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Functional ultrasound imaging of recent and remote memory recall in the associative fear neural network in mice

View ORCID ProfileGillian Grohs-Metz, View ORCID ProfileRebecca Smausz, View ORCID ProfileJohn Gigg, View ORCID ProfileTobias Boeckers, View ORCID ProfileBastian Hengerer
doi: https://doi.org/10.1101/2021.11.13.468469
Gillian Grohs-Metz
1CNS Discovery Research, Boehringer Ingelheim Pharma GmbH & Co. KG, Biberach an der Riss, Germany
2Institute of Anatomy and Cell Biology, University of Ulm, Ulm, Germany
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  • ORCID record for Gillian Grohs-Metz
Rebecca Smausz
1CNS Discovery Research, Boehringer Ingelheim Pharma GmbH & Co. KG, Biberach an der Riss, Germany
3Division of Neuroscience and Experimental Psychology, University of Manchester, Manchester, UK
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John Gigg
3Division of Neuroscience and Experimental Psychology, University of Manchester, Manchester, UK
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Tobias Boeckers
2Institute of Anatomy and Cell Biology, University of Ulm, Ulm, Germany
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Bastian Hengerer
1CNS Discovery Research, Boehringer Ingelheim Pharma GmbH & Co. KG, Biberach an der Riss, Germany
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  • For correspondence: Bastian.Hengerer@boehringer-ingelheim.com
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Scientific Abstract

Emotional learning and memory are affected in numerous psychiatric disorders. At a systems level, however, the underlying neural circuitry is not well defined. Rodent fear conditioning (FC) provides a translational model to study the networks underlying associative memory retrieval. In the current study, functional connectivity among regions related to the cue associative fear network were investigated using functional ultrasound (fUS), a novel imaging technique with great potential for detecting regional neural activity through cerebral blood flow. Behavioral fear expression and fUS imaging were performed one and thirty-one days after FC to assess recent and remote memory recall. Cue-evoked increases in functional connectivity were detected throughout the amygdala, with the lateral (LA) and central (CeA) amygdalar nuclei emerging as major hubs of connectivity, though CeA connectivity was reduced during remote recall. The hippocampus and sensory cortical regions displayed heightened connectivity with the LA during remote recall, whereas interconnectivity between the primary auditory cortex and temporal association areas was reduced. Subregions of the prefrontal cortex exhibited variable connectivity changes, where prelimbic connectivity with the amygdala was refined while specific connections between the infralimbic cortex and amygdalar subregions emerged during remote memory retrieval. Moreover, freezing behavior positively correlated with functional connectivity between hubs of the associative fear network, suggesting that emotional response intensity reflected the strength of the cue-evoked functional network. Overall, our data provide evidence of the functionality of fUS imaging to investigate the neural dynamics of memory encoding and retrieval, applicable in the development of innovative treatments for affective disorders.

Highlights Functional ultrasound imaging can elucidate fear associated neural networks

Freezing behavior correlates with cue-evoked functional connectivity changes

The lateral and central amygdalar nuclei are major hubs in the fear network

The hippocampus is active during recent and remote cued fear memory retrieval

Connectivity profiles of the prelimbic and infralimbic areas vary in remote recall

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted November 30, 2021.
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Functional ultrasound imaging of recent and remote memory recall in the associative fear neural network in mice
Gillian Grohs-Metz, Rebecca Smausz, John Gigg, Tobias Boeckers, Bastian Hengerer
bioRxiv 2021.11.13.468469; doi: https://doi.org/10.1101/2021.11.13.468469
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Functional ultrasound imaging of recent and remote memory recall in the associative fear neural network in mice
Gillian Grohs-Metz, Rebecca Smausz, John Gigg, Tobias Boeckers, Bastian Hengerer
bioRxiv 2021.11.13.468469; doi: https://doi.org/10.1101/2021.11.13.468469

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