Deep Encoding Research Articles

The relationship between level of processing and hippocampal–cortical functional connectivity during episodic memory formation in humans

New episodic memory traces represent a record of the ongoing neocortical processing engaged during memory formation (encoding). Thus, during encoding, deep (semantic) processing typically establishes more distinctive and retrievable memory traces than does shallow (perceptual) processing, as assessed by later episodic memory tests. By contrast, the hippocampus appears to play a processing-independent role in encoding, because hippocampal lesions impair encoding regardless of level of processing. Here, we clarified the neural relationship between processing and encoding by examining hippocampal-cortical connectivity during deep and shallow encoding. Participants studied words during functional magnetic resonance imaging and freely recalled these words after distraction. Deep study processing led to better recall than shallow study processing. For both levels of processing, successful encoding elicited activations of bilateral hippocampus and left prefrontal cortex, and increased functional connectivity between left hippocampus and bilateral medial prefrontal, cingulate and extrastriate cortices. Successful encoding during deep processing was additionally associated with increased functional connectivity between left hippocampus and bilateral ventrolateral prefrontal cortex and right temporoparietal junction. In the shallow encoding condition, on the other hand, pronounced functional connectivity increases were observed between the right hippocampus and the frontoparietal attention network activated during shallow study processing. Our results further specify how the hippocampus coordinates recording of ongoing neocortical activity into long-term memory, and begin to provide a neural explanation for the typical advantage of deep over shallow study processing for later episodic memory.

Reply to Rousselet et al.: A robust relationship between fiber density and memory recall

Using Pearson's correlation, we reported that fiber density between activated ventrolateral prefrontal cortex (VLPFC) and perirhinal cortex (PRC) and entorhinal cortex (ERC) correlated with memory recalled after deep and shallow encoding (1). Rousselet and Pernet (2) correctly point out that Pearson's correlation is susceptible to outliers. To circumvent this problem we used a random split half and showed that our main correlations were significant in both resulting subcohorts. Other statistical techniques for outlier detection confirm this robustness. Cook's distance estimates the influence that a single data point has on the result of a correlation or regression (3). With the conservative cutoff criterion of 4/N (4), Cook's distance showed no outliers in the deep study condition and one to three outliers in the shallow condition (which also showed weaker correlations in our original article). Without these outliers, all correlations remained significant (VLPFC–ERC shallow: r = 0.4255, P = 0.026; all other r > 0.627; all other P 0.532; all P < 0.0035).

The effect of semantic orientation at encoding on free-recall performance in amnestic mild cognitive impairment and probable Alzheimer's disease

The present study manipulated the nature of orientation provided at encoding in an intentional word memory task. Performance on the memory task was then compared between 23 elderly persons with amnestic mild cognitive impairment (aMCI), 13 patients with probable Alzheimer's disease (AD), and 23 healthy elderly persons. When tested following shallow (reading orientation) encoding, free-recall performance was impaired in AD compared to aMCI and healthy older adults. When tested following deep (categorical semantic orientation) encoding, both AD and aMCI groups were impaired relative to healthy older adults. The latter result was related to larger memory improvement due to semantic orientation in healthy controls than in aMCI and AD participants. Overall, these findings indicate that the encoding put up by aMCI and healthy elderly persons is comparably efficient in situations where shallow supportive cues are provided at encoding, but that healthy controls benefit more than aMCI and AD in situations where supportive cues are strong.

Level of Processing Modulates the Neural Correlates of Emotional Memory Formation

Emotion is known to influence multiple aspects of memory formation, including the initial encoding of the memory trace and its consolidation over time. However, the neural mechanisms whereby emotion impacts memory encoding remain largely unexplored. The present study used a levels-of-processing manipulation to characterize the impact of emotion on encoding with and without the influence of elaborative processes. Participants viewed emotionally negative, neutral, and positive scenes under two conditions: a shallow condition focused on the perceptual features of the scenes and a deep condition that queried their semantic meaning. Recognition memory was tested 2 days later. Results showed that emotional memory enhancements were greatest in the shallow condition. fMRI analyses revealed that the right amygdala predicted subsequent emotional memory in the shallow more than deep condition, whereas the right ventrolateral PFC demonstrated the reverse pattern. Furthermore, the association of these regions with the hippocampus was modulated by valence: the amygdala-hippocampal link was strongest for negative stimuli, whereas the prefrontal-hippocampal link was strongest for positive stimuli. Taken together, these results suggest two distinct activation patterns underlying emotional memory formation: an amygdala component that promotes memory during shallow encoding, especially for negative information, and a prefrontal component that provides extra benefits during deep encoding, especially for positive information.

