Working Memory for Complex Scenes: Age Differences in Frontal and Hippocampal Activations

Park, Denise C.; Welsh, Robert C.; Marshuetz, Christy; Gutchess, Angela H.; Mikels, Joseph A.; Polk, Thad A.; Noll, Douglas C.; Taylor, Stephan F.

doi:10.1162/089892903322598094

Cited by 131 publications

(92 citation statements)

References 37 publications

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“…One recent study found progressively greater impairments across subjects from 30 to 90 years of age (Davis et al, 2003), whereas another reported a steady decrease across multiple measures of memory in healthy adults from age 20 forward (Park et al, 2003). Declines in memory from young adulthood to middle age have also been described previously for rats (Deupree et al, 1993;Granger et al, 1996;Oler and Markus, 1998;Ward et al, 1999;Meneses et al, 2004) and monkeys (Herndon et al, 1997;Sloane et al, 1997), suggesting that this effect could be a general feature of mammalian brain.…”

Section: Introductionmentioning

confidence: 57%

Long-Term Potentiation Is Impaired in Middle-Aged Rats: Regional Specificity and Reversal by Adenosine Receptor Antagonists

Rex¹,

Kramár²,

Colgin³

et al. 2005

J. Neurosci.

126

106

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Memory loss in humans begins early in adult life and progresses thereafter. It is not known whether these losses reflect the failure of cellular processes that encode memory or disturbances in events that retrieve it. Here, we report that impairments in hippocampal long-term potentiation (LTP), a form of synaptic plasticity associated with memory, are present by middle age in rats but only in select portions of pyramidal cell dendritic trees. Specifically, LTP induced with theta-burst stimulation in basal dendrites of hippocampal field CA1 decayed rapidly in slices prepared from 7-to 10-month-old rats but not in slices from young adults. There were no evident age-related differences in LTP in the apical dendrites. Both the adenosine A 1 receptor antagonist 8-cyclopentyl-1,3-dipropylxanthine and a positive AMPA receptor modulator (ampakine) offset age-related LTP deficits. Adenosine produced greater depression of synaptic responses in middle-aged versus young adult slices and in basal versus apical dendrites. These results were not associated with variations in A 1 receptor densities and may instead reflect regional and age-related differences in adenosine clearance. Pertinent to this, brief applications of A 1 receptor antagonists immediately after theta stimulation fully restored LTP in middle-aged rats. We hypothesize that the build-up of extracellular adenosine during theta activity persists into the postinduction period in the basal dendrites of middle-aged slices and thereby activates the A 1 receptor-dependent LTP reversal effect. Regardless of the underlying mechanism, the present results provide a candidate explanation for memory losses during normal aging and indicate that, with regard to plasticity, different segments of pyramidal neurons age at different rates.

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Section: Introductionmentioning

confidence: 57%

Long-Term Potentiation Is Impaired in Middle-Aged Rats: Regional Specificity and Reversal by Adenosine Receptor Antagonists

Rex¹,

Kramár²,

Colgin³

et al. 2005

J. Neurosci.

126

106

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“…Indeed, several studies of patients with HC atrophy have reported scene‐specific deficits for both memory and perceptual tasks [Bird et al, 2008; Hartley et al, 2007; Lee et al, 2005a, 2005b; Mullally et al, 2012; but see Kim et al, 2011, 2015]. Functional neuroimaging studies have likewise found group‐level HC activation during scene discrimination [Aly et al, 2013; Lee et al, 2008], scene construction/imagining [Zeidman et al, 2015], and working memory [Lee and Rudebeck, 2010b; Park et al, 2003]. Studies applying multivariate analysis techniques have also found evidence that the HC contains activation patterns that are sensitive to scene‐related information [Bonnici et al, 2012; Liang et al, 2013; but see Diana et al, 2008].…”

Section: Discussionmentioning

confidence: 99%

“…Beyond the seminal work in both rats and non‐human primates—which identified HC cells attuned to allocentric location [O'Keefe and Nadel, 1978] and spatial view [Rolls, 1999]—recent models of human medial temporal lobe (MTL) function highlight the HC as an important structure for scene processing, via a proposed role in representing complex and conjunctive scene stimuli [Graham et al, 2010; Lee et al, 2012; Murray et al, 2007] and/or by contributions to viewpoint‐independent scene construction [Bird and Burgess, 2008; Maguire and Mullally, 2013; Zeidman et al, 2015]. These complex HC scene representations have been shown to support behavioural performance across a range of cognitive domains, including recognition memory [Bird et al, 2008; Taylor et al, 2007], short‐term memory [Hannula et al, 2006; Hartley et al, 2007], working memory [Lee and Rudebeck, 2010a, 2010b; Park et al, 2003], perceptual learning [Mundy et al, 2013], higher‐order perception [Aly et al, 2013; Barense et al, 2005, 2010; Kolarik et al, 2016; Lee et al, 2005b] and scene imagination [Hassabis et al, 2007]. …”

