Publications by authors named "Michael D Rugg"

152 Publications

When the brain, but not the person, remembers: Cortical reinstatement is modulated by retrieval goal in developmental amnesia.

Neuropsychologia 2021 Feb 12;154:107788. Epub 2021 Feb 12.

UCL Great Ormond Street Institute for Child Health, London, UK. Electronic address:

Developmental amnesia (DA) is associated with early hippocampal damage and subsequent episodic amnesia emerging in childhood alongside age-appropriate development of semantic knowledge. We employed fMRI to assess whether patients with DA show evidence of 'cortical reinstatement', a neural correlate of episodic memory, despite their amnesia. At study, 23 participants (5 patients) were presented with words overlaid on a scene or a scrambled image for later recognition. Scene reinstatement was indexed by scene memory effects (greater activity for previously presented words paired with a scene rather than scrambled images) that overlapped with scene perception effects. Patients with DA demonstrated scene reinstatement effects in the parahippocampal and retrosplenial cortex that were equivalent to those shown by healthy controls. Behaviourally, however, patients with DA showed markedly impaired scene memory. The data indicate that reinstatement can occur despite hippocampal damage, but that cortical reinstatement is insufficient to support accurate memory performance. Furthermore, scene reinstatement effects were diminished during a retrieval task in which scene information was not relevant for accurate responding, indicating that strategic mnemonic processes operate normally in DA. The data suggest that cortical reinstatement of trial-specific contextual information is decoupled from the experience of recollection in the presence of severe hippocampal atrophy.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1016/j.neuropsychologia.2021.107788DOI Listing
February 2021

Neural correlates of post-retrieval monitoring in older adults are preserved under divided attention, but are decoupled from memory performance.

Neurobiol Aging 2021 01 17;97:106-119. Epub 2020 Oct 17.

Center for Vital Longevity, University of Texas at Dallas, Dallas, TX, USA; School of Psychology, University of East Anglia, Norwich, UK.

Post-retrieval monitoring is associated with engagement of anterior cingulate and dorsolateral prefrontal cortex. Recent fMRI studies reported age-invariant monitoring effects in these regions and an age-invariant correlation between these effects and memory performance. The present study examined monitoring effects during associative recognition (difference in activity elicited by 'rearranged' and 'intact' test pairs) under single and dual (tone detection) task conditions in young and older adults (Ns = 28 per group). It was predicted that, for the older adults only, dual tasking would attenuate memory performance and monitoring effects and weaken their correlation. Consistent with this prediction, in the older group imposition of the secondary task led to lower memory performance and elimination of the relationship between monitoring effects and performance. However, the size of the effects did not differ between single and dual task conditions. The findings suggest that the decline in older adults' memory performance in the dual task condition resulted not from impaired monitoring, but from a different cause that also weakened the dependence of performance on monitoring.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1016/j.neurobiolaging.2020.10.010DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7736156PMC
January 2021

Hippocampal Theta Oscillations Support Successful Associative Memory Formation.

J Neurosci 2020 12 6;40(49):9507-9518. Epub 2020 Nov 6.

Department of Neurosurgery, University of Texas Southwestern Medical Center, Dallas, Texas 75390

Models of memory formation posit that episodic memory formation depends critically on the hippocampus, which binds features of an event to its context. For this reason, the contrast between study items that are later recollected with their associative pair versus those for which no association is made fails should reveal electrophysiological patterns in the hippocampus selectively involved in associative memory encoding. Extensive data from studies in rodents support a model in which theta oscillations fulfill this role, but results in humans have not been as clear. Here, we used an associative recognition memory procedure to identify hippocampal correlates of successful associative memory encoding and retrieval in patients (10 females and 9 males) undergoing intracranial EEG monitoring. We identified a dissociation between 2-5 Hz and 5-9 Hz theta oscillations, by which power increases in 2-5 Hz oscillations were uniquely linked with successful associative memory in both the anterior and posterior hippocampus. These oscillations exhibited a significant phase reset that also predicted successful associative encoding and distinguished recollected from nonrecollected items at retrieval, as well as contributing to relatively greater reinstatement of encoding-related patterns for recollected versus nonrecollected items. Our results provide direct electrophysiological evidence that 2-5 Hz hippocampal theta oscillations preferentially support the formation of associative memories, although we also observed memory-related effects in the 5-9 Hz frequency range using measures such as phase reset and reinstatement of oscillatory activity. Models of episodic memory encoding predict that theta oscillations support the formation of interitem associations. We used an associative recognition task designed to elicit strong hippocampal activation to test this prediction in human neurosurgical patients implanted with intracranial electrodes. The findings suggest that 2-5 Hz theta oscillatory power and phase reset in the hippocampus are selectively associated with associative memory judgments. Furthermore, reinstatement of oscillatory patterns in the hippocampus was stronger for successful recollection. Collectively, the findings support a role for hippocampal theta oscillations in human associative memory.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1523/JNEUROSCI.0767-20.2020DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7724134PMC
December 2020

Electrophysiological correlates of the perceptual fluency effect on recognition memory in different fluency contexts.

Neuropsychologia 2020 11 29;148:107639. Epub 2020 Sep 29.

Center for Vital Longevity, University of Texas at Dallas, Dallas, 75235, USA; School of Psychology, University of East Anglia, Norwich, NR4 7TJ, UK.

