The medial entorhinal cortex mediates basolateral amygdala effects on spatial memory and downstream activity-regulated cytoskeletal-associated protein expression

Wahlstrom, Krista L.; Alvarez-Dieppa, Amanda; McIntyre, Christa K.; LaLumiere, Ryan T.

doi:10.1038/s41386-020-00875-6

Cited by 9 publications

(5 citation statements)

References 95 publications

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“…Therefore post-injury testing targeted the ability to recall a previously learned task. Second, mice completed the Barnes maze (Barnes et al, 1980), which is a hippocampal-dependent spatial memory task (McNaughton et al, 1986) that also engages other brain regions such as the basolateral amygdala and entorhinal cortex for memory consolidation (Wahlstrom et al, 2020). Third, mice completed fear conditioning which includes both hippocampaldependent and -independent components and is associated with cholinergic signaling (Gould and Wehner, 1999;Gale et al, 2001;Maren, 2003;Feiro and Gould, 2005;Pape and Pare, 2010).…”

Section: Discussionmentioning

confidence: 99%

“…These data show that TBI does not induce gross pathological changes near the site of injury 17 weeks post-injury; however, other brain regions may be important in modulating behavioral recovery. For example, Barnes maze also engages other brain regions such as the basolateral amygdala and entorhinal cortex for memory consolidation (Wahlstrom et al, 2020). In addition, the hippocampus is required for the US-context association but the amygdala is required for the CS-US association (Kim and Fanselow, 1992;Phillips and LeDoux, 1992;Rudy, 1993;Gerlai, 1998).…”

Section: Discussionmentioning

confidence: 99%

“…Brain regions of interest were in close proximity to the epicenter of the injury and included the ipsilateral primary somatosensory cortex, dentate gyrus, and dorsolateral thalamus. We also examined the basolateral amygdala because of its involvement in spatial and conditioned fear memory (Maren, 2003;Pape and Pare, 2010;Wahlstrom et al, 2020). No significant differences in Iba1 and NeuN were identified between experimental groups in the thalamus.…”

Section: Gross Pathological Change Is Absent Near the Site Of Injury ...mentioning

confidence: 99%

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Lateral Fluid Percussion Injury Causes Sex-Specific Deficits in Anterograde but Not Retrograde Memory

Fitzgerald

Houle

Cotter

et al. 2022

Front. Behav. Neurosci.

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Cognitive impairment is a common symptom after traumatic brain injury (TBI). Memory, in particular, is often disrupted during chronic post-injury recovery. To understand the sex-specific effects of brain injury on retrograde and anterograde memory, we examined paired associate learning (PAL), spatial learning and memory, and fear memory after lateral fluid percussion TBI. We hypothesized that male and female mice would display unique memory deficits after TBI. PAL task acquisition was initiated via touchscreen operant conditioning 22 weeks before sham injury or TBI. Post-injury PAL testing occurred 7 weeks post-injury. Barnes maze and fear conditioning were completed at 14- and 15-weeks post-injury, respectively. Contrary to our expectations, behavioral outcomes were not primarily influenced by TBI. Instead, sex-specific differences were observed in all tasks which exposed task-specific trends in male TBI mice. Male mice took longer to complete the PAL task, but this was not affected by TBI and did not compromise the ability to make a correct choice. Latency to reach the goal box decreased across testing days in Barnes maze, but male TBI mice lagged in improvement compared to all other groups. Use of two learning indices revealed that male TBI mice were deficient in transferring information from 1 day to the next. Finally, acquisition and contextual retention of fear memory were similar between all groups. Cued retention of the tone-shock pairing was influenced by both injury and sex. Male sham mice displayed the strongest cued retention of fear memory, evidenced by increased freezing behavior across the test trial. In contrast, male TBI mice displayed reduced freezing behavior with repetitive tone exposure. An inverse relationship in freezing behavior to tone exposure was detected between female sham and TBI mice, although the difference was not as striking. Together, these studies show that retrograde memory is intact after lateral TBI. However, male mice are more vulnerable to post-injury anterograde memory deficits. These behaviors were not associated with gross pathological change near the site injury or in subcortical brain regions associated with memory formation. Future studies that incorporate pre- and post-injury behavioral analysis will be integral in defining sex-specific memory impairment after TBI.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Gross Pathological Change Is Absent Near the Site Of Injury ...mentioning

confidence: 99%

See 1 more Smart Citation

Lateral Fluid Percussion Injury Causes Sex-Specific Deficits in Anterograde but Not Retrograde Memory

Fitzgerald

Houle

Cotter

et al. 2022

Front. Behav. Neurosci.

