The use of sequential hippocampal-dependent and -non-dependent tasks to study the activation profile of the anterior cingulate cortex during recent and remote memory tests

Wartman, Brianne C.; Holahan, Matthew R.

doi:10.1016/j.nlm.2013.08.011

Cited by 18 publications

(22 citation statements)

References 62 publications

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“…This finding supports the hypothesis that taxing the demand placed upon the hippocampus, by training rats on two hippocampal-dependent tasks, results in structural changes indicative of memory storage, in the ACC. This is consistent with results from Wartman and Holahan (2013) that showed increased number of c-Fos positive cells in remotely probed groups compared to recently probed groups. In that report, the group trained on two hippocampal-dependent tasks (WM/RAM) and probed recently demonstrated increased c-Fos labeling in the ACC compared to the other recently probed groups, and similar to the level of c-Fos labeling noted in remotely probed groups, suggesting an accelerated reliance on the ACC.…”

Section: Resultssupporting

confidence: 92%

The impact of multiple memory formation on dendritic complexity in the hippocampus and anterior cingulate cortex assessed at recent and remote time points

Wartman

Holahan

2014

Front. Behav. Neurosci.

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Consolidation processes, involving synaptic and systems level changes, are suggested to stabilize memories once they are formed. At the synaptic level, dendritic structural changes are associated with long-term memory storage. At the systems level, memory storage dynamics between the hippocampus and anterior cingulate cortex (ACC) may be influenced by the number of sequentially encoded memories. The present experiment utilized Golgi-Cox staining and neuron reconstruction to examine recent and remote structural changes in the hippocampus and ACC following training on three different behavioral procedures. Rats were trained on one hippocampal-dependent task only (a water maze task), two hippocampal-dependent tasks (a water maze task followed by a radial arm maze task), or one hippocampal-dependent and one non-hippocampal-dependent task (a water maze task followed by an operant conditioning task). Rats were euthanized recently or remotely. Brains underwent Golgi-Cox processing and neurons were reconstructed using Neurolucida software (MicroBrightField, Williston, VT, USA). Rats trained on two hippocampal-dependent tasks displayed increased dendritic complexity compared to control rats, in neurons examined in both the ACC and hippocampus at recent and remote time points. Importantly, this behavioral group showed consistent, significant structural differences in the ACC compared to the control group at the recent time point. These findings suggest that taxing the demand placed upon the hippocampus, by training rats on two hippocampal-dependent tasks, engages synaptic and systems consolidation processes in the ACC at an accelerated rate for recent and remote storage of spatial memories.

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Section: Resultssupporting

confidence: 92%

The impact of multiple memory formation on dendritic complexity in the hippocampus and anterior cingulate cortex assessed at recent and remote time points

Wartman

Holahan

2014

Front. Behav. Neurosci.

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“…Indeed, unbiased stereological quantification of c-Fos expression in the ACC confirmed a greater number of c-Fos-positive cells following retrieval of the remote over the recent memory, similar to the findings of other studies (Teixeira et al 2006;Lopez et al 2012;Wartman and Holahan 2013). The recruitment of the ACC for remote memory is typically interpreted as evidence that the memory becomes dependent on and stored in the ACC (Frankland and Bontempi 2005;Weible 2013).…”

supporting

confidence: 84%

“…A cognitive map of the platform location is established by making use of extra-pool cues present in the testing room (Morris 1984;Sutherland and Hamilton 2004). Importantly, past work has shown that ACC activation is greater following the retrieval of a remote than a recent memory in this task (Teixeira et al 2006;Lopez et al 2012;Wartman and Holahan 2013). However, because performance on the MWT is sensitive to cue-availability (Lopez et al 2012), it is therefore possible to increase retrieval difficulty during the retention test by removing some of the cues from the room.…”

mentioning

confidence: 99%

Increased task demand during spatial memory testing recruits the anterior cingulate cortex

