ABSTRACT NEURAL CORRELATES OF SUCCESSFUL DECLARATIVE MEMORY FORMATION AND RETRIEVAL: THE ANATOMICAL OVERLAP (original) (raw)
Neuroscience Letters, 2003
The present event-related fMRI study examined in ten healthy participants neural correlates of recognition memory for intact, rearranged, and new pairs of visual stimuli. The correct categorization of both intact and rearranged pairs relative to pairs of new, never presented before stimuli relies on the retrieval of associative information whereas the discrimination of rearranged pairs from intact pairs additionally involves a recall-to-reject process by which subjects retrieve additional information to reach a recognition decision. Relative to new pairs, both intact and rearranged pairs yielded activation in inferior prefrontal cortex bilaterally and left dorsolateral prefrontal cortex. Relative to intact pairs, rearranged pairs were associated with increased activity in left dorsolateral prefrontal cortex. The latter could reflect the neural correlates of a recall-to-reject process, a pivotal process of associative recognition memory. q
Brain Activity During the Encoding, Retention, and Retrieval of Stimulus Representations
Learning & Memory, 2001
Studies of delayed nonmatching-to-sample (DNMS) performance following lesions of the monkey cortex have revealed a critical circuit of brain regions involved in forming memories and retaining and retrieving stimulus representations. Using event-related functional magnetic resonance imaging (fMRI), we measured brain activity in 10 healthy human participants during performance of a trial-unique visual DNMS task using novel barcode stimuli. The event-related design enabled the identification of activity during the different phases of the task (encoding, retention, and retrieval). Several brain regions identified by monkey studies as being important for successful DNMS performance showed selective activity during the different phases, including the mediodorsal thalamic nucleus (encoding), ventrolateral prefrontal cortex (retention), and perirhinal cortex (retrieval). Regions showing sustained activity within trials included the ventromedial and dorsal prefrontal cortices and occipital cortex. The present study shows the utility of investigating performance on tasks derived from animal models to assist in the identification of brain regions involved in human recognition memory.
Rapid Sequential Implication of the Human Medial Temporal Lobe in Memory Encoding and Recognition
Frontiers in Behavioral Neuroscience, 2021
The medial temporal lobe (MTL) is crucial for memory encoding and recognition. The time course of these processes is unknown. The present study juxtaposed encoding and recognition in a single paradigm. Twenty healthy subjects performed a continuous recognition task as brain activity was monitored with a high-density electroencephalography. The task presented New pictures thought to evoke encoding. The stimuli were then repeated up to 4 consecutive times to produce over-familiarity. These repeated stimuli served as “baseline” for comparison with the other stimuli. Stimuli later reappeared after 9–15 intervening items, presumably associated with new encoding and recognition. Encoding-related differences in evoked response potential amplitudes and in spatiotemporal analysis were observed at 145–300 ms, whereby source estimation indicated MTL and orbitofrontal activity from 145 to 205 ms. Recognition-related activity evoked by late repetitions occurred at 405–470 ms, implicating the MTL...
Cognitive Brain Research, 2004
Results from behavioral studies have supported the idea that recognition memory can be supported by at least two different processes, recollection and familiarity. However, it remains unclear whether these two forms of memory reflect neurally distinct processes. Furthermore, it is unclear whether recollection and familiarity can be best conceived as differing primarily in terms of retrieval processing, or whether they additionally differ at encoding. To address these issues, we used event-related brain potentials (ERPs) to monitor neural correlates of familiarity and recollection at both encoding and retrieval. Participants studied pictures of objects in two types of study blocks and subsequently made remember -know and source memory judgments during retrieval. Results showed that, during encoding, neural correlates of subsequent familiarity and recollection onsetted in parallel, but exhibited differences in scalp topography and time course. Subsequent familiarity-based recognition was associated with a left-lateralized enhanced positivity and observed at anterior scalp sites from 300 to 450 ms, whereas subsequent recollection was associated with a topographically distinct right-lateralized positivity at anterior scalp sites from 300 to 450 ms and bilateral activity from 450 to 600 ms. During retrieval, neural correlates of familiarity emerged earlier than correlates of recollection. Familiarity was associated with an enhanced positivity at frontopolar scalp sites from 150 to 450 ms, whereas recollection was associated with positive ERP modulations over bilateral frontal (300 -600 ms) and parietal (450 -800 ms) sites. These results demonstrate that familiarity and recollection reflect the outcome of neurally distinct memory processes at both encoding and retrieval. D
An fMRI Study of Episodic Memory: Retrieval of Object, Spatial, and Temporal Information
Behavioral Neuroscience, 2004
Sixteen participants viewed a videotaped tour of 4 houses that highlighted a series of objects and their spatial locations. Participants were tested for memory of object, spatial, and temporal-order information while undergoing functional magnetic resonance imaging. Preferential activation was observed in the right parahippocampal gyrus during the retrieval of spatial-location information. Retrieval of contextual information (spatial location and temporal order) was associated with activation in the right dorsolateral prefrontal cortex. In bilateral posterior parietal regions, greater activation was associated with processing of visual scenes regardless of the memory judgment. These findings support current theories positing roles for frontal and medial temporal regions during episodic retrieval and suggest a specific role for the hippocampal complex in the retrieval of spatial-location information.
