Behaviorally activated mRNA expression profiles produce signatures of learning and enhanced inhibition in aged rats with preserved memory
Aging is often associated with cognitive decline, but many elderly individuals maintain a high level of function throughout life. Here we studied outbred rats, which also exhibit individual differences across a spectrum of outcomes that includes both preserved and impaired spatial memory. Previous w...
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| creator | Haberman, Rebecca P Colantuoni, Carlo Koh, Ming Teng Gallagher, Michela |
| description | Aging is often associated with cognitive decline, but many elderly individuals maintain a high level of function throughout life. Here we studied outbred rats, which also exhibit individual differences across a spectrum of outcomes that includes both preserved and impaired spatial memory. Previous work in this model identified the CA3 subfield of the hippocampus as a region critically affected by age and integral to differing cognitive outcomes. Earlier microarray profiling revealed distinct gene expression profiles in the CA3 region, under basal conditions, for aged rats with intact memory and those with impairment. Because prominent age-related deficits within the CA3 occur during neural encoding of new information, here we used microarray analysis to gain a broad perspective of the aged CA3 transcriptome under activated conditions. Behaviorally-induced CA3 expression profiles differentiated aged rats with intact memory from those with impaired memory. In the activated profile, we observed substantial numbers of genes (greater than 1000) exhibiting increased expression in aged unimpaired rats relative to aged impaired, including many involved in synaptic plasticity and memory mechanisms. This unimpaired aged profile also overlapped significantly with a learning induced gene profile previously acquired in young adults. Alongside the increased transcripts common to both young learning and aged rats with preserved memory, many transcripts behaviorally-activated in the current study had previously been identified as repressed in the aged unimpaired phenotype in basal expression. A further distinct feature of the activated profile of aged rats with intact memory is the increased expression of an ensemble of genes involved in inhibitory synapse function, which could control the phenotype of neural hyperexcitability found in the CA3 region of aged impaired rats. These data support the conclusion that aged subjects with preserved memory recruit adaptive mechanisms to retain tight control over excitability under both basal and activated conditions. |
| doi_str_mv | 10.1371/journal.pone.0083674 |
| format | Article |
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Here we studied outbred rats, which also exhibit individual differences across a spectrum of outcomes that includes both preserved and impaired spatial memory. Previous work in this model identified the CA3 subfield of the hippocampus as a region critically affected by age and integral to differing cognitive outcomes. Earlier microarray profiling revealed distinct gene expression profiles in the CA3 region, under basal conditions, for aged rats with intact memory and those with impairment. Because prominent age-related deficits within the CA3 occur during neural encoding of new information, here we used microarray analysis to gain a broad perspective of the aged CA3 transcriptome under activated conditions. Behaviorally-induced CA3 expression profiles differentiated aged rats with intact memory from those with impaired memory. In the activated profile, we observed substantial numbers of genes (greater than 1000) exhibiting increased expression in aged unimpaired rats relative to aged impaired, including many involved in synaptic plasticity and memory mechanisms. This unimpaired aged profile also overlapped significantly with a learning induced gene profile previously acquired in young adults. Alongside the increased transcripts common to both young learning and aged rats with preserved memory, many transcripts behaviorally-activated in the current study had previously been identified as repressed in the aged unimpaired phenotype in basal expression. A further distinct feature of the activated profile of aged rats with intact memory is the increased expression of an ensemble of genes involved in inhibitory synapse function, which could control the phenotype of neural hyperexcitability found in the CA3 region of aged impaired rats. These data support the conclusion that aged subjects with preserved memory recruit adaptive mechanisms to retain tight control over excitability under both basal and activated conditions.