Evolution of brain-wide activity in the awake behaving mouse after acute fear by longitudinal manganese-enhanced MRI

Uselman, Taylor W.; Barto, Daniel; Jacobs, Russell E.; Bearer, Elaine L.

doi:10.1016/j.neuroimage.2020.116975

Cited by 13 publications

(74 citation statements)

References 147 publications

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“…Caution must be taken in older mice as there is some suggestion that age may increase vulnerability to the side effects of Mn(II), as it also increases Mn(II) uptake in the hippocampus 99 . At least one transgenic, SERT‐KO, is more vulnerable to systemic Mn(II) 18 . Care also must be taken to monitor dosage, by observing effects on cardiac function, behavior, weight, and even electrophysiology in the living animal, as well as postmortem histology after stereotactic injections looking for inflammation and necrosis.…”

Section: Manganese Propertiesmentioning

confidence: 99%

“…These properties allow longitudinal imaging of the same individual over time, either at short or long intervals. Importantly, knowledge of both individual and of group averages can also be obtained, provided residual Mn(II) is accounted for 17–20 . Together with computational processing and statistical analysis, longitudinal imaging of neural activity will illuminate the influences of drugs, experience, genetics or disease progression on the brain.…”

Section: Introductionmentioning

confidence: 99%

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Longitudinal manganese‐enhanced magnetic resonance imaging of neural projections and activity

et al. 2022

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Manganese-enhanced magnetic resonance imaging (MEMRI) holds exceptional promise for preclinical studies of brain-wide physiology in awake-behaving animals. The objectives of this review are to update the current information regarding MEMRI and to inform new investigators as to its potential. Mn(II) is a powerful contrast agent for two main reasons: (1) high signal intensity at low doses; and (2) biological interactions, such as projection tracing and neural activity mapping via entry into electrically active neurons in the living brain. High-spin Mn(II) reduces the relaxation time of water protons: at Mn(II) concentrations typically encountered in MEMRI, robust hyperintensity is obtained without adverse effects. By selectively entering neurons through voltagegated calcium channels, Mn(II) highlights active neurons. Safe doses may be repeated over weeks to allow for longitudinal imaging of brain-wide dynamics in the same individual across time. When delivered by stereotactic intracerebral injection, Mn(II) enters active neurons at the injection site and then travels inside axons for long distances, tracing neuronal projection anatomy. Rates of axonal transport within the brain were measured for the first time in "time-lapse" MEMRI. When delivered systemically, Mn(II) enters active neurons throughout the brain via voltage-sensitive calcium channels and clears slowly. Thus behavior can be monitored during Mn(II) uptake and hyperintense signals due to Mn(II) uptake captured retrospectively, allowing pairing of behavior with neural activity maps for the first time. Here we review critical information gained from MEMRI projection mapping about human

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Section: Manganese Propertiesmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Longitudinal manganese‐enhanced magnetic resonance imaging of neural projections and activity

et al. 2022

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“…Although traditional functional magnetic resonance imaging (MRI) allows in vivo analysis, its ability to detect dynamic transmission is limited. Manganese-enhanced magnetic resonance imaging (MEMRI) has been proven to be a valuable method for noninvasive assessment of axonal transport in vivo(Almeida-Corrêa et al 2018; Uselman et al 2020;Yang et al 2020). The mechanism behind MEMRI involves the ability of Mn 2+ , a paramagnetic substance, to shorten the T1 relaxation time, making it to appear as a strong signal in T1-weighted (T1W) images (Lin et al 1997).…”

Section: Introductionmentioning

confidence: 99%

Detection of heroin addiction- and relapse-induced axonal transport dysfunction in the brain in vivo by MRI