Neural activity that predicts subsequent memory and forgetting: A meta-analysis of 74 fMRI studies
NeuroImage, 2011
The present study performed a quantitative meta-analysis of functional MRI studies that used a subsequent memory approach. The meta-analysis considered both subsequent memory (SM; remembered N forgotten) and subsequent forgetting (SF; forgotten N remembered) effects, restricting the data used to that concerning visual information encoding in healthy young adults. The meta-analysis of SM effects indicated that they most consistently associated with five neural regions: left inferior frontal cortex (IFC), bilateral fusiform cortex, bilateral hippocampal formation, bilateral premotor cortex (PMC), and bilateral posterior parietal cortex (PPC). Direct comparisons of the SM effects between the studies using verbal versus pictorial material and item-memory versus associative-memory tasks yielded three main sets of findings. First, the left IFC exhibited greater SM effects during verbal material than pictorial material encoding, whereas the fusiform cortex exhibited greater SM effects during pictorial material rather than verbal material encoding. Second, bilateral hippocampal regions showed greater SM effects during pictorial material encoding compared to verbal material encoding. Furthermore, the left hippocampal region showed greater SM effects during pictorialassociative versus pictorial-item encoding. Third, bilateral PMC and PPC regions, which may support attention during encoding, exhibited greater SM effects during item encoding than during associative encoding. The meta-analysis of SF effects indicated they associated mostly with default-mode network regions, including the anterior and posterior midline cortex, the bilateral temporoparietal junction, and the bilateral superior frontal cortex. Recurrent activity oscillations between the task-positive and task-negative/default-mode networks may account for trial-to-trial variability in participants' encoding performances, which is a fundamental source of both SM and SF effects. Taken together, these findings clarify the neural activity that supports successful encoding, as well as the neural activity that leads to encoding failure.
Imaging distributed and massed repetitions of natural scenes: Spontaneous retrieval and maintenance
Human Brain Mapping, 2014
Repetitions that are distributed (spaced) across time prompt enhancement of a memory-related event-related potential, compared to when repetitions are massed (contiguous). Here, we used fMRI to investigate neural enhancement and suppression effects during free viewing of natural scenes that were either novel or repeated four times with massed or distributed repetitions. Distributed repetition was uniquely associated with a repetition enhancement effect in a bilateral posterior parietal cluster that included the precuneus and posterior cingulate and which has previously been implicated in episodic memory retrieval. Unique to massed repetition, conversely, was enhancement in a right dorsolateral prefrontal cluster that has been implicated in short-term maintenance. Repetition suppression effects for both types of spacing were widespread in regions activated during novel picture processing. Taken together, the data are consistent with a hypothesis that distributed repetition prompts spontaneous retrieval of prior occurrences, whereas massed repetition prompts short-term maintenance of the episodic representation, due to contiguous presentation. These processing differences may mediate the classic spacing effect in learning and memory.