The present study used event-related potentials (ERPs) to investigate the contribution of perceptual fluency to recognition memory in different fluency contexts. In a recognition memory test with a modified remember-know paradigm, we employed conceptually impoverished items (kaleidoscope images) as stimuli and manipulated the perceptual fluency of recognition test cues through masked repetition priming. There were two fluency context conditions. In the random fluency context (RC) condition, primed and unprimed trials were randomly inter-mixed. In the blocked fluency context (BC) condition, primed and unprimed trials were grouped into blocks. Behavioral results showed that priming elevated the incidence of remember hits and the accuracy of remember judgements in the RC condition; no such effects were evident in the BC condition. In addition, priming effects on reaction times were found only for remember hit responses in the RC condition. The ERP results revealed an early100-200 ms effect related to masked repetition priming, which took the form of greater positivity for primed than unprimed trials. This effect was modulated neither by fluency context or response type. The present findings suggest that perceptual fluency induced by masked repetition priming affects recollection-related memory judgments in a specific fluency context and indicate that relative, rather absolute, fluency plays a critical role in influencing recognition memory judgments.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1016/j.neuropsychologia.2020.107639DOI Listing
November 2020

Effects of Age on Prestimulus Neural Activity Predictive of Successful Memory Encoding: An fMRI Study.

Cereb Cortex 2021 Jan;31(2):917-932

Center for Vital Longevity, University of Texas at Dallas, Dallas, TX 75235, USA.

Prestimulus subsequent memory effects (SMEs)-differences in neural activity preceding the onset of study items that are predictive of later memory performance-have consistently been reported in young adults. The present functional magnetic resonance imaging experiment investigated potential age-related differences in prestimulus SMEs. During study, healthy young and older participants made one of two semantic judgments on images, with the judgment signaled by a preceding cue. In test phase, participants first made an item recognition judgment and, for each item judged old, a source memory judgment. Age-invariant prestimulus SMEs were observed in left dorsomedial prefrontal cortex, left hippocampus, and right subgenual cortex. In each case, the effects reflected lower blood oxygen level dependent signal for later recognized items, regardless of source accuracy, than for unrecognized items. A similar age-invariant pattern was observed in left orbitofrontal cortex, but this effect was specific to items attracting a correct source response compared to unrecognized items. In contrast, the left angular gyrus and fusiform cortex demonstrated negative prestimulus SMEs that were exclusive to young participants. The findings indicate that age differences in prestimulus SMEs are regionally specific and suggest that prestimulus SMEs reflect multiple cognitive processes, only some of which are vulnerable to advancing age.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1093/cercor/bhaa265DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7906785PMC
January 2021

Direct brain recordings identify hippocampal and cortical networks that distinguish successful versus failed episodic memory retrieval.

Neuropsychologia 2020 10 29;147:107595. Epub 2020 Aug 29.

Department of Neurosurgery, University of Texas Southwestern, Dallas, TX 75390, USA.

Human data collected using noninvasive imaging techniques have established the importance of parietal regions towards episodic memory retrieval, including the angular gyrus and posterior cingulate cortex. Such regions comprise part of a putative core episodic retrieval network. In free recall, comparisons between contextually appropriate and inappropriate recall events (i.e. prior list intrusions) provide the opportunity to study memory retrieval networks supporting veridical recall, and existing findings predict that differences in electrical activity in these brain regions should be identified according to the accuracy of recall. However, prior iEEG studies, utilizing principally subdural grid electrodes, have not fully characterized brain activity in parietal regions during memory retrieval and have not examined connectivity between core recollection areas and the hippocampus or prefrontal cortex. Here, we employed a data set obtained from 100 human patients implanted with stereo EEG electrodes for seizure mapping purposes as they performed a free recall task. This data set allowed us to separately analyze activity in midline versus lateral parietal brain regions, and in anterior versus posterior hippocampus, to identify areas in which retrieval-related activity predicted the recollection of a correct versus an incorrect memory. With the wide coverage afforded by the stereo EEG approach, we were also able to examine interregional connectivity. Our key findings were that differences in gamma band activity in the angular gyrus, precuneus, posterior temporal cortex, and posterior (more than anterior) hippocampus discriminated accurate versus inaccurate recall as well as active retrieval versus memory search. The left angular gyrus exhibited a significant power decrease preceding list intrusions as well as unique phase-amplitude coupling properties, whereas the prefrontal cortex was unique in exhibiting a power increase during list intrusions. Analysis of connectivity revealed significant hemispheric asymmetry, with relatively sparse left-sided functional connections compared to the right hemisphere. One exception to this finding was elevated connectivity between the prefrontal cortex and left angular gyrus. This finding is interpreted as evidence for the engagement of prefrontal cortex in memory monitoring and mnemonic decision-making.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1016/j.neuropsychologia.2020.107595DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7554101PMC
October 2020

The effect of age on recollection is not moderated by differential estimation methods.

Memory 2020 09 1;28(8):1067-1077. Epub 2020 Sep 1.

Center for Vital Longevity, University of Texas at Dallas, Dallas, TX, USA.