Processing Speed and Working Memory Span: Their Differential Role in Superficial and Deep Memory Processes in Schizophrenia

Previous work has suggested that decrement in both processing speed and working memory span plays a role in the memory impairment observed in patients with schizophrenia. We undertook a study to examine simultaneously the effect of these two factors. A sample of 49 patients with schizophrenia and 43 healthy controls underwent a battery of verbal and visual memory tasks. Superficial and deep encoding memory measures were tallied. We conducted regression analyses on the various memory measures, using processing speed and working memory span as independent variables. In the patient group, processing speed was a significant predictor of superficial and deep memory measures in verbal and visual memory. Working memory span was an additional significant predictor of the deep memory measures only. Regression analyses involving all participants revealed that the effect of diagnosis on all the deep encoding memory measures was reduced to non-significance when processing speed was entered in the regression. Decreased processing speed is involved in verbal and visual memory deficit in patients, whether the task require superficial or deep encoding. Working memory is involved only insofar as the task requires a certain amount of effort.

Knowing You Beyond Race: The Importance of Individual Feature Encoding in the Other-Race Effect

Knowing You Beyond Race: The Importance of Individual Feature Encoding in the Other-Race Effect

Double dissociation between familiarity and recollection in Parkinson's disease as a function of encoding tasks

Parkinson's disease (PD) is associated with episodic memory deficits, but their exact nature is unclear. Some dual-process studies have suggested that recollection is impaired and familiarity is spared in PD, yet others have found the opposite. Our goal was to investigate these memory processes in PD and determine whether the inconsistency among existing findings is related to differences in encoding conditions. We used a process-dissociation procedure with word pairs to estimate familiarity and recollection. In Experiment 1, we used a directed, deep, relational encoding condition (i.e., sentence generation), and in Experiment 2, we contrasted this encoding condition with a shallower, non-directed encoding condition (i.e., read condition). We found a double dissociation as a function of the encoding task: In the sentence generation encoding condition, recollection was impaired in the PD patients, but familiarity was spared. In contrast, in the read encoding condition, there was no group difference in recollection, but familiarity was impaired in the PD group. Within-subject comparisons revealed that both control and PD participants benefitted from the provision of a directed, deep relational encoding strategy. However, this benefit was manifested as an increase in recollection in the controls, but an increase in familiarity in the PD patients. These findings help to reconcile the extant literature and suggest that episodic memory deficits in PD are two-fold, involving: (1) difficulties instantiating encoding strategies independently, leading to deficits in familiarity, and (2) impaired recollection when encoding strategies are equated across groups. Our results highlight the importance of controlling encoding conditions between groups and of taking account of other variables that may influence the participants’ performance, such as deficits associated with normal aging, which may mask deficits in neurodegenerative diseases in particular situations. More generally, our study raises the possibility that deficits in recollection or familiarity in patient populations are not immutably linked to the structure that is affected, as is typically assumed, but that such deficits may interact with type of encoding, and possibly with the nature of the retrieval process.

Conceptual and non-conceptual repetition priming in category exemplar generation: Evidence from bilinguals

One measure of conceptual implicit memory is repetition priming in the generation of exemplars from a semantic category, but does such priming transfer across languages? That is, do the overlapping conceptual representations for translation equivalents provide a sufficient basis for such priming? In Experiment 1 (N=96) participants carried out a deep encoding task, and priming between languages was statistically reliable, but attenuated, relative to within-language priming. Experiment 2 (N=96) replicated the findings of Experiment 1 and assessed the contributions of conceptual and non-conceptual processes using a levels-of-processing manipulation. Words that underwent shallow encoding exhibited within-language, but not between-language, priming. Priming in shallow conditions cannot therefore be explained by incidental activation of the concept. Instead, part of the within-language priming effect, even under deep-encoding conditions, is due to increased availability of language-specific lemmas or phonological word forms.

