Cholinergic deafferentation of the hippocampus causes non-temporally graded retrograde amnesia in an odor discrimination task

Köppen, Jenny R.; Stuebing, Sarah L.; Sieg, Megan L.; Blackwell, Ashley A.; Blankenship, Philip A.; Cheatwood, Joseph L.; Wallace, Douglas G.

doi:10.1016/j.bbr.2015.11.021

Cited by 10 publications

(4 citation statements)

References 36 publications

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“…In the granular dentate gyrus and pyramidal CA1–CA3, M 2 mAChRs are located in inhibitory GABAergic presynaptic terminals, whereas M 1 and M 4 mAChRs are distributed in the somatodendritic compartment of pyramidal neurons. The increase in cortical M 2 mAChR may indicate a secondary regulation of cortical M 2 mAChR, which is consistent with previous studies. ,− Regarding the modulation of hippocampal cholinergic signaling, lesions directed at the medial septum-vertical diagonal band complex have demonstrated a decrease in both density and activity of mAChR, revealing completely opposite effects to those observed when the NBM is lesioned. − The absence of nonspecific damage to the SM-vertical diagonal band complex indicates that the increase in M 2 /M 4 mAChR-mediated signaling in the hippocampus should also be considered as a secondary modulation of muscarinic signaling. In the hippocampus, M 2 mAChR inhibits ACh release, while M 1 mAChR potentiates glutamatergic signaling. ,− Moreover, mice lacking M 2 mAChR showed deficits in learning during avoidance and spatial memory tests, demonstrating the role of this receptor subtype in cognitive processes which are dependent on both short- and long-term potentiation and completely reversed with GABA A receptor antagonists. , Therefore, the immunotoxin-induced increase in hippocampal muscarinic functionality mediated by M 2 mAChR could be decreasing the GABAergic tone and increasing glutamatergic transmission as a compensatory mechanism following the lesion of the NBM, contributing to the so-called “muscarinic long-term potentiation”, which is essential to explain hippocampal neuronal plasticity …”

Section: Results and Discussionsupporting

confidence: 87%

“… 16 , 57 − 61 Regarding the modulation of hippocampal cholinergic signaling, lesions directed at the medial septum-vertical diagonal band complex have demonstrated a decrease in both density and activity of mAChR, revealing completely opposite effects to those observed when the NBM is lesioned. 62 − 66 The absence of nonspecific damage to the SM-vertical diagonal band complex indicates that the increase in M 2 /M 4 mAChR-mediated signaling in the hippocampus should also be considered as a secondary modulation of muscarinic signaling. In the hippocampus, M 2 mAChR inhibits ACh release, while M 1 mAChR potentiates glutamatergic signaling.…”

Section: Results and Discussionmentioning

confidence: 99%

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Specific Phospholipid Modulation by Muscarinic Signaling in a Rat Lesion Model of Alzheimer’s Disease

Llorente-Ovejero

Martínez‐Gardeazabal

Moreno‐Rodríguez

et al. 2021

ACS Chem. Neurosci.

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Alzheimer’s disease (AD) represents the most common cause of dementia worldwide and has been consistently associated with the loss of basal forebrain cholinergic neurons (BFCNs) leading to impaired cholinergic neurotransmission, aberrant synaptic function, and altered structural lipid metabolism. In this sense, membrane phospholipids (PLs) can be used for de novo synthesis of choline (Ch) for the further obtaining of acetylcholine (ACh) when its availability is compromised. Specific lipid species involved in the metabolism of Ch have been identified as possible biomarkers of phenoconversion to AD. Using a rat model of BFCN lesion, we have evaluated the lipid composition and muscarinic signaling in brain areas related to cognitive processes. The loss of BFCN resulted in alterations of varied lipid species related to Ch metabolism at nucleus basalis magnocellularis (NMB) and cortical projection areas. The activity of muscarinic receptors (mAChR) was decreased in the NMB and increased in the hippocampus according to the subcellular distribution of M 1 /M 2 mAChR which could explain the learning and memory impairment reported in this AD rat model. These results suggest that the modulation of specific lipid metabolic routes could represent an alternative therapeutic strategy to potentiate cholinergic neurotransmission and preserve cell membrane integrity in AD.

