Human aging reduces the neurobehavioral influence of motivation on episodic memory

The neural circuitry mediating the influence of motivation on long-term declarative or episodic memory formation is delineated in young adults, but its status is unknown in healthy aging. We examined the effect of reward and punishment anticipation on intentional declarative memory formation for wor...

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Main Authors: Geddes, Maiya, Mattfeld, Aaron T, de los Angeles, Carlo S, Keshavan, Anisha, Gabrieli, John D. E.
Other Authors: Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences
Format: Article
Language:English
Published: Elsevier 2019
Online Access:https://hdl.handle.net/1721.1/122935
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author Geddes, Maiya
Mattfeld, Aaron T
de los Angeles, Carlo S
Keshavan, Anisha
Gabrieli, John D. E.
author2 Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences
author_facet Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences
Geddes, Maiya
Mattfeld, Aaron T
de los Angeles, Carlo S
Keshavan, Anisha
Gabrieli, John D. E.
author_sort Geddes, Maiya
collection MIT
description The neural circuitry mediating the influence of motivation on long-term declarative or episodic memory formation is delineated in young adults, but its status is unknown in healthy aging. We examined the effect of reward and punishment anticipation on intentional declarative memory formation for words using an event-related functional magnetic resonance imaging (fMRI) monetary incentive encoding task in twenty-one younger and nineteen older adults. At 24-hour memory retrieval testing, younger adults were significantly more likely to remember words associated with motivational cues than neutral cues. Motivational enhancement of memory in younger adults occurred only for recollection (“remember” responses) and not for familiarity (“familiar” responses). Older adults had overall diminished memory and did not show memory gains in association with motivational cues. Memory encoding associated with monetary rewards or punishments activated motivational (substantia nigra/ventral tegmental area) and memory-related (hippocampus) brain regions in younger, but not older, adults during the target word periods. In contrast, older and younger adults showed similar activation of these brain regions during the anticipatory motivational cue interval. In a separate monetary incentive delay task that did not require learning, we found evidence for relatively preserved striatal reward anticipation in older adults. This supports a potential dissociation between incidental and intentional motivational processes in healthy aging. The finding that motivation to obtain rewards and avoid punishments had reduced behavioral and neural influence on intentional episodic memory formation in older compared to younger adults is relevant to life-span theories of cognitive aging including the dopaminergic vulnerability hypothesis. Keywords: monetary incentive encoding; monetary incentive delay; reward; punishment; aging; fMRI; memory; learning; motivation; hippocampus; ventral tegmental area; striatum
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spelling mit-1721.1/1229352022-09-26T15:31:36Z Human aging reduces the neurobehavioral influence of motivation on episodic memory Geddes, Maiya Mattfeld, Aaron T de los Angeles, Carlo S Keshavan, Anisha Gabrieli, John D. E. Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences McGovern Institute for Brain Research at MIT The neural circuitry mediating the influence of motivation on long-term declarative or episodic memory formation is delineated in young adults, but its status is unknown in healthy aging. We examined the effect of reward and punishment anticipation on intentional declarative memory formation for words using an event-related functional magnetic resonance imaging (fMRI) monetary incentive encoding task in twenty-one younger and nineteen older adults. At 24-hour memory retrieval testing, younger adults were significantly more likely to remember words associated with motivational cues than neutral cues. Motivational enhancement of memory in younger adults occurred only for recollection (“remember” responses) and not for familiarity (“familiar” responses). Older adults had overall diminished memory and did not show memory gains in association with motivational cues. Memory encoding associated with monetary rewards or punishments activated motivational (substantia nigra/ventral tegmental area) and memory-related (hippocampus) brain regions in younger, but not older, adults during the target word periods. In contrast, older and younger adults showed similar activation of these brain regions during the anticipatory motivational cue interval. In a separate monetary incentive delay task that did not require learning, we found evidence for relatively preserved striatal reward anticipation in older adults. This supports a potential dissociation between incidental and intentional motivational processes in healthy aging. The finding that motivation to obtain rewards and avoid punishments had reduced behavioral and neural influence on intentional episodic memory formation in older compared to younger adults is relevant to life-span theories of cognitive aging including the dopaminergic vulnerability hypothesis. Keywords: monetary incentive encoding; monetary incentive delay; reward; punishment; aging; fMRI; memory; learning; motivation; hippocampus; ventral tegmental area; striatum 2019-11-14T18:30:26Z 2019-11-14T18:30:26Z 2018-05-01 2015-12-16 2019-10-01T14:09:27Z Article http://purl.org/eprint/type/JournalArticle 1053-8119 https://hdl.handle.net/1721.1/122935 Geddes, Maiya R. et al. "Human aging reduces the neurobehavioral influence of motivation on episodic memory." NeuroImage 171 (May 2018): 296-310 © 2017 The Author(s) en http://dx.doi.org/10.1016/j.neuroimage.2017.12.053 NeuroImage Creative Commons Attribution-NonCommercial-NoDerivs License http://creativecommons.org/licenses/by-nc-nd/4.0/ application/pdf Elsevier Elsevier
spellingShingle Geddes, Maiya
Mattfeld, Aaron T
de los Angeles, Carlo S
Keshavan, Anisha
Gabrieli, John D. E.
Human aging reduces the neurobehavioral influence of motivation on episodic memory
title Human aging reduces the neurobehavioral influence of motivation on episodic memory
title_full Human aging reduces the neurobehavioral influence of motivation on episodic memory
title_fullStr Human aging reduces the neurobehavioral influence of motivation on episodic memory
title_full_unstemmed Human aging reduces the neurobehavioral influence of motivation on episodic memory
title_short Human aging reduces the neurobehavioral influence of motivation on episodic memory
title_sort human aging reduces the neurobehavioral influence of motivation on episodic memory
url https://hdl.handle.net/1721.1/122935
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