Event-related rTMS at encoding affects differently deep and shallow memory traces

The “level of processing” effect is a classical finding of the experimental psychology of memory. Actually, the depth of information processing at encoding predicts the accuracy of the subsequent episodic memory performance. When the incoming stimuli are analyzed in terms of their meaning (semantic, or deep, encoding), the memory performance is superior with respect to the case in which the same stimuli are analyzed in terms of their perceptual features (shallow encoding).As suggested by previous neuroimaging studies and by some preliminary findings with transcranial magnetic stimulation (TMS), the left prefrontal cortex may play a role in semantic processing requiring the allocation of working memory resources. However, it still remains unclear whether deep and shallow encoding share or not the same cortical networks, as well as how these networks contribute to the “level of processing” effect.To investigate the brain areas casually involved in this phenomenon, we applied event-related repetitive TMS (rTMS) during deep (semantic) and shallow (perceptual) encoding of words. Retrieval was subsequently tested without rTMS interference. RTMS applied to the left dorsolateral prefrontal cortex (DLPFC) abolished the beneficial effect of deep encoding on memory performance, both in terms of accuracy (decrease) and reaction times (increase). Neither accuracy nor reaction times were instead affected by rTMS to the right DLPFC or to an additional control site excluded by the memory process (vertex). The fact that online measures of semantic processing at encoding were unaffected suggests that the detrimental effect on memory performance for semantically encoded items took place in the subsequent consolidation phase. These results highlight the specific causal role of the left DLPFC among the wide left-lateralized cortical network engaged by long-term memory, suggesting that it probably represents a crucial node responsible for the improved memory performance induced by semantic processing.

Can corrective feedback improve recognition memory?

An understanding of the effects of corrective feedback on recognition memory can inform both recognition theory and memory training programs, but few published studies have investigated the issue. Although the evidence to date suggests that feedback does not improve recognition accuracy, few studies have directly examined its effect on sensitivity, and fewer have created conditions that facilitate a feedback advantage by encouraging controlled processing at test. In Experiment 1, null effects of feedback were observed following both deep and shallow encoding of categorized study lists. In Experiment 2, feedback robustly influenced response bias by allowing participants to discern highly uneven base rates of old and new items, but sensitivity remained unaffected. In Experiment 3, a false-memory procedure, feedback failed to attenuate false recognition of critical lures. In Experiment 4, participants were unable to use feedback to learn a simple category rule separating old items from new items, despite the fact that feedback was of substantial benefit in a nearly identical categorization task. The recognition system, despite a documented ability to utilize controlled strategic or inferential decision-making processes, appears largely impenetrable to a benefit of corrective feedback.

Motivational priming and processing interrupt: Startle reflex modulation during shallow and deep processing of emotional words

Valence-driven modulation of the startle reflex, that is larger eyeblinks during viewing of unpleasant pictures and inhibited blinks while viewing pleasant pictures, is well documented. The current study investigated, whether this motivational priming pattern also occurs during processing of unpleasant and pleasant words, and to what extent it is influenced by shallow vs. deep encoding of verbal stimuli. Emotional and neutral adjectives were presented for 5 s, and the acoustically elicited startle eyeblink response was measured while subjects memorized the words by means of shallow or deep processing strategies. Results showed blink potentiation to unpleasant and blink inhibition to pleasant adjectives in subjects using shallow encoding strategies. In subjects using deep-encoding strategies, blinks were larger for pleasant than unpleasant or neutral adjectives. In line with this, free recall of pleasant words was also better in subjects who engaged in deep processing. The results suggest that motivational priming holds as long as processing is perceptual. However, during deep processing the startle reflex appears to represent a measure of “processing interrupt”, facilitating blinks to those stimuli that are more deeply encoded.

Investigating the attentional demands of recognition memory: Manipulating depth of encoding at study and level of attention at test

Two experiments investigated the effects of divided attention at test after manipulating levels of processing at study. In Experiment 1 items were studied either intact or as anagrams. In Experiment 2 items were studied with either full or divided attention (DA). In both experiments participants carried out a recognition test with either full or divided attention. Analysis of remember and know responses revealed that DA at test had no effect on remember responses to anagrams or to items studied with full attention. In contrast, Know responses decreased with DA at test, and this occurred for items studied in both deep and shallow encoding conditions. The present study confirms recent findings (Knott & Dewhurst, 2007a) that knowing can rely on more controlled retrieval processes, whereas remembering can rely on more automatic retrieval processes. Differences in the controlled processes associated with recollection and familiarity and remember and know responses are discussed.