Frontiers in Behavioral Neuroscience, 2015
In functional magnetic resonance imaging (fMRI) studies that apply a "subsequent memory" approach, successful encoding is indicated by increased fMRI activity during the encoding phase for hits vs. misses, in areas underlying memory encoding such as the hippocampal formation. Signal-detection theory (SDT) can be used to analyze memoryrelated fMRI activity as a function of the participant's memory trace strength (d). The goal of the present study was to use SDT to examine the relationship between fMRI activity during incidental encoding and participants' recognition performance. To implement a new approach, post-experimental group assignment into High-or Low Performers (HP or LP) was based on 29 healthy participants' recognition performance, assessed with SDT. The analyses focused on the interaction between the factors group (HP vs. LP) and recognition performance (hits vs. misses). A whole-brain analysis revealed increased activation for HP vs. LP during incidental encoding for remembered vs. forgotten items (hits > misses) in the insula/temporo-parietal junction (TPJ) and the fusiform gyrus (FFG). Parameter estimates in these regions exhibited a significant positive correlation with d. As these brain regions are highly relevant for salience detection (insula), stimulus-driven attention (TPJ), and content-specific processing of mnemonic stimuli (FFG), we suggest that HPs' elevated memory performance was associated with enhanced attentional and content-specific sensory processing during the encoding phase. We provide first correlative evidence that encoding-related activity in content-specific sensory areas and content-independent attention and salience detection areas influences memory performance in a task with incidental encoding of facial stimuli. Based on our findings, we discuss whether the aforementioned group differences in brain activity during incidental encoding might constitute the basis of general differences in memory performance between HP and LP.
Brain, 1998
Functional neuroimaging studies of episodic recognition memory consistently demonstrate retrieval-associated activation in right prefrontal regions, including the right anterior and right dorsolateral prefrontal cortices. In theory, these activations could reflect processes associated with retrieval success, retrieval effort or retrieval attempt; each of these hypotheses has some support from previous studies. In Experiment 1, we examined these functional interpretations using functional MRI to measure prefrontal activation across multiple levels of recognition performance. Results revealed similar patterns of right prefrontal activation across varying levels of retrieval success and retrieval effort, suggesting that these activations reflect retrieval attempt. Retrieval attempt may include initiation of retrieval search or evaluation of the products of retrieval, such as scrutiny of specific attributes of the test item in an effort to determine whether it was encountered previously. In Experiment 2, we examined whether engagement of retrieval attempt is Abbreviations: AC ϭ anterior commissure; ANOVA ϭ analysis of variance; APC ϭ anterior prefrontal cortex; BA ϭ Brodmann area; DLPC ϭ dorsolateral prefrontal cortex; ERP ϭ event-related potential; fMRI ϭ functional MRI; rCBF ϭ regional cerebral blood flow
Neuropsychologia, 1999
In the present PET study we explore some functional aspects of the interaction between attentional:control processes and learning:memory processes[ The network of brain regions supporting recall of abstract designs were studied in a less practiced and in a well practiced state[ The results indicate that automaticity\ i[e[\ a decreased dependence on attentional and working memory resources\ develops as a consequence of practice[ This corresponds to the practice related decreases of activity in the prefrontal\ anterior cingulate\ and posterior parietal regions[ In addition\ the activity of the medial temporal regions decreased as a function of practice[ This indicates an inverse relation between the strength of encoding and the activation of the MTL during retrieval[ Furthermore\ the pattern of practice related increases in the auditory\ posterior insular!opercular extending into perisylvian supra! marginal region\ and the right mid occipito!temporal region\ may re~ect a lower degree of inhibitory attentional modulation of task irrelevant processing and more fully developed representations of the abstract designs\ respectively[ We also suggest that free recall is dependent on bilateral prefrontal processing\ in particular non!automatic free recall[ The present results con_rm previous functional neuroimaging studies of memory retrieval indicating that recall is subserved by a network of interacting brain regions[ Furthermore\ the results indicate that some components of the neural network subserving free recall may have a dynamic role and that there is a functional restructuring of the information processing networks during the learning process[ Þ 0888 Elsevier Science Ltd[ All rights reserved[ Keywords] PET^Memory^Learning^Practice related changes^Medial temporal lobe^Prefrontal cortex Corresponding author[ Tel[] ¦35!7!406 619 28^fax] ¦35!7!23 30 35^e!mail] karlmpÝneuro[ks[se
Separating the brain regions involved in recollection and familiarity in recognition memory
The Journal of neuroscience : the official journal of the Society for Neuroscience, 2005
The neural substrates of recognition memory retrieval were examined in a functional magnetic resonance imaging study designed to separate activity related to recollection from that related to continuous variations in familiarity. Across a variety of brain regions, the neural signature of recollection was found to be distinct from familiarity, demonstrating that recollection cannot be attributed to familiarity strength. In the prefrontal cortex, an anterior medial region was related to recollection, but lateral regions, including the anterior and dorsolateral prefrontal cortex, were related to familiarity. Along the lateral parietal cortex, two functionally distinct regions were also observed: a lateral parietal/temporal region related to recollection and a more superior parietal region involved in familiarity. Similarly, in medial parietal regions, the posterior cingulate was related to recollection, whereas the precuneus was related to familiarity. The hippocampus was related to re...
