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      Bidirectional plasticity of cortical pattern recognition and behavioral sensory acuity

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      Nature Neuroscience

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          Abstract

          Learning to adapt to a complex and fluctuating environment requires the ability to adjust neural representations of sensory stimuli. Through pattern completion processes, cortical networks can reconstruct familiar patterns from degraded input patterns, while pattern separation processes allow discrimination of even highly overlapping inputs. Here we show that the balance between pattern separation and completion is experience-dependent. Rats given extensive training with overlapping complex odorant mixtures show improved behavioral discrimination ability and enhanced cortical ensemble pattern separation. In contrast, behavioral training to disregard normally detectable differences between overlapping mixtures results in impaired cortical ensemble pattern separation (enhanced pattern completion) and impaired discrimination. This bidirectional effect was not found in the olfactory bulb, and may be due to plasticity within olfactory cortex itself. Thus pattern recognition, and the balance between pattern separation and completion, is highly malleable based on task demands and occurs in concert with changes in perceptual performance.

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          Most cited references46

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          Requirement for hippocampal CA3 NMDA receptors in associative memory recall.

          Pattern completion, the ability to retrieve complete memories on the basis of incomplete sets of cues, is a crucial function of biological memory systems. The extensive recurrent connectivity of the CA3 area of hippocampus has led to suggestions that it might provide this function. We have tested this hypothesis by generating and analyzing a genetically engineered mouse strain in which the N-methyl-D-asparate (NMDA) receptor gene is ablated specifically in the CA3 pyramidal cells of adult mice. The mutant mice normally acquired and retrieved spatial reference memory in the Morris water maze, but they were impaired in retrieving this memory when presented with a fraction of the original cues. Similarly, hippocampal CA1 pyramidal cells in mutant mice displayed normal place-related activity in a full-cue environment but showed a reduction in activity upon partial cue removal. These results provide direct evidence for CA3 NMDA receptor involvement in associative memory recall.
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            Cortical map reorganization enabled by nucleus basalis activity.

            Little is known about the mechanisms that allow the cortex to selectively improve the neural representations of behaviorally important stimuli while ignoring irrelevant stimuli. Diffuse neuromodulatory systems may facilitate cortical plasticity by acting as teachers to mark important stimuli. This study demonstrates that episodic electrical stimulation of the nucleus basalis, paired with an auditory stimulus, results in a massive progressive reorganization of the primary auditory cortex in the adult rat. Receptive field sizes can be narrowed, broadened, or left unaltered depending on specific parameters of the acoustic stimulus paired with nucleus basalis activation. This differential plasticity parallels the receptive field remodeling that results from different types of behavioral training. This result suggests that input characteristics may be able to drive appropriate alterations of receptive fields independently of explicit knowledge of the task. These findings also suggest that the basal forebrain plays an active instructional role in representational plasticity.
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              Distinct ensemble codes in hippocampal areas CA3 and CA1.

              The hippocampus has differentiated into an extensively connected recurrent stage (CA3) followed by a feed-forward stage (CA1). We examined the function of this structural differentiation by determining how cell ensembles in rat CA3 and CA1 generate representations of rooms with common spatial elements. In CA3, distinct subsets of pyramidal cells were activated in each room, regardless of the similarity of the testing enclosure. In CA1, the activated populations overlapped, and the overlap increased in similar enclosures. After exposure to a novel room, ensemble activity developed slower in CA3 than CA1, suggesting that the representations emerged independently.
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                Author and article information

                Journal
                9809671
                21092
                Nat Neurosci
                Nat. Neurosci.
                Nature Neuroscience
                1097-6256
                1546-1726
                30 September 2011
                20 November 2011
                01 July 2012
                : 15
                : 1
                : 155-161
                Affiliations
                Emotional Brain Institute, Nathan S. Kline Institute for Psychiatric Research, Orangeburg, NY, 10962, and Department of Child & Adolescent Psychiatry, New York University Langone School of Medicine, New York, NY, 10016
                Author notes
                Correspondence to: Julie Chapuis: jchapuis@ 123456nki.rfmh.org , or Donald Wilson: donald.wilson@ 123456nyumc.org , Emotional Brain Institute, Nathan Kline Institute for Psychiatric Research, 140 Old Orangeburg Road, Orangeburg, New York 10962 USA, Tel: 845-398-2178, FAX: 845-398-2193
                Article
                nihpa328221
                10.1038/nn.2966
                3245808
                22101640
                3e8f3770-df7a-40cb-a560-8023b8bd1b34

                Users may view, print, copy, download and text and data- mine the content in such documents, for the purposes of academic research, subject always to the full Conditions of use: http://www.nature.com/authors/editorial_policies/license.html#terms

                History
                Funding
                Funded by: National Institute on Deafness and Other Communication Disorders : NIDCD
                Award ID: R01 DC003906-14 || DC
                Categories
                Article

                Neurosciences
                Neurosciences

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