The effect of age on word-stem cued recall: A behavioral and electrophysiological study

The present study investigated the effects of aging on behavioral cued-recall performance and on the neural correlates of explicit memory using event-related potentials (ERPs) under shallow and deep encoding conditions. At test, participants were required to complete old and new three-letter word stems using the letters as retrieval cues. The main results were as follows: (1) older participants exhibited the same level of explicit memory as young adults with the same high level of education. Moreover older adults benefited as much as young ones from deep processing at encoding; (2) brain activity at frontal sites showed that the shallow old/new effect developed and ended earlier for older than young adults. In contrast, the deep old/new effect started later for older than for young adults and was sustained up to 1000 ms in both age groups. Moreover, the results suggest that the frontal old/new effect was bilateral but greater over the right than the left electrode sites from 600 ms onward; (3) there were no differences at parietal sites between age groups: the old/new effect developed from 400 ms under both encoding conditions and was sustained up to 1000 ms under the deep condition but ended earlier (800 ms) under the shallow condition. These ERP results indicate significant age-related changes in brain activity associated with the voluntary retrieval of previously encoded information, in spite of similar behavioral performance of young and older adults.

Depression, Avolition, and Attention Disorders in Patients with Schizophrenia: Associations with Verbal Memory Efficiency

Depression, Avolition, and Attention Disorders in Patients with Schizophrenia: Associations with Verbal Memory Efficiency

Increased activation of the left hippocampus region in Complex PTSD during encoding and recognition of emotional words: A pilot study

To gain insight into memory disturbances in Complex Posttraumatic Stress Disorder (Complex PTSD), we investigated declarative memory function and medial temporal lobe activity in patients and healthy non-traumatized controls. A case-control study was performed in nine patients with Complex PTSD and nine controls. All respondents performed a declarative memory task with neutral and emotional, negative words during functional magnetic resonance imaging. Memory performance of neutral words was impaired in Complex PTSD with a relative conservation of recall of negative words. Deep encoding of later remembered negative words, as well as correct recognition of negative words and false alarms, was associated with an enhanced Blood Oxygenation Level Dependent (BOLD) response in the left hippocampus extending into the parahippocampal gyrus of Complex PTSD patients compared with controls. Post-hoc volumetric comparisons did not reveal significant anatomical differences in the medial temporal lobe between Complex PTSD patients and controls. We conclude that in Complex PTSD preferential recall of negative words is associated with increased activation in the left hippocampus and parahippocampal gyrus during both successful and false recall. These findings support a model of an abnormally functioning hippocampus in Complex PTSD.

Autobiographical elaboration reduces memory distortion: Cognitive operations and the distinctiveness heuristic.

Retrieval monitoring enhances episodic memory accuracy. For instance, false recognition is reduced when participants base their decisions on more distinctive recollections, a retrieval monitoring process called the distinctiveness heuristic. The experiments reported here tested the hypothesis that autobiographical elaboration during study (i.e., generating autobiographical memories in response to cue words) would lead to more distinctive recollections than other item-specific encoding tasks, enhancing retrieval monitoring accuracy at test. Consistent with this hypothesis, false recognition was less likely when participants had to search their memory for previous autobiographical elaborations, compared to previous semantic judgments. These false recognition effects were dissociated from true recognition effects across four experiments, implicating a recollection-based monitoring process that was independent from familiarity-based processes. Separately obtained subjective measures provided converging evidence for this conclusion. The cognitive operations engaged during autobiographical elaboration can lead to distinctive recollections, making them less prone to memory distortion than other types of deep or semantic encoding.