Section: Introductionmentioning

confidence: 99%

Evidencing a place for the hippocampus within the core scene processing network

Hodgetts

Shine

Lawrence

et al. 2016

Human Brain Mapping

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Functional neuroimaging studies have identified several “core” brain regions that are preferentially activated by scene stimuli, namely posterior parahippocampal gyrus (PHG), retrosplenial cortex (RSC), and transverse occipital sulcus (TOS). The hippocampus (HC), too, is thought to play a key role in scene processing, although no study has yet investigated scene‐sensitivity in the HC relative to these other “core” regions. Here, we characterised the frequency and consistency of individual scene‐preferential responses within these regions by analysing a large dataset (n = 51) in which participants performed a one‐back working memory task for scenes, objects, and scrambled objects. An unbiased approach was adopted by applying independently‐defined anatomical ROIs to individual‐level functional data across different voxel‐wise thresholds and spatial filters. It was found that the majority of subjects had preferential scene clusters in PHG (max = 100% of participants), RSC (max = 76%), and TOS (max = 94%). A comparable number of individuals also possessed significant scene‐related clusters within their individually defined HC ROIs (max = 88%), evidencing a HC contribution to scene processing. While probabilistic overlap maps of individual clusters showed that overlap “peaks” were close to those identified in group‐level analyses (particularly for TOS and HC), inter‐individual consistency varied across regions and statistical thresholds. The inter‐regional and inter‐individual variability revealed by these analyses has implications for how scene‐sensitive cortex is localised and interrogated in functional neuroimaging studies, particularly in medial temporal lobe regions, such as the HC. Hum Brain Mapp 37:3779–3794, 2016. © 2016 Wiley Periodicals, Inc.

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“…Despite the powerful behavioral results demonstrating the centrality of speed for cognition in older adults, it has been difficult to identify the neural analog of decreased speed with age. Up to this point, demyelination and decreases in dopamine receptors have been the primary neural candidates accounting for age-related declines in perceptual speed (5,11), but these accounts fail to explain why simple choice reaction time does not account for as much age-related variance in cognition as perceptual speed does (30). The present findings suggest that perceptual comparison times may be slower in older subjects due to functional dedifferentiation in high-level sensory cortex that results in more time needed to disambiguate similarities between visual stimuli.…”

Section: Discussionmentioning

confidence: 99%

“…For one thing, the functions performed by different areas of prefrontal cortex are poorly understood. It is therefore difficult to interpret the functional significance of bilateral prefrontal activation in elderly subjects (11)(12)(13). Does the additional activation reflect the recruitment of more neural resources that are functionally specialized for the task being performed (which does not imply dedifferentiation of function)?…”

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confidence: 99%

Aging reduces neural specialization in ventral visual cortex

Park

Polk

Park

et al. 2004

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

577

493

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The present study investigated whether neural structures become less functionally differentiated and specialized with age. We studied ventral visual cortex, an area of the brain that responds selectively to visual categories (faces, places, and words) in young adults, and that shows little atrophy with age. Functional MRI was used to estimate neural activity in this cortical area, while young and old adults viewed faces, houses, pseudowords, and chairs. The results demonstrated significantly less neural specialization for these stimulus categories in older adults across a range of analyses. There is growing behavioral evidence that the functional architecture of cognition becomes dedifferentiated with age: A number of studies have found that correlations among distinct measures of cognitive function are more intercorrelated in older subjects than in younger adult subjects (1-5). Furthermore, markers of central sensory function (e.g., corrected visual and auditory acuity) account for virtually all age-related variance on a broad array of higher-order cognitive tasks, including speed of processing, memory, verbal fluency, and reasoning (4, 6). Based on these and related findings, Baltes and Lindenberger (6) argued that aging reduces the degree to which behavior is specialized (or differentiated) for individual tasks and that a domain-independent decline in neural integrity is the mechanism underlying this dedifferentiation. Providing a more specific mechanism for dedifferentiation, Li et al. (7) have argued that both empirical and computational data suggest that increased age results in a decrease in distinctiveness of neural representations due to deficient dopaminergic modulation. With the advent of neuroimaging techniques, the dedifferentiation hypothesis can be addressed more directly than is possible with behavioral techniques alone. Thus, in the present study, we test whether neural structures become dedifferentiated with age, by examining the degree of category-specificity that is present in ventral visual cortex in young and old adults.

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Working Memory for Complex Scenes: Age Differences in Frontal and Hippocampal Activations

Cited by 131 publications

References 37 publications

Long-Term Potentiation Is Impaired in Middle-Aged Rats: Regional Specificity and Reversal by Adenosine Receptor Antagonists

Long-Term Potentiation Is Impaired in Middle-Aged Rats: Regional Specificity and Reversal by Adenosine Receptor Antagonists

Evidencing a place for the hippocampus within the core scene processing network

Aging reduces neural specialization in ventral visual cortex

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