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Section: Results and Discussionsupporting

confidence: 87%

Section: Results and Discussionmentioning

confidence: 99%

Specific Phospholipid Modulation by Muscarinic Signaling in a Rat Lesion Model of Alzheimer’s Disease

Llorente-Ovejero

Martínez‐Gardeazabal

Moreno‐Rodríguez

et al. 2021

ACS Chem. Neurosci.

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“…Previous analyses of exploratory behavior have primarily used female subjects [33, 35–37]. Neither sexual dimorphisms nor phase of estrous cycle has been observed to influence self-movement cue processing during food hoarding [38]; however, further work is needed to determine if these results generalize to exploratory movement.…”

Section: Methodsmentioning

confidence: 99%

Otolith dysfunction alters exploratory movement in mice

Blankenship

Cherep

Donaldson

et al. 2017

Behavioural Brain Research

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The organization of rodent exploratory behavior appears to depend on self-movement cue processing. As of yet, however, no studies have directly examined the vestibular system’s contribution to the organization of exploratory movement. The current study sequentially segmented open field behavior into progressions and stops in order to characterize differences in movement organization between control and otoconia-deficient tilted mice under conditions with and without access to visual cues. Under completely dark conditions, tilted mice exhibited similar distance traveled and stop times overall, but had significantly more circuitous progressions, larger changes in heading between progressions, and less stable clustering of home bases, relative to control mice. In light conditions, control and tilted mice were similar on all measures except for the change in heading between progressions. This pattern of results is consistent with otoconia-deficient tilted mice using visual cues to compensate for impaired self-movement cue processing. This work provides the first empirical evidence that signals from the otolithic organs mediate the organization of exploratory behavior, based on a novel assessment of spatial orientation.

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“…cFos immunoreactivity was determined with a mean optical density method similar to previous studies (Köppen et al, 2016; Liu et al, 2001; Maken et al, 2010; Pan et al, 2009). Using ImageJ (National Institutes of Health, Bethesda, MD), a standardized oval shape (with the area of 0.083 mm 2 per hemisphere) was used to determine the density reading of the PVN.…”

Section: Methodsmentioning

confidence: 99%

Voluntary physical exercise protects against behavioral and endocrine reactivity to social and environmental stressors in the prairie vole

Watanasriyakul

Wardwell

McNeal

et al. 2017

Social Neuroscience

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Physical activity can combat detrimental effects of stress. The current study examined the potential protective effects of exercise against a combination of social isolation and chronic mild stress (CMS) in a prairie vole model. Female voles were isolated for 4 weeks, with the addition of CMS during the final 2 weeks. Half of the voles were allowed access to a running wheel during this final 2 weeks, while the other half remained sedentary. Animals underwent behavioral tests to assess depressive- and anxiety-behaviors. In a subset of animals, plasma was collected 10 minutes after behavioral testing for corticosterone analysis. In a separate subset, brains were collected 2 hours after behavioral testing for cFos analysis in the paraventricular nucleus (PVN). Voles in the exercise group displayed significantly lower depressive- and anxiety-behaviors, and displayed significantly lower corticosterone levels, compared to animals in the sedentary group. There was no difference in PVN cFos activity between groups. Interestingly, animals that moderately exercised displayed lower levels of depressive-behavior and attenuated corticosterone reactivity compared to animals in the low and high activity subgroups. These findings suggest that physical activity can protect against a combination of social and environmental stressors.

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Cholinergic deafferentation of the hippocampus causes non-temporally graded retrograde amnesia in an odor discrimination task

Cited by 10 publications

References 36 publications

Specific Phospholipid Modulation by Muscarinic Signaling in a Rat Lesion Model of Alzheimer’s Disease

Specific Phospholipid Modulation by Muscarinic Signaling in a Rat Lesion Model of Alzheimer’s Disease

Otolith dysfunction alters exploratory movement in mice

Voluntary physical exercise protects against behavioral and endocrine reactivity to social and environmental stressors in the prairie vole

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