Spontaneous Changes of Neocortical Code for Associative Memory During Consolidation

Takehara‐Nishiuchi, Kaori; McNaughton, Bruce L.

doi:10.1126/science.1161299

Cited by 210 publications

(195 citation statements)

References 27 publications

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“…Retention of long-but not short-term memory in certain types of associative learning has indeed been shown to require delayed synaptic changes in the mPFC (TakeharaNishiuchi et al, 2006;Takehara-Nishiuchi and McNaughton, 2008). This hypothesis is also consistent with the role of the mPFC in other studies, which show that mPFC is not required for primary learning but becomes essential when experimental conditions, such as CS-US contingencies, are reversed in a subsequent phase (Schoenbaum et al, 2000).…”

Section: Discussionsupporting

confidence: 77%

Lack of Medial Prefrontal Cortex Activation Underlies the Immediate Extinction Deficit

Kim¹,

Jo²,

Kim³

et al. 2010

J. Neurosci.

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We conducted a series of experiments to investigate the neural basis of the immediate extinction deficit, the lack of extinction when the interval between fear memory acquisition and extinction is short. In experiment 1, rats were given extinction training composed of 15 conditioned stimuli (CSs) either 15 min (immediate extinction: I-EXT) or 24 h (delayed extinction: D-EXT) after five tone-shock pairings. In the retention test performed 48 h after conditioning, I-EXT group exhibited significantly higher freezing than D-EXT group. In experiment 2, functional activation in the medial prefrontal cortex (mPFC) was detected using c-fos immunoreactivity. The number of Fos-positive neurons in the mPFC was significantly lower in I-EXT group than in D-EXT group. In experiment 3, rats received immediate extinction with microstimulation of the infralimbic region (IL) of the mPFC, either contingently paired or unpaired with the CS. In a subsequent retention test, the paired stimulation group exhibited decreased freezing relative to the unpaired stimulation group. Together, our results suggest that the immediate extinction deficit may be linked to the lack of neuronal activity in the IL.

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Section: Discussionsupporting

confidence: 77%

Lack of Medial Prefrontal Cortex Activation Underlies the Immediate Extinction Deficit

Kim¹,

Jo²,

Kim³

et al. 2010

J. Neurosci.

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“…These results confirm that the mPFC plays a key role in retrieving consolidated memories (Frankland and Bontempi, 2006;Takashima et al, 2006;Takehara-Nishiuchi and McNaughton, 2008). Additionally, since semantic congruency reflects the degree to which the newly learned information fits to preexisting knowledge (i.e., schema) (Kim et al, 2008), and given the assumption that such congruent information is more rapidly assimilated than information that does not fit a prior schema (Tse et al, 2007;van Kesteren et al, 2010), our data further support the view that such a fast track in memory consolidation might also be present in humans.…”

Section: Discussionsupporting

confidence: 74%

“…Along with its putative role in systems consolidation and retrieval (Maguire, 2001;Frankland and Bontempi, 2006;Takashima et al, 2006;Takehara-Nishiuchi and McNaughton, 2008), the mPFC has been indicated as a region involved in a diversity of functions, among which many with a mnemonic nature. The prefrontal cortex in general is believed to be involved in updating, maintenance, and manipulation of memory traces (Buckner and Wheeler, 2001;Fletcher and Henson, 2001), and the mPFC in particular is thought to be related to feeling of knowing (Kikyo et al, 2002), conceptual knowledge integration (Kumaran et al, 2009), perceptual matching (Summerfield and Koechlin, 2008), comprehension (Maguire et al, 1999;Mar, 2004), and remote associative memory (Takashima et al, 2007;Takehara-Nishiuchi and McNaughton, 2008), and is shown to actively replay learning-related neuronal spiking patterns during sleep (Takehara-Nishiuchi and McNaughton, 2008;Peyrache et al, 2009). Furthermore, mPFC lesions lead to specific retrieval impairments for remote, presumably consolidated memories (Takehara-Nishiuchi et al, 2006;Gilboa et al, 2009), and an absence of semantic congruency memory enhancement (Kan et al, 2009).…”