Episodic memory performance declines with increasing age. It has sometimes been reported that this decline is more marked when episodic recollection is estimated by "objective" measures such as source memory performance than when it is estimated by "subjective" measures such as the "Remember/Know" procedure. Here, our main goal was to directly contrast recollection estimates derived from these procedures in the same samples of young and older participants (24 adults per age group, within-subjects manipulation of test procedure). Following identical study phases in which words were paired with either faces or scenes, participants' memories were assessed in separate test blocks using either Remember/Know or source memory procedures. Contrary to several prior reports, the deleterious effects of age on recollection estimates did not differ according to test type. Thus, we found no evidence that age differentially impacts subjective and objective recollection estimates. Additionally, and consistent with prior findings, effects of age on estimates of familiarity-driven recognition were small and non-significant.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1080/09658211.2020.1813781DOI Listing
September 2020

Age Differences In Retrieval-Related Reinstatement Reflect Age-Related Dedifferentiation At Encoding.

Cereb Cortex 2021 Jan;31(1):106-122

Center for Vital Longevity, University of Texas at Dallas, 1600 Viceroy Dr. #800, Dallas, TX 75235.

Age-related reductions in neural selectivity have been linked to cognitive decline. We examined whether age differences in the strength of retrieval-related cortical reinstatement could be explained by analogous differences in neural selectivity at encoding, and whether reinstatement was associated with memory performance in an age-dependent or an age-independent manner. Young and older adults underwent fMRI as they encoded words paired with images of faces or scenes. During a subsequent scanned memory test participants judged whether test words were studied or unstudied and, for words judged studied, also made a source memory judgment about the associated image category. Using multi-voxel pattern similarity analyses, we identified robust evidence for reduced scene reinstatement in older relative to younger adults. This decline was however largely explained by age differences in neural differentiation at encoding; moreover, a similar relationship between neural selectivity at encoding and retrieval was evident in young participants. The results suggest that, regardless of age, the selectivity with which events are neurally processed at the time of encoding can determine the strength of retrieval-related cortical reinstatement.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1093/cercor/bhaa210DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7727391PMC
January 2021

Recollection-related hippocampal fMRI effects predict longitudinal memory change in healthy older adults.

Neuropsychologia 2020 09 19;146:107537. Epub 2020 Jun 19.

Center for Vital Longevity and School of Behavioral and Brain Sciences, The University of Texas at Dallas, Dallas, TX, 75235, USA; School of Psychology, University of East Anglia, Norwich, NR4 7TJ, UK.

Prior fMRI studies have reported relationships between memory-related activity in the hippocampus and in-scanner memory performance, but whether such activity is predictive of longitudinal memory change remains unclear. Here, we administered a neuropsychological test battery to a sample of cognitively healthy older adults on three occasions, the second and third sessions occurring one month and three years after the first session. Structural and functional MRI data were acquired between the first two sessions. The fMRI data were derived from an associative recognition procedure and allowed estimation of hippocampal effects associated with both successful associative encoding and successful associative recognition (recollection). Baseline memory performance and memory change were evaluated using memory component scores derived from a principal components analysis of the neuropsychological test scores. Across participants, right hippocampal encoding effects correlated significantly with baseline memory performance after controlling for chronological age. Additionally, both left and right hippocampal associative recognition effects correlated negatively with longitudinal memory decline after controlling for age, and the relationship with the left hippocampal effect remained after also controlling for left hippocampal volume. Thus, in cognitively healthy older adults, the magnitude of hippocampal recollection effects appears to be a robust predictor of future memory change.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1016/j.neuropsychologia.2020.107537DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7502538PMC
September 2020

Early-life education may help bolster declarative memory in old age, especially for women.

Neuropsychol Dev Cogn B Aging Neuropsychol Cogn 2021 Mar 5;28(2):218-252. Epub 2020 Jun 5.

Department of Neuroscience, Georgetown University , Washington, DC, USA.

Although declarative memory declines with age, sex and education might moderate these weaknesses. We investigated effects of sex and education on nonverbal declarative (recognition) memory in 704 older adults (aged 58-98, 0-17 years of education). Items were drawings of real and made-up objects. Age negatively impacted declarative memory, though this age effect was moderated by sex and object-type: it was steeper for males than females, but only for real objects. Education was positively associated with memory, but also interacted with sex and object-type: education benefited women more than men (countering the age effects, especially for women), and remembering real more than made-up objects. The findings suggest that nonverbal memory in older adults is associated negatively with age but positively with education; both effects are modulated by sex, and by whether learning relates to preexisting or new information. The study suggests downstream benefits from education, especially for girls.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1080/13825585.2020.1736497DOI Listing
March 2021

Neural Differentiation is Moderated by Age in Scene-Selective, But Not Face-Selective, Cortical Regions.

eNeuro 2020 May/Jun;7(3). Epub 2020 May 21.

Center for Vital Longevity, University of Texas at Dallas, Dallas, TX 75235.

The aging brain is characterized by neural dedifferentiation, an apparent decrease in the functional selectivity of category-selective cortical regions. Age-related reductions in neural differentiation have been proposed to play a causal role in cognitive aging. Recent findings suggest, however, that age-related dedifferentiation is not equally evident for all stimulus categories and, additionally, that the relationship between neural differentiation and cognitive performance is not moderated by age. In light of these findings, in the present experiment, younger and older human adults (males and females) underwent fMRI as they studied words paired with images of scenes or faces before a subsequent memory task. Neural selectivity was measured in two scene-selective (parahippocampal place area (PPA) and retrosplenial cortex (RSC)] and two face-selective [fusiform face area (FFA) and occipital face area (OFA)] regions using both a univariate differentiation index and multivoxel pattern similarity analysis. Both methods provided highly convergent results, which revealed evidence of age-related reductions in neural dedifferentiation in scene-selective but not face-selective cortical regions. Additionally, neural differentiation in the PPA demonstrated a positive, age-invariant relationship with subsequent source memory performance (recall of the image category paired with each recognized test word). These findings extend prior findings suggesting that age-related neural dedifferentiation is not a ubiquitous phenomenon, and that the specificity of neural responses to scenes is predictive of subsequent memory performance independently of age.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1523/ENEURO.0142-20.2020DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7242814PMC
May 2020

Age-related neural dedifferentiation and cognition.