2016

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We examined whether increasing retrieval difficulty in a spatial memory task would promote the recruitment of the anterior cingulate cortex (ACC) similar to what is typically observed during remote memory retrieval. Rats were trained on the hidden platform version of the Morris Water Task and tested three or 30 d later. Retrieval difficulty was manipulated by removing several prominent extra-pool cues from the testing room. Immediate early gene expression (c-Fos) in the ACC was greater following the cue removal and comparable to remote memory retrieval (30-d retention interval) levels, supporting the view of increased ACC contribution during high cognitive-demand memory processes.[Supplemental material is available for this article.]Long-term systems consolidation suggests that memories that are initially dependent on the hippocampus (HPC) become increasingly represented in other cortical structures over time, such that they can eventually survive complete HPC damage (Squire and Alvarez 1995;Frankland and Bontempi 2005). The anterior cingulate cortex (ACC) is one structure that is thought to come to support these HPC-independent memories. This is based largely on findings suggesting that inactivation or damage to the ACC impairs the recall of remote memories while sparing recent ones Teixeira et al. 2006;Ding et al. 2008) and that the ACC shows greater activation during recall of a remote memory than a recent one. For example, Teixeira et al. (2006) found that the retrieval of a remote (1 mo old) spatial memory in mice elicited greater expression of the immediate-early genes c-Fos and zif268 in the ACC than retrieval of a recent (1 d old) memory, concluding that spatial memory becomes consolidated and dependent on the ACC over a protracted period of time.Although these previous findings suggest that the ACC contributes to the recall of remote memories, these observations could be alternatively explained by the increased cognitive demand that would follow the retrieval of older and temporally degraded memories (Rudy et al. 2005). Specifically, Rudy et al. (2005) proposed that memories, through either forgetting or interference, become weaker with the passage of time, which in turn requires greater cognitive effort for successful retrieval. This increase in cognitive demand would also cause the recruitment of additional cortical structures, including the ACC, in order to overcome the retrieval difficulty. According to this view, the ACC would not be directly involved in long-term systems consolidation and the storage of remote memories per se, but would play a key role in additional cognitive processes associated with the retrieval of remote memories. The aim of this study was to assess whether the ACC is indeed recruited under retrieval conditions that require greater cognitive processing.If the role of the ACC in remote memory is due to an increase in cognitive processing to compensate for the retrieval difficulty of a degraded memory, then it should be possible to increase ACC activation for a recent memory b...

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“…), indicating that a higher demand of information processing leads to an accelerated ACC‐dependency of CFC memory. This idea is supported by two recent articles (Wartman and Holahan, ), showing that multiple learning experiences induce changes in dendritic spine complexity and c‐fos expression in ACC at short delays that resemble those of remote memories. In addition, the HPC plays a crucial role in neocortical memory‐related plasticity (Sutherland et al, ), suggesting that the accelerated HPC‐to‐ACC memory reorganization is actively induced by the HPC.…”

Section: Discussionmentioning

confidence: 66%

Novel learning accelerates systems consolidation of a contextual fear memory

et al. 2016

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After initial encoding memories may undergo a time-dependent reorganization, becoming progressively independent from the hippocampus (HPC) and dependent on cortical regions such as the anterior cingulate cortex (ACC). Although the mechanisms underlying systems consolidation are somewhat known, the factors determining its temporal dynamics are still poorly understood. Here, we studied the influence of novel learning occurring between training and test sessions on the time-course of HPC- and ACC-dependency of contextual fear conditioning (CFC) memory expression. We found that muscimol was disruptive when infused into the HPC up to 35 days after training, while the ACC is vulnerable only after 45 days. However, when animals were subjected to a series of additional, distinct tasks to be learned within the first 3 weeks, muscimol became effective sooner. Muscimol had no effect in the HPC at 20 days after training, exactly when the ACC becomes responsive to this treatment. Thus, our data indicates that the encoding of new information generates a tight interplay between distinct memories, accelerating the reorganization of previously stored long term memories between the hippocampal and cortical areas. © 2016 Wiley Periodicals, Inc.

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The use of sequential hippocampal-dependent and -non-dependent tasks to study the activation profile of the anterior cingulate cortex during recent and remote memory tests

Cited by 18 publications

References 62 publications

The impact of multiple memory formation on dendritic complexity in the hippocampus and anterior cingulate cortex assessed at recent and remote time points

The impact of multiple memory formation on dendritic complexity in the hippocampus and anterior cingulate cortex assessed at recent and remote time points

Increased task demand during spatial memory testing recruits the anterior cingulate cortex

Novel learning accelerates systems consolidation of a contextual fear memory

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