Section: Discussionmentioning

confidence: 99%

“…Along with the hippocampus, an important brain region that is indicated to be involved in the retrieval of consolidated memories is the medial prefrontal cortex (mPFC) (Frankland and Bontempi, 2006;Takashima et al, 2006;Takehara-Nishiuchi and McNaughton, 2008). Moreover, the interaction between the hippocampus and the mPFC is believed to be important already in early stages of memory formation, as discovered in rodents (Benchenane et al, 2010), as well as humans (van Kesteren et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

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Retrieval of Associative Information Congruent with Prior Knowledge Is Related to Increased Medial Prefrontal Activity and Connectivity

Kesteren¹,

Rijpkema²,

Ruiter³

et al. 2010

J. Neurosci.

215

167

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We remember information that is congruent instead of incongruent with prior knowledge better, but the underlying neural mechanisms related to this enhancement are still relatively unknown. Recently, this memory enhancement due to a prior schema has been suggested to be based on rapid neocortical assimilation of new information, related to optimized encoding and consolidation processes. The medial prefrontal cortex (mPFC) is thought to be important in mediating this process, but its role in retrieval of schema-consistent information is still unclear. In this study, we regarded multisensory congruency with prior knowledge as a schema and used this factor to probe retrieval of consolidated memories either consistent or inconsistent with prior knowledge. We conducted a visuotactile learning paradigm in which participants studied visual motifs randomly associated with word-fabric combinations that were either congruent or incongruent with common knowledge. The next day, participants were scanned using functional magnetic resonance imaging while their memory was tested. Congruent associations were remembered better than incongruent ones. This behavioral finding was parallelized by stronger retrieval-related activity in and connectivity between medial prefrontal and left somatosensory cortex. Moreover, we found a positive across-subject correlation between the connectivity enhancement and the behavioral congruency effect. These results show that successful retrieval of congruent compared to incongruent visuotactile associations is related to enhanced processing in an mPFCsomatosensory network, and support the hypothesis that new information that fits a preexisting schema is more rapidly assimilated in neocortical networks, a process that may be mediated, at least in part, by the mPFC.

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“…In addition, several regions of the neocortex become more important for memory retrieval with the passage of time. Remote memory for context fear, spatial locations, and eyeblink conditioning requires the medial prefrontal cortex (Takehara et al 2003;Frankland et al 2004;Maviel et al 2004;Takehara-Nishiuchi and McNaughton 2008;TakeharaNishiuchi et al 2011), while socially transmitted food preferences depend on the oribitofrontal cortex (Lesburgueres et al 2011). Increased immediate early gene expression in the neocortex is also observed during remote memory retrieval in these tasks (Maviel et al 2004;Lesburgueres et al 2011).…”

Section: Animal Models Of Systems Consolidationmentioning

confidence: 99%

New methods for understanding systems consolidation

Tayler

Wiltgen

2013

Learn. Mem.

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According to the standard model of systems consolidation (SMC), neocortical circuits are reactivated during the retrieval of declarative memories. This process initially requires the hippocampus. However, with the passage of time, neocortical circuits become strengthened and can eventually retrieve memory without input from the hippocampus. Although consistent with lesion data, these assumptions have been difficult to confirm experimentally. In the current review, we discuss recent methodological advances in behavioral neuroscience that are making it possible to test the basic assumptions of SMC for the first time. For example, new transgenic mice can be used to monitor the activity of individual neurons across the entire brain while optogenetic approaches provide precise control over the activity of these cells using light stimulation. These tools can be used to examine the reactivation of neocortical neurons during recent and remote memory retrieval and determine if this process requires the hippocampus.

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Spontaneous Changes of Neocortical Code for Associative Memory During Consolidation

Cited by 210 publications

References 27 publications

Lack of Medial Prefrontal Cortex Activation Underlies the Immediate Extinction Deficit

Lack of Medial Prefrontal Cortex Activation Underlies the Immediate Extinction Deficit

Retrieval of Associative Information Congruent with Prior Knowledge Is Related to Increased Medial Prefrontal Activity and Connectivity

New methods for understanding systems consolidation

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