Curr Opin Behav Sci 2020 Apr 3;32:7-14. Epub 2020 Feb 3.

Center for Vital Longevity and School of Behavioral and Brain Sciences, University of Texas at Dallas, 1600 Viceroy Dr., Suite 800, Dallas, TX, 75235, United States.

This review focuses on possible contributions of neural dedifferentiation to age-related cognitive decline. Neural dedifferentiation is held to reflect a breakdown in the functional specificity of brain regions and networks that compromises the fidelity of neural representations supporting episodic memory and related cognitive functions. The evidence for age-related dedifferentiation is robust when it is operationalized as neural selectivity for different categories of perceptual stimuli or as decreased segregation or modularity of resting-state functional brain networks. Neural dedifferentiation for perceptual categories appears to demonstrate a negative, age-invariant relationship with performance on tests of memory and fluid processing. Whether this pattern extends to network-level measures of dedifferentiation cannot currently be determined due to insufficient evidence. The existing data highlight the importance of further examination of neural dedifferentiation as a factor contributing to episodic memory and to cognitive performance more generally.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1016/j.cobeha.2020.01.006DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7039299PMC
April 2020

Age differences in the neural correlates of the specificity of recollection: An event-related potential study.

Neuropsychologia 2020 03 13;140:107394. Epub 2020 Feb 13.

Center for Vital Longevity and School of Behavioral and Brain Sciences, University of Texas at Dallas, Dallas, TX, 75235, USA.

In young adults, the neural correlates of successful recollection vary with the specificity (or amount) of information retrieved. We examined whether the neural correlates of recollection are modulated in a similar fashion in older adults. We compared event-related potential (ERP) correlates of recollection in samples of healthy young and older adults (N = 20 per age group). At study, participants were cued to make one of two judgments about each of a series of words. Subsequently, participants completed a memory test for studied and unstudied words in which they first made a Remember/Know/New (RKN) judgment, followed by a source memory judgment when a word attracted a 'Remember' (R) response. In young adults, the 'left parietal effect' - a putative ERP correlate of successful recollection - was largest for test items endorsed as recollected (R judgment) and attracting a correct source judgment, intermediate for items endorsed as recollected but attracting an incorrect or uncertain source judgment, and, relative to correct rejections, absent for items endorsed as familiar only (K judgment). In marked contrast, the left parietal effect was not detectable in older adults. Rather, regardless of source accuracy, studied items attracting an R response elicited a sustained, centrally maximum negative-going deflection relative to both correct rejections and studied items where recollection failed (K judgment). A similar retrieval-related negativity has been described previously in older adults, but the present findings are among the few to link this effect specifically to recollection. Finally, relative to correct rejections, all classes of correctly recognized old items elicited an age-invariant, late-onsetting positive deflection that was maximal over the right frontal scalp. This finding, which replicates several prior results, suggests that post-retrieval monitoring operations were engaged to an equivalent extent in the two age groups. Together, the present results suggest that there are circumstances where young and older adults engage qualitatively distinct retrieval-related processes during successful recollection.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1016/j.neuropsychologia.2020.107394DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7078048PMC
March 2020

An historical perspective on Endel Tulving's episodic-semantic distinction.

Neuropsychologia 2020 03 30;139:107366. Epub 2020 Jan 30.

School of Psychology, University of East Anglia, Norwich, UK; Center for Vital Longevity and School of Behavioral and Brain Sciences, University of Texas, Dallas, USA.

The distinction between episodic and semantic memory, proposed by Endel Tulving in 1972, remains a key concept in contemporary Cognitive Neuroscience. Here we review how this distinction evolved in Tulving's writings over the years. Crucially, from 1972 onward, he argued that the two forms of memory were inter-dependent and that their interaction was an essential feature of normal episodic memory function. Moreover, later elaborations of the theory clearly proposed that these interactions formed the basis of normal declarative memory functioning. A later but crucial aspect of Tulving's contribution was his stress on the importance of subjective experience, which, according to him, "should be the ultimate object of interest, the central aspect of remembering that is to be explained and understood". We relate these and his numerous other ideas to current perspectives about the organization and function of human memory.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1016/j.neuropsychologia.2020.107366DOI Listing
March 2020

Comparison of fMRI correlates of successful episodic memory encoding in temporal lobe epilepsy patients and healthy controls.

Neuroimage 2020 02 23;207:116397. Epub 2019 Nov 23.

Center for Vital Longevity, University of Texas at Dallas, 1600 Viceroy Dr. #800, Dallas, TX, 75235, USA; School of Behavioral and Brain Sciences, University of Texas at Dallas, 800 W Campbell Rd, Richardson, TX, 75080, USA; Department of Psychiatry, University of Texas Southwestern Medical Center, 6363 Forest Park Rd 7th Floor Suite 749, Dallas, TX, 75235, USA.

