Neural differentiation is moderated by age in scene- but not face-selective cortical regions

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

The relationship between age, neural differentiation, and memory performance

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

Modulation of Oscillatory Power and Connectivity in the Human Posterior Cingulate Cortex Supports the Encoding and Retrieval of Episodic Memories

Existing data from noninvasive studies have led researchers to posit that the posterior cingulate cortex (PCC) supports mnemonic processes: It exhibits degeneration in memory disorders, and fMRI investigations have demonstrated memory-related activation principally during the retrieval of memory items. Despite these data, the role of the PCC in episodic memory has received only limited treatment using the spatial and temporal precision of intracranial EEG, with previous analyses focused on item retrieval. Using data gathered from 21 human participants who underwent stereo-EEG for seizure localization, we characterized oscillatory patterns in the PCC during the encoding and retrieval of episodic memories. We identified a subsequent memory effect during item encoding characterized by increased gamma band oscillatory power and a low-frequency power desynchronization. Fourteen participants had stereotactic electrodes located simultaneously in the hippocampus and PCC, and with these unique data, we describe connectivity changes between these structures that predict successful item encoding and that precede item retrieval. Oscillatory power during retrieval matched the pattern we observed during encoding, with low-frequency (below 15 Hz) desynchronization and a gamma band (especially high gamma, 70–180 Hz) power increase. Encoding is characterized by synchrony between the hippocampus and PCC, centered at 3 Hz, consistent with other observations of properties of this oscillation akin to those for rodent theta activity. We discuss our findings in light of existing theories of episodic memory processing, including the information via desynchronization hypothesis and retrieved context theory, and examine how our data fit with existing theories for the functional role of the PCC. These include a postulated role for the PCC in modulating internally directed attention and for representing or integrating contextual information for memory items

Recollection, Familiarity, and Cortical Reinstatement: A Multivoxel Pattern Analysis

SummaryEpisodic memory retrieval is thought to involve reinstatement of the neurocognitive processes engaged when an episode was encoded. Prior fMRI studies and computational models have suggested that reinstatement is limited to instances in which specific episodic details are recollected. We used multivoxel pattern-classification analyses of fMRI data to investigate how reinstatement is associated with different memory judgments, particularly those accompanied by recollection versus a feeling of familiarity (when recollection is absent). Classifiers were trained to distinguish between brain activity patterns associated with different encoding tasks and were subsequently applied to recognition-related fMRI data to determine the degree to which patterns were reinstated. Reinstatement was evident during both recollection- and familiarity-based judgments, providing clear evidence that reinstatement is not sufficient for eliciting a recollective experience. The findings are interpreted as support for a continuous, recollection-related neural signal that has been central to recent debate over the nature of recognition memory processes

Remembrance of Odors Past Human Olfactory Cortex in Cross-Modal Recognition Memory

AbstractEpisodic memory is often imbued with multisensory richness, such that the recall of an event can be endowed with the sights, sounds, and smells of its prior occurrence. While hippocampus and related medial temporal structures are implicated in episodic memory retrieval, the participation of sensory-specific cortex in representing the qualities of an episode is less well established. We combined functional magnetic resonance imaging (fMRI) with a cross-modal paradigm, where objects were presented with odors during memory encoding. We then examined the effect of odor context on neural responses at retrieval when these same objects were presented alone. Primary olfactory (piriform) cortex, as well as anterior hippocampus, was activated during the successful retrieval of old (compared to new) objects. Our findings indicate that sensory features of the original engram are preserved in unimodal olfactory cortex. We suggest that reactivation of memory traces distributed across modality-specific brain areas underpins the sensory qualities of episodic memories

Effects of age on prestimulus neural activity predictive of successful memory encoding: An fMRI study

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

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

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

Hippocampal theta oscillations support successful associative memory formation

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 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

The retrieval-related anterior shift is moderated by age and correlates with memory performance

Recent research suggests that episodic memory is associated with systematic differences in the localization of neural activity observed during memory encoding and retrieval. The retrieval-related anterior shift is a phenomenon whereby the retrieval of a stimulus event (e.g., a scene image) is associated with a peak neural response which is localized more anteriorly than the response elicited when the stimulus is experienced directly. Here, we examine whether the magnitude of the anterior shift (i.e., the distance between encoding- and retrieval-related response peaks) is moderated by age, and also whether the shift is associated with memory performance. Younger and older human subjects of both sexes underwent fMRI as they completed encoding and retrieval tasks on word-face and word-scene pairs. We localized peak scene and face selectivity for each individual participant within the face-selective precuneus and in three scene-selective (parahippocampal place area [PPA], medial place area, occipital place area) ROIs. In line with recent findings, we identified an anterior shift in the PPA and occipital place area in both age groups and, in older adults only, in the medial place area and precuneus also. Of importance, the magnitude of the anterior shift was larger in older than in younger adults. The shift within the PPA exhibited an age-invariant across-participant negative correlation with source memory performance, such that a smaller displacement between encoding- and retrieval-related neural activity was associated with better performance. These findings provide novel insights into the functional significance of the anterior shift, especially in relation to memory decline in older age

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

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