Yang

Luo

Liao

et al. 2022

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Purpose Heroin is a highly addictive drug that causes axonal damage. Here, manganese-enhanced magnetic resonance imaging (MEMRI) was used to dynamically monitor axonal transport in different stages after heroin addiction.Methods Rodent models of heroin addiction (HA) and heroin relapse (HR) were established by injection of different doses of heroin solution at different times. Heroin-induced learning and memory deficits were evaluated by the Morris water maze (MWM). MEMRI was used to dynamically evaluate axonal transport through the olfactory pathway. The expression of proteins related to axonal structure and function were assessed by western blotting. Transmission electron microscopy (TEM) was used to observe ultrastructural changes. Neurofilament heavy chain (NF-H) protein levels were analyzed by immunofluorescence staining.Result HA model rats and especially HR model rats showed worse spatial learning and memory abilities than control rats. Compared with HA model rats and control rats, HR model rats exhibited a significant increase in escape latency and significant decreases in the number of platform location crossings and time spent in the target quadrant. Mn2+ transport was accelerated in HA model rats. HR model rats exhibited a severely insufficient capacity for Mn2+ transport, and the axonal transport rate (ATR) was significantly reduced in these rats compared to control rats (P<0.001). The levels of cytoplasmic dynein and KIF5 in rats in the HR group were significantly decreased (P<0.001), and the levels of energy-related proteins, including COX IV and ATPB, were lower in the HR group than the control group (P<0.001). The brains of heroin-exposed rats showed an abnormal ultrastructure, exhibiting neuronal apoptosis and mitochondrial dysfunction. Heroin decreased the expression of NF-H, with the staining intensity being significantly reduced in tissues from HA and HR model rats (P<0.05).Conclusion MEMRI can detect axonal transport dysfunction caused by long-term repeated exposure to heroin, and decreases in the levels of motor proteins and mitochondrial dysfunction may be the main causes of this axonal transport impairment. Thus, the study shows that MEMRI is a potential tool for visualizing axonal transport in individuals experiencing drug addiction, providing a new direction for the evaluation of addictive drug withdrawal.

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“…Uselman et al (2020) used manganese-enhanced MRI to analyze innate fear response to predator odor. In the only other study using PET imaging associated with auditory fear conditioning,Luyten et al (2012) focused their analysis on the neurocircuitry of contextual anxiety.…”

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confidence: 99%

PET Metabolic Imaging of Time-Dependent Reorganization of Olfactory Cued Fear Memory Networks in Rats

et al. 2021

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Memory consolidation involves reorganization at both the synaptic and system levels.The latter involves gradual reorganization of the brain regions that support memory and has been mostly highlighted using hippocampal-dependent tasks. The standard memory consolidation model posits that the hippocampus becomes gradually less important over time in favor of neocortical regions. By contrast, this reorganization of circuits in amygdala-dependent tasks has been less investigated. Moreover, this question has been addressed using primarily lesion or cellular imaging approaches thus precluding the comparison of recent and remote memory networks in the same animals. To overcome this limitation, we used microPET imaging to characterize, in the same animals, the networks activated during the recall of a recent vs remote memory in an olfactory cued fear conditioning paradigm. The data highlighted the drastic difference between the extent of the two networks. Indeed, while the recall of a recent odor fear memory activates a large network of structures spanning from the prefrontal cortex to the cerebellum, significant activations during remote memory retrieval are limited to the piriform cortex. These results strongly support the view that amygdala-dependent memories also undergo system-level reorganization, and that sensory cortical areas might participate in the long-term storage of emotional memories.

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Evolution of brain-wide activity in the awake behaving mouse after acute fear by longitudinal manganese-enhanced MRI

Cited by 13 publications

References 147 publications

Longitudinal manganese‐enhanced magnetic resonance imaging of neural projections and activity

Longitudinal manganese‐enhanced magnetic resonance imaging of neural projections and activity

Detection of heroin addiction- and relapse-induced axonal transport dysfunction in the brain in vivo by MRI

PET Metabolic Imaging of Time-Dependent Reorganization of Olfactory Cued Fear Memory Networks in Rats

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