Intra-cranial electroencephalographic brain recordings (iEEG) provide a powerful tool for investigating the neural processes supporting episodic memory encoding and form the basis of experimental therapies aimed at improving memory dysfunction. However, given the invasiveness of iEEG, investigations are constrained to patients with drug-resistant epilepsy for whom such recordings are clinically indicated. Particularly in the case of temporal lobe epilepsy (TLE), neuropathology and the possibility of functional reorganization are potential constraints on the generalizability of intra-cerebral findings and pose challenges to the development of therapies for memory disorders stemming from other etiologies. Here, samples of TLE (N ​= ​16; all of whom had undergone iEEG) and age-matched healthy control (N ​= ​19) participants underwent fMRI as they studied lists of concrete nouns. fMRI BOLD responses elicited by the study words were segregated according to subsequent performance on tests of delayed free recall and recognition memory. Subsequent memory effects predictive of both successful recall and recognition memory were evident in several neural regions, most prominently in the left inferior frontal gyrus, and did not demonstrate any group differences. Behaviorally, the groups did not differ in overall recall performance or in the strength of temporal contiguity effects. However, group differences in serial position effects and false alarm rates were evident during the free recall and recognition memory tasks, respectively. Despite these behavioral differences, neuropathology associated with temporal lobe epilepsy was apparently insufficient to give rise to detectable differences in the functional neuroanatomy of episodic memory encoding relative to neurologically healthy controls. The findings provide reassurance that iEEG findings derived from experimental paradigms similar to those employed here generalize to the neurotypical population.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1016/j.neuroimage.2019.116397DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7238288PMC
February 2020

From Knowing to Remembering: The Semantic-Episodic Distinction.

Trends Cogn Sci 2019 12 28;23(12):1041-1057. Epub 2019 Oct 28.

School of Psychology, University of East Anglia, Norwich, UK; Center for Vital Longevity and School of Behavioral and Brain Sciences, University of Texas, Dallas, TX, USA.

The distinction between episodic and semantic memory was first proposed in 1972 by Endel Tulving and is still of central importance in cognitive neuroscience. However, data obtained over the past 30 years or so support the idea that the frontiers between perception and knowledge and between episodic and semantic memory are not as clear cut as previously thought, prompting a rethink of the episodic-semantic distinction. Here, we review recent research on episodic and semantic memory, highlighting similarities between the two systems. Taken together, current behavioral, neuropsychological, and neuroimaging data are compatible with the idea that episodic and semantic memory are inextricably intertwined, yet retain a measure of distinctiveness, despite the fact that their neural correlates demonstrate considerable overlap.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1016/j.tics.2019.09.008DOI Listing
December 2019

Publisher Correction: Maintenance, reserve and compensation: the cognitive neuroscience of healthy ageing.

Nat Rev Neurosci 2018 12;19(12):772

Departments of Psychiatry & Psychology, McGill University and Douglas Hospital Research Centre, Montreal, Quebec, Canada.

In Figure 3b of the originally published article, the colours of the bars were incorrectly reversed. The bars shown in green should have been shown in blue to represent the findings from older adults, whereas the bars shown in blue should have been shown in green to represent the findings from young adults. This has been corrected in the HTML and PDF versions of the article. Images of the original figure are shown in the correction notice.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1038/s41583-018-0087-zDOI Listing
December 2018

Stimulation of the Posterior Cingulate Cortex Impairs Episodic Memory Encoding.

J Neurosci 2019 09 29;39(36):7173-7182. Epub 2019 Jul 29.

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

Neuroimaging experiments implicate the posterior cingulate cortex (PCC) in episodic memory processing, making it a potential target for responsive neuromodulation strategies outside of the hippocampal network. However, causal evidence for the role that PCC plays in memory encoding is lacking. In human female and male participants ( = 17) undergoing seizure mapping, we investigated functional properties of the PCC using deep brain stimulation (DBS) and stereotactic electroencephalography. We used a verbal free recall paradigm in which the PCC was stimulated during presentation of half of the study lists, whereas no stimulation was applied during presentation of the remaining lists. We investigated whether stimulation affected memory and modulated hippocampal activity. Results revealed four main findings. First, stimulation during episodic memory encoding impaired subsequent free recall, predominantly for items presented early in the study lists. Second, PCC stimulation increased hippocampal gamma-band power. Third, stimulation-induced hippocampal gamma power predicted the magnitude of memory impairment. Fourth, functional connectivity between the hippocampus and PCC predicted the strength of the stimulation effect on memory. Our findings offer causal evidence implicating the PCC in episodic memory encoding. Importantly, the results indicate that stimulation targeted outside of the temporal lobe can modulate hippocampal activity and impact behavior. Furthermore, measures of connectivity between brain regions within a functional network can be informative in predicting behavioral effects of stimulation. Our findings have significant implications for developing therapies to treat memory disorders and cognitive impairment using DBS. Cognitive impairment and memory loss are critical public health challenges. Deep brain stimulation (DBS) is a promising tool for developing strategies to ameliorate memory disorders by targeting brain regions involved in mnemonic processing. Using DBS, our study sheds light on the lesser-known role of the posterior cingulate cortex (PCC) in memory encoding. Stimulating the PCC during encoding impairs subsequent recall memory. The degree of impairment is predicted by stimulation-induced hippocampal gamma oscillations and functional connectivity between PCC and hippocampus. Our findings provide the first causal evidence implicating PCC in memory encoding and highlight the PCC as a favorable target for neuromodulation strategies using connectivity measures to predict stimulation effects. This has significant implications for developing therapies for memory diseases.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1523/JNEUROSCI.0698-19.2019DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6733540PMC
September 2019

Age moderates the relationship between cortical thickness and cognitive performance.