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“…Work from our laboratory found that stimulation of basolateral amygdala (BLA) cell bodies and BLA projections to other brain regions influenced memory consolidation in a frequency‐dependent manner—i.e., stimulation at a specific frequency produced memory enhancement or impairment not observed with other frequencies (Huff et al., 2016; Huff et al., 2013; Wahlstrom et al., 2018). Moreover, the stimulation frequency determined whether there were downstream alterations in synaptic plasticity‐associated proteins (Wahlstrom et al., 2021). A substantial body of literature supports the idea that specific neural rhythms or oscillations play a role in facilitating neural activity across structures important for memory and suggests the importance of these oscillations in memory consolidation (Bauer et al., 2007; Buzsaki, 2005; Buzsaki & Moser, 2013; Kanta et al., 2019; Popescu et al., 2009).…”

Section: Frequency Specificitymentioning

confidence: 99%

Theoretical Considerations for Optimizing the Use of Optogenetics with Complex Behavior

Glickman,

LaLumiere

2023

Current Protocols

Self Cite

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Optogenetic approaches have allowed researchers to address complex questions about behavior that were previously unanswerable. However, as optogenetic procedures involve a large parameter space across multiple dimensions, it is crucial to consider such parameters in conjunction with the behaviors under study. Here, we discuss strategies to optimize optogenetic approaches with complex behavior by identifying critical experimental design considerations, including frequency specificity, temporal precision, activitycontrolled optogenetics, stimulation pattern, and cell-type specificity. We highlight potential limitations or theoretical considerations to be made when manipulating each of these factors of optogenetic experiments. This overview emphasizes the importance of optimizing optogenetic study design to enhance the conclusions that can be drawn about the neuroscience of behavior.

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“…dCA3 outputs to the dCA1 have been implicated in contextual fear-memory reconsolidation 43 , and the dCA1 and BLA exhibit synchronized theta activity during fear-memory reconsolidation 44 . Some other relay regions between the dCA1 or the dCA1-dCA3 circuit and the BLA may include the ventral hippocampus 42,45,46 , entorhinal cortex 47,48 , and perirhinal cortex 42,49 , based on their connectivity with both the BLA and DH and their recognized involvement in memory reconsolidation in other paradigms.…”

Section: Reconsolidationmentioning

confidence: 99%

Optogenetic inhibition of the dorsal hippocampus CA3 region during early-stage cocaine-memory reconsolidation disrupts subsequent context-induced cocaine seeking in rats

Tan

Wang

et al. 2022

Neuropsychopharmacol.

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The dorsal hippocampus (DH) is key to the long-term maintenance of cocaine memories following retrieval-induced memory destabilization; even though, it is not the site of protein synthesis-dependent memory reconsolidation. Here, we took advantage of the temporal and spatial specificity of an optogenetic manipulation to examine the role of the cornu ammonis 3 subregion of the DH (dCA3) in early-stage cocaine-memory reconsolidation. Male Sprague-Dawley rats expressing eNpHR3.0 in the DH were trained to self-administer cocaine in a distinct context and underwent extinction training in a different context. Rats then received a 15-min memory-reactivation session, to destabilize cocaine memories and trigger reconsolidation, or remained in their home cages (no-reactivation controls).Optogenetic inhibition of the dCA3 for 1 h immediately, but not 1 h, after memory reactivation resulted in cocaine-memory impairment as indicated by reduction in drug-seeking behavior selectively in the cocaine-paired context 3 d later, at test, relative to responding in no-inhibition, no-reactivation, and no-eNpHR3.0 controls. Cocaine-memory impairment was associated with reduced c-Fos expression, an index of neuronal activation, in the dCA3 stratum lucidum (SL) and stratum pyramidale (SP) at test.Based on these observations and extant literature, we postulate that recurrent circuits in the SP are activated during early-stage memory reconsolidation to maintain labile cocaine memories prior to protein synthesis-dependent restabilization in another brain region, such as the basolateral amygdala.Furthermore, SL and SP interneurons may enhance memory reconsolidation by limiting synaptic noise in the SP and also contribute to recall as elements of the updated cocaine engram or retrieval links..

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The medial entorhinal cortex mediates basolateral amygdala effects on spatial memory and downstream activity-regulated cytoskeletal-associated protein expression

Abstract: The authors thank John Wemmie, Rong Fan, and Joshua Weiner for their excellent technical assistance and for allowing us to utilize their laboratory facilities for the experiments involving Western blotting.

Cited by 9 publications

References 95 publications

Lateral Fluid Percussion Injury Causes Sex-Specific Deficits in Anterograde but Not Retrograde Memory

Lateral Fluid Percussion Injury Causes Sex-Specific Deficits in Anterograde but Not Retrograde Memory

Theoretical Considerations for Optimizing the Use of Optogenetics with Complex Behavior

Optogenetic inhibition of the dorsal hippocampus CA3 region during early-stage cocaine-memory reconsolidation disrupts subsequent context-induced cocaine seeking in rats

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