similar to those from the object category previously paired with shock were mistaken for old items more often than items from the shock-unpaired category. This finding indicates that threat learning promotes generalization of episodic memory, and is consistent with the idea that threat generalization is an active process that may be adaptive for avoiding a myriad of potential threats following an emotional experience. Enhanced generalization of aversive episodic memories may be maladaptive, however, when old threat memories are inappropriately reactivated in harmless situations, exemplified in a number of stress- and anxiety-related disorders. (PsycINFO Database Record (c) 2019 APA, all rights reserved).
Songs naturally bind lyrics and melody into a unified representation. Using a subsequent memory p... more Songs naturally bind lyrics and melody into a unified representation. Using a subsequent memory paradigm, we examined the neural processes associated with binding lyrics and melodies during song encoding. Participants were presented with songs in two conditions: a unified condition (melodies sung with lyrics), and a separate condition (melodies sung with the syllable "la"). In both cases, written lyrics were displayed and participants were instructed to memorize them by repeating them covertly or by generating mental images of the songs. We expected the unified condition to recruit the posterior superior temporal gyrus, known to be involved in perceptual integration of songs, as well as the left inferior frontal gyrus (IFG). Conversely, we hypothesized that the separate condition would engage a larger network including the hippocampus to bind lyrics and melodies of songs, and the basal ganglia and the cerebellum to ensure the correct sequence coupling of verbal and musical information in time. Binding lyrics and melodies in the unified condition revealed activation of the left IFG, bilateral middle temporal gyrus (MTG), and left motor cortex, suggesting a strong linguistic processing for this condition. Binding in the separate compared to the unified condition revealed greater activity in the right hippocampus as well as other areas including the left caudate, left cerebellum, and right IFG. This study provides novel evidence for the role of the right hippocampus in binding lyrics and melodies in songs. Results are discussed in light of studies of binding in the visual domain and highlight the role of regions involved in timing and synchronization such as the basal ganglia and the cerebellum.
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