Neuropsychologia 2019 09 6;132:107136. Epub 2019 Jul 6.

Center for Vital Longevity and School of Behavioral and Brain Sciences, The University of Texas at Dallas, Dallas, TX, 75235, USA.

Findings from cross-sectional and longitudinal magnetic resonance imaging (MRI) studies indicate that cortical thickness declines across the adult lifespan, with regional differences in rate of decline. Global and regional thickness have also been found to co-vary with cognitive performance. Here we examined the relationships between age, mean cortical thickness, and associative recognition performance across three age groups (younger, middle-aged and older adults; total n = 133). Measures of cortical thickness were obtained using a semi-automated method. Older age was associated with decreased memory performance and a reduction in mean cortical thickness. After controlling for the potentially confounding effects of head motion, mean cortical thickness was negatively associated with associative memory performance in the younger participants, but was positively correlated with performance in older participants. A similar but weaker pattern was evident in the relationships between cortical thickness and scores on four cognitive constructs derived from a neuropsychological test battery. This pattern is consistent with prior findings indicating that the direction of the association between cortical thickness and cognitive performance reverses between early and later adulthood. In addition, head motion was independently and negatively correlated with associative recognition performance in younger and middle-aged, but not older, participants, suggesting that variance in head motion is determined by multiple factors that vary in their relative influences with age.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1016/j.neuropsychologia.2019.107136DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6702041PMC
September 2019

Neural Dedifferentiation in the Aging Brain.

Trends Cogn Sci 2019 07 4;23(7):547-559. Epub 2019 Jun 4.

Center for Vital Longevity, School of Behavioral and Brain Sciences, University of Texas at Dallas, Richardson, TX 75235, USA.

Many cognitive abilities decline with age even in the absence of detectable pathology. Recent evidence indicates that age-related neural dedifferentiation, operationalized in terms of neural selectivity, may contribute to this decline. We review here work exploring the relationship between neural dedifferentiation, cognition, and age. Compelling evidence for age effects on neural selectivity comes from both non-human animal and human research. However, current data suggest that age does not moderate the observed relationships between neural dedifferentiation and cognitive performance. We propose that functionally significant variance in measures of neural dedifferentiation reflects both age-dependent and age-independent factors. We further propose that the effects of age on neural dedifferentiation do not exclusively reflect detrimental consequences of aging.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1016/j.tics.2019.04.012DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6635135PMC
July 2019

Effects of age on across-participant variability of cortical reinstatement effects.

Neuroimage 2019 05 5;191:162-175. Epub 2019 Feb 5.

Center for Vital Longevity and School of Behavioral and Brain Sciences, University of Texas at Dallas, USA.

Using functional magnetic resonance imaging data, we assessed whether across-participant variability of content-selective retrieval-related neural activity differs with age. We addressed this question by employing across-participant multi-voxel pattern analysis (MVPA), predicting that increasing age would be associated with reduced variability of retrieval-related cortical reinstatement across participants. During study, 24 young and 24 older participants viewed objects and concrete words. Test items comprised studied words, names of studied objects, and unstudied words. Participants judged whether the items were recollected, familiar, or new by making 'Remember', 'Know' and 'New' responses, respectively. MVPA was conducted on each region belonging to the 'core recollection network', dorsolateral prefrontal cortex, and a previously identified content-selective voxel set. A leave-one-participant-out classification approach was employed whereby a classifier was trained on a subset of participants and tested on the data from a yoked pair of held-out participants. Classifiers were trained on the study phase data to discriminate the study trials as a function of content (picture or word). The classifiers were then applied to the test phase data to discriminate studied test words according to their study condition. In all of the examined regions, classifier performance demonstrated little or no sensitivity to age and, for the test data, was robustly above chance. Thus, there was little evidence to support the hypothesis that across-participant variability of retrieval-related cortical reinstatement differs with age. The findings extend prior evidence by demonstrating that content-selective cortical reinstatement is sufficiently invariant to support across-participant multi-voxel classification across the healthy adult lifespan.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1016/j.neuroimage.2019.02.005DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6506574PMC
May 2019

Author Correction: Maintenance, reserve and compensation: the cognitive neuroscience of healthy ageing.

Nat Rev Neurosci 2018 Dec;19(12):772

Departments of Psychiatry & Psychology, McGill University and Douglas Hospital Research Centre, Montreal, Quebec, Canada.

In the originally published version of article, there were two errors in the references. The reference "Nilsson, J. & Lövdén, M. Naming is not explaining: future directions for the "cognitive reserve" and "brain maintenance" theories. Alzheimer's Res. Ther. 10, 34 (2018)" was missing. This reference has been added as REF.  in the HTML and PDF versions of the article and cited at the end of the sentence "However, over the years, these terms have been used inconsistently, creating confusion and slowing progress." on page 701 and at the end of the sentence "If reserve is defined merely as the factor that individuals with greater reserve have and then this factor is used to explain why some individuals have greater reserve, the argument is clearly circular." on page 704. The reference list has been renumbered accordingly. In addition, in the original reference list, REF.  was incorrect. The reference should have read "Cabeza, R. Hemispheric asymmetry reduction in older adults. The HAROLD model. Psychol. Aging 17, 85-100 (2002)". This reference, which is REF.  in the corrected reference list, has been corrected in the HTML and PDF versions of the article.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1038/s41583-018-0086-0DOI Listing
December 2018

Gamma oscillations during episodic memory processing provide evidence for functional specialization in the longitudinal axis of the human hippocampus.