Behavioral and Brain Functions, 2007
Background: Many human neuroimaging investigations on recognition memory employ verbal instructions to direct subject's attention to a stimulus attribute. But do the same or a similar neurophysiological process occur during nonverbal experiences, such as those involving contingency-shaped responses? Establishing the spatially distributed neural network underlying recognition memory for instructed stimuli and operant, contingency-shaped (i.e., discriminative) stimuli would extend the generality of contemporary domain-general views of recognition memory and clarify the involvement of declarative memory processes in human operant behavior.
Human Brain Mapping, 2007
Since the brain may engage different neuronal systems for a single behavioral goal, activation may show intersubject variability expressed in the systematic recruitment of multiple distinct networks. We apply a principal component analysis (PCA) to activation over task conditions and subjects to reveal cortical networks that may underlie this intersubject variability. Normal subjects were presented with novel meaningless objects, which appeared in personally familiar or unfamiliar places. During a subsequent, event-related functional MRI (fMRI) experiment, each subject was presented with learned or novel objects in isolation and performed a learned/novel judgment. Recollection of places was not essential for the task, and may exhibit large intersubject variations. The right posterodorsal posterior cingulate cortex (pPCC) and left retrosplenial cortex, whose involvement in placerecognition has been previously established, were selected as regions of interest for the PCA. Neural responses to objects associated with familiar relative to unfamiliar places in pPCC, but not in the retrosplenial cortex, were negatively correlated with task-related activation (common over all objects) in the right anterolateral prefrontal cortex and the left intraparietal sulcus. The latter areas have been implicated previously in cognitive control and object recognition, respectively. These results suggest right prefrontal control over neural processes both in the left parietal cortex, related to object-recognition (enhancement), and pPCC, related to nonessential recollection of place-memory (suppression), but not in the retrosplenial cortex, related to the sense of familiarity. This analysis revealed an important aspect of functional anatomy that was not detectable using a conventional analysis of average activations. Hum Brain Mapp 28: 49-58, 2007.
The neural correlates of everyday recognition memory
Brain and Cognition, 2011
We used a novel automatic camera, SenseCam, to create a recognition memory test for real-life events. Adapting a 'Remember/Know' paradigm, we asked healthy undergraduates, who wore SenseCam for two days, in their everyday environments, to classify images as strongly or weakly remembered, strongly or weakly familiar or novel, while brain activation was recorded with functional MRI. Overlapping, widely distributed sets of brain regions were activated by recollected and familiar stimuli. Within the medial temporal lobes, 'Remember' responses specifically elicited greater activity in the right anterior and posterior parahippocampal gyrus than 'Know' responses. 'New' responses activated anterior parahippocampal regions. A parametric analysis, across correctly recognised items, revealed increasing activation in the right hippocampus and posterior parahippocampal gyrus (pPHG). This may reflect modulation of these regions by the degree of recollection or, alternatively, by increasing memory strength. Strong recollection elicited greater activity in the left posterior hippocampus/pPHG than weak recollection indicating that this region is specifically modulated by the degree of recollection.
Interleaving brain systems for episodic and recognition memory
Trends in Cognitive Sciences, 2006
Conflicting models persist over the nature of long-term memory. Crucial issues are whether episodic memory and recognition memory reflect the same underlying processes, and the extent to which various brain structures work as a single unit to support these processes. New findings that have resulted from improved resolution of functional brain imaging, together with recent studies of amnesia and developments in animal testing, reinforce the view that recognition memory comprises at least two independent processes: one recollective and the other using familiarity detection. Only recollective recognition appears to depend on episodic memory. Attempts to map brain areas supporting these two putative components of recognition memory indicate that they depend on separate, but interlinked, structures.