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0083674</identifier><identifier>PMID: 24349543</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Adaptive control ; Adults ; Age ; Aging ; Aging - metabolism ; Animal behavior ; Animals ; Behavior, Animal - physiology ; Brain ; CA3 Region, Hippocampal - cytology ; CA3 Region, Hippocampal - metabolism ; Cognition & reasoning ; Cognitive ability ; DNA microarrays ; Excitability ; Gene expression ; Genes ; Genetic research ; Geriatrics ; Learning ; Learning - physiology ; Male ; Memory ; Memory - physiology ; Memory tasks ; Messenger RNA ; Neural coding ; Neurobiology ; Neurophysiology ; Older people ; Principal components analysis ; Rats ; Rats, Long-Evans ; RNA, Messenger - biosynthesis ; Rodents ; Spatial analysis ; Spatial memory ; Synapses ; Synaptic plasticity ; Young adults</subject><ispartof>PloS one, 2013-12, Vol.8 (12), p.e83674-e83674</ispartof><rights>COPYRIGHT 2013 Public Library of Science</rights><rights>2013 Haberman et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 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These data support the conclusion that aged subjects with preserved memory recruit adaptive mechanisms to retain tight control over excitability under both basal and activated conditions.</description><subject>Adaptive control</subject><subject>Adults</subject><subject>Age</subject><subject>Aging</subject><subject>Aging - metabolism</subject><subject>Animal behavior</subject><subject>Animals</subject><subject>Behavior, Animal - physiology</subject><subject>Brain</subject><subject>CA3 Region, Hippocampal - cytology</subject><subject>CA3 Region, Hippocampal - metabolism</subject><subject>Cognition & reasoning</subject><subject>Cognitive ability</subject><subject>DNA microarrays</subject><subject>Excitability</subject><subject>Gene expression</subject><subject>Genes</subject><subject>Genetic research</subject><subject>Geriatrics</subject><subject>Learning</subject><subject>Learning - physiology</subject><subject>Male</subject><subject>Memory</subject><subject>Memory - physiology</subject><subject>Memory tasks</subject><subject>Messenger RNA</subject><subject>Neural coding</subject><subject>Neurobiology</subject><subject>Neurophysiology</subject><subject>Older people</subject><subject>Principal components analysis</subject><subject>Rats</subject><subject>Rats, Long-Evans</subject><subject>RNA, Messenger - 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Here we studied outbred rats, which also exhibit individual differences across a spectrum of outcomes that includes both preserved and impaired spatial memory. Previous work in this model identified the CA3 subfield of the hippocampus as a region critically affected by age and integral to differing cognitive outcomes. Earlier microarray profiling revealed distinct gene expression profiles in the CA3 region, under basal conditions, for aged rats with intact memory and those with impairment. Because prominent age-related deficits within the CA3 occur during neural encoding of new information, here we used microarray analysis to gain a broad perspective of the aged CA3 transcriptome under activated conditions. Behaviorally-induced CA3 expression profiles differentiated aged rats with intact memory from those with impaired memory. In the activated profile, we observed substantial numbers of genes (greater than 1000) exhibiting increased expression in aged unimpaired rats relative to aged impaired, including many involved in synaptic plasticity and memory mechanisms. This unimpaired aged profile also overlapped significantly with a learning induced gene profile previously acquired in young adults. Alongside the increased transcripts common to both young learning and aged rats with preserved memory, many transcripts behaviorally-activated in the current study had previously been identified as repressed in the aged unimpaired phenotype in basal expression. A further distinct feature of the activated profile of aged rats with intact memory is the increased expression of an ensemble of genes involved in inhibitory synapse function, which could control the phenotype of neural hyperexcitability found in the CA3 region of aged impaired rats. These data support the conclusion that aged subjects with preserved memory recruit adaptive mechanisms to retain tight control over excitability under both basal and activated conditions.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>24349543</pmid><doi>10.1371/journal.pone.0083674</doi><tpages>e83674</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Adaptive control Adults Age Aging Aging - metabolism Animal behavior Animals Behavior, Animal - physiology Brain CA3 Region, Hippocampal - cytology CA3 Region, Hippocampal - metabolism Cognition & reasoning Cognitive ability DNA microarrays Excitability Gene expression Genes Genetic research Geriatrics Learning Learning - physiology Male Memory Memory - physiology Memory tasks Messenger RNA Neural coding Neurobiology Neurophysiology Older people Principal components analysis Rats Rats, Long-Evans RNA, Messenger - biosynthesis Rodents Spatial analysis Spatial memory Synapses Synaptic plasticity Young adults |
| title | Behaviorally activated mRNA expression profiles produce signatures of learning and enhanced inhibition in aged rats with preserved memory |
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