Hippocampus 2019 02 5;29(2):68-72. Epub 2018 Nov 5.

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

The question of whether the anterior and posterior hippocampus serve different or complementary functional roles during episodic memory processing has been motivated by noteworthy findings in rodent experiments and from noninvasive studies in humans. Researchers have synthesized these data to postulate several models of functional specialization, However, the issue has not been explored in detail using direct brain recordings. We recently published evidence that theta power increases during episodic memory encoding occur in the posterior hippocampus in humans. In our current investigation we analyzed an expanded data set of 32 epilepsy patients undergoing stereo EEG seizure mapping surgery with electrodes precisely targeted to the anterior and posterior hippocampus simultaneously who performed an episodic memory task. Using a repeated measures design, we looked for an interaction between encoding versus retrieval differences in gamma oscillatory power and anterior versus posterior hippocampal location. Our findings are consistent with a recently articulated model (the HERNET model) favoring posterior hippocampal activation during retrieval related processing. We also tested for encoding versus retrieval differences in the preferred gamma frequency band (high versus low gamma oscillations) motivated by published rodent data.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1002/hipo.23016DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6519081PMC
February 2019

The Relationship between Age, Neural Differentiation, and Memory Performance.

J Neurosci 2019 01 2;39(1):149-162. Epub 2018 Nov 2.

Center for Vital Longevity, University of Texas at Dallas, Dallas, Texas 75235.

Healthy aging is associated with decreased neural selectivity (dedifferentiation) in category-selective cortical regions. This finding has prompted the suggestion that dedifferentiation contributes to age-related cognitive decline. Consistent with this possibility, dedifferentiation has been reported to negatively correlate with fluid intelligence in older adults. Here, we examined whether dedifferentiation is associated with performance in another cognitive domain-episodic memory-that is also highly vulnerable to aging. Given the proposed role of dedifferentiation in age-related cognitive decline, we predicted there would be a stronger link between dedifferentiation and episodic memory performance in older than in younger adults. Young (18-30 years) and older (64-75 years) male and female humans underwent fMRI scanning while viewing images of objects and scenes before a subsequent recognition memory test. We computed a differentiation index in two regions of interest (ROIs): parahippocampal place area (PPA) and lateral occipital complex (LOC). This index quantified the selectivity of the BOLD response to preferred versus nonpreferred category of an ROI (scenes for PPA, objects for LOC). The differentiation index in the PPA, but not the LOC, was lower in older than in younger adults. Additionally, the PPA differentiation index predicted recognition memory performance for the studied items. This relationship was independent of and not moderated by age. The PPA differentiation index also predicted performance on a latent "fluency" factor derived from a neuropsychological test battery; this relationship was also age invariant. These findings suggest that two independent factors, one associated with age, and the other with cognitive performance, influence neural differentiation. Aging is associated with neural dedifferentiation-reduced neural selectivity in "category-selective" cortical brain regions-which has been proposed to contribute to cognitive aging. Here, we examined whether neural differentiation is predictive of episodic memory performance, and whether the relationship is moderated by age. A neural differentiation index was estimated for scene-selective (PPA) and object-selective (LOC) cortical regions while participants studied images for a subsequent memory test. Age-related reductions were observed for the PPA, but not for the LOC, differentiation index. Importantly, the PPA differentiation index demonstrated age-invariant correlations with subsequent memory performance and a fluency factor derived from a neuropsychological battery. Together, these findings suggest that neural differentiation is associated with two independent factors: age and cognitive performance.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1523/JNEUROSCI.1498-18.2018DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6325265PMC
January 2019

Maintenance, reserve and compensation: the cognitive neuroscience of healthy ageing.

Nat Rev Neurosci 2018 11;19(11):701-710

Departments of Psychiatry & Psychology, McGill University and Douglas Hospital Research Centre, Montreal, Quebec, Canada.

Cognitive ageing research examines the cognitive abilities that are preserved and/or those that decline with advanced age. There is great individual variability in cognitive ageing trajectories. Some older adults show little decline in cognitive ability compared with young adults and are thus termed 'optimally ageing'. By contrast, others exhibit substantial cognitive decline and may develop dementia. Human neuroimaging research has led to a number of important advances in our understanding of the neural mechanisms underlying these two outcomes. However, interpreting the age-related changes and differences in brain structure, activation and functional connectivity that this research reveals is an ongoing challenge. Ambiguous terminology is a major source of difficulty in this venture. Three terms in particular - compensation, maintenance and reserve - have been used in a number of different ways, and researchers continue to disagree about the kinds of evidence or patterns of results that are required to interpret findings related to these concepts. As such inconsistencies can impede progress in both theoretical and empirical research, here, we aim to clarify and propose consensual definitions of these terms.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1038/s41583-018-0068-2DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6472256PMC
November 2018

Transcranial magnetic stimulation of the left angular gyrus during encoding does not impair associative memory performance.

Cogn Neurosci 2018 Jul - Oct;9(3-4):127-138. Epub 2018 Jul 5.

a Center for Vital Longevity and School of Behavioral and Brain Sciences, University of Texas at Dallas , Dallas , USA.