Orienting, emotion, and memory: Phasic and tonic variation in heart rate predicts memory for emotional pictures in men

Arousal-related processes associated with heightened heart rate (HR) predict memory enhancement, especially for emotionally arousing stimuli. In addition, phasic HR deceleration reflects “orienting” and sensory receptivity during perception of stimuli. We hypothesized that both tonic elevations in HR as well as phasic HR deceleration during viewing of pictures would be associated with deeper encoding and better subsequent memory for stimuli. Emotional pictures are more memorable and cause greater HR deceleration than neutral pictures. Thus, we predicted that the relations between cardiac activity and memory enhancement would be most pronounced for emotionally-laden compared to neutral pictures. We measured HR in 53 males during viewing of unpleasant, neutral, and pleasant pictures, and tested memory for the pictures two days later. Phasic HR deceleration during viewing of individual pictures was greater for subsequently remembered than forgotten pictures across all three emotion categories. Elevated mean HR across the entire encoding epoch also predicted better memory performance, but only for emotionally arousing pictures. Elevated mean HR and phasic HR deceleration were associated, such that individuals with greater tonic HR also showed greater HR decelerations during picture viewing, but only for emotionally arousing pictures. Results suggest that tonic elevations in HR are associated both with greater orienting and heightened memory for emotionally arousing stimuli.

Low-dose Propofol–induced Amnesia Is Not due to a Failure of Encoding

Propofol may produce amnesia by affecting encoding. The hypothesis that propofol weakens encoding was tested by measuring regional cerebral blood flow during verbal encoding. Seventeen volunteer participants (12 men; aged 30.4 +/- 6.5 yr) had regional cerebral blood flow measured using H2O positron emission tomography during complex and simple encoding tasks (deep vs. shallow level of processing) to identify a region of interest in the left inferior prefrontal cortex (LIPFC). The effect of either propofol (n = 6, 0.9 microg/ml target concentration), placebo with a divided attention task (n = 5), or thiopental at sedative doses (n = 6, 3 microg/ml) on regional cerebral blood flow activation in the LIPFC was tested. The divided attention task was expected to decrease activation in the LIPFC. Propofol did not impair encoding performance or reaction times, but impaired recognition memory of deeply encoded words 4 h later (median recognition of 35% [interquartile range, 17-54%] of words presented during propofol vs. 65% [38-91%] before drug; P < 0.05). Statistical parametric mapping analysis identified a region of interest of 6.6 cm in the LIPFC (T = 7.44, P = 0.014). Regional cerebral blood flow response to deep encoding was present in this region of interest in each group before drug (T > 4.41, P < 0.04). During drug infusion, only the propofol group continued to have borderline significant activation in this region (T = 4.00, P = 0.063). If the amnesic effect of propofol were solely due to effects on encoding, activation in the LIPFC should be minimal. Because LIPFC activation was not totally eliminated by propofol, the amnesic action of propofol must be present in other brain regions and/or affect other memory processes.

Neural correlates of incidental memory in mild cognitive impairment: An fMRI study

Behaviour and fMRI brain activation patterns were compared during encoding and recognition tasks in mild cognitive impairment (MCI) ( n = 14) and normal controls (NC) ( n = 14). Deep (natural vs. man-made) and shallow (color vs. black and white) decisions were made at encoding and pictures from each condition were presented for yes/no recognition 20 min later. MCI showed less inferior frontal activation during deep (left only) and superficial encoding (bilaterally) and in both medial temporal lobes (MTL). When performance was equivalent (recognition of words encoded superficially), MTL activation was similar for the two groups, but during recognition testing of deeply encoded items NC showed more activation in both prefrontal and left MTL region. In a region of interest analysis, the extent of activation during deep encoding in the parahippocampi bilaterally and in left hippocampus correlated with subsequent recognition accuracy for those items in controls but not in MCI, which may reflect the heterogeneity of activation responses in conjunction with different degrees of pathology burden and progression status in the MCI group.

Dissociating measures of associative memory: Evidence and theoretical implications

In four experiments, the authors investigated whether two measures of associative recognition memory (associative identification and associative reinstatement) are dissociable from one-another on the basis of their reliance on strategic retrieval and are dissociable from item recognition memory. Experiment 1 showed that deep encoding of relational information, but not of individual items, increased both types of associative memory significantly, as indexed by both measures, while it only marginally increased item memory. Experiments 2–4 showed that a short response deadline, a speeded recognition and an overlapping pairing condition interfered with associative identification, but left associative reinstatement unaffected. Associative reinstatement provides a measure of associative memory, but unlike associative identification, it is less reliant on strategic retrieval processes. We propose that associative familiarity underlies this measure. This process may index binding of information at encoding without involving the vivid, conscious re-experiencing characteristic of recollection at retrieval.