The left angular gyrus (AG) is thought to play a critical role in episodic retrieval and has been implicated in the recollection of specific details of prior episodes. Motivated by recent fMRI studies in which it was reported that elevated neural activity in left AG during study is predictive of subsequent associative memory, the present study investigated whether the region plays a causal role in associative memory encoding. Participants underwent online transcranial magnetic stimulation (TMS) while encoding word pairs prior to an associative memory test. We predicted that TMS to left AG during encoding would result in reduced subsequent memory accuracy, especially for estimates of recollection. The results did not support this prediction: estimates of both recollection and familiarity-driven recognition were essentially identical for words pairs encoded during TMS to left AG relative to a vertex control site. These results suggest that the left AG may not play a necessary role in associative memory encoding. TMS to left AG did however affect confidence for incorrect 'intact' judgments to rearranged pairs and incorrect 'rearranged' judgments to intact pairs. These findings suggest that the left AG supports encoding processes that contribute to aspects of subjective mnemonic experience.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1080/17588928.2018.1484723DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6185791PMC
March 2019

Age-related Differences in Prestimulus Subsequent Memory Effects Assessed with Event-related Potentials.

J Cogn Neurosci 2018 06 28;30(6):829-850. Epub 2018 Feb 28.

University of Texas at Dallas.

Prestimulus subsequent memory effects (preSMEs)-differences in neural activity elicited by a task cue at encoding that are predictive of later memory performance-are thought to reflect differential engagement of preparatory processes that benefit episodic memory encoding. We investigated age differences in preSMEs indexed by differences in ERP amplitude just before the onset of a study item. Young and older adults incidentally encoded words for a subsequent memory test. Each study word was preceded by a task cue that signaled a judgment to perform on the word. Words were presented for either a short (300 msec) or long (1000 msec) duration with the aim of placing differential benefits on engaging preparatory processes initiated by the task cue. ERPs associated with subsequent successful and unsuccessful recollection, operationalized here by source memory accuracy, were estimated time-locked to the onset of the task cue. In a late time window (1000-2000 msec after onset of the cue), young adults demonstrated frontally distributed preSMEs for both the short and long study durations, albeit with opposite polarities in the two conditions. This finding suggests that preSMEs in young adults are sensitive to perceived task demands. Although older adults showed no evidence of preSMEs in the same late time window, significant preSMEs were observed in an earlier time window (500-1000 msec) that was invariant with study duration. These results are broadly consistent with the proposal that older adults differ from their younger counterparts in how they engage preparatory processes during memory encoding.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1162/jocn_a_01249DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5932257PMC
June 2018

Recollection-related increases in functional connectivity across the healthy adult lifespan.

Neurobiol Aging 2018 02 6;62:1-19. Epub 2017 Oct 6.

Center for Vital Longevity and School of Behavioral and Brain Sciences, University of Texas at Dallas, Dallas, TX, USA.

In young adults, recollection-sensitive brain regions exhibit enhanced connectivity with a widely distributed set of other regions during successful versus unsuccessful recollection, and the magnitude of connectivity change correlates with individual differences in recollection accuracy. Here, we examined whether recollection-related changes in connectivity and their relationship with performance varied across samples of young, middle-aged, and older adults. Psychophysiological interaction analyses identified recollection-related increases in connectivity both with recollection-sensitive seed regions and among regions distributed throughout the whole brain. The seed-based approach failed to identify age-related differences in recollection-related connectivity change. However, the whole-brain analysis revealed a number of age-related effects. Numerous pairs of regions exhibited a main effect of age on connectivity change, mostly due to decreased change with increasing age. After controlling for recollection accuracy, however, these effects of age were for the most part no longer significant, and those effects that were detected now reflected age-related increases in connectivity change. A subset of pairs of regions also exhibited an age by performance interaction, driven mostly by a weaker relationship between connectivity change and recollection accuracy with increasing age. We conjecture that these effects reflect age-related differences in neuromodulation.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1016/j.neurobiolaging.2017.09.026DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5753578PMC
February 2018

Dissociation between the neural correlates of recollection and familiarity in the striatum and hippocampus: Across-study convergence.

Behav Brain Res 2018 11 10;354:1-7. Epub 2017 Aug 10.

Center for Vital Longevity and School of Behavioral and Brain Sciences, University of Texas, Dallas, USA. Electronic address:

In tests of recognition memory, neural activity in the striatum has consistently been reported to differ according to the study status of the test item. A full understanding of the functional significance of striatal 'retrieval success' effects is impeded by a paucity of evidence concerning whether the effects differ according to the nature of the memory signal supporting the recognition judgment (recollection vs. familiarity). Here, we address this issue through an analysis of retrieval-related striatal activity in three independent fMRI studies (total N = 88). Recollection and familiarity were operationalized in a different way in each study, allowing the identification of test-independent, generic recollection- and familiarity-related effects. While activity in a bilateral dorsal striatal region, mainly encompassing the caudate nucleus, was enhanced equally by recollected and 'familiar only' test items, activity in bilateral ventral striatum and adjacent subgenual frontal cortex was enhanced only in response to items that elicited successful recollection. By contrast, relative to familiar items, activity in anterior hippocampus was enhanced for both recollected and novel test items. Thus, recollection- and familiarity-driven recognition memory judgments are associated with anatomically distinct patterns of retrieval-related striatal activity, and these patterns are at least partially independent of recollection and novelty effects in the hippocampus.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1016/j.bbr.2017.07.031DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5809243PMC
November 2018