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Article: Myeloid cell activation during Zika virus encephalitis predicts recovery of functional cortical connectivity.

Agner, Shannon C / Brier, Lindsey M / Hill, Jeremy / Liu, Ethan / Bice, Annie / Rahn, Rachel M / Culver, Joseph P / Klein, Robyn S

bioRxiv : the preprint server for biology

2023

Abstract: Neurologic complications of Zika virus (ZIKV) infection across the lifespan have been described during outbreaks in Southeast Asia, South America, and Central America since 2016. In the adult CNS ZIKV tropism for neurons is tightly linked to its effects, ...

Abstract	Neurologic complications of Zika virus (ZIKV) infection across the lifespan have been described during outbreaks in Southeast Asia, South America, and Central America since 2016. In the adult CNS ZIKV tropism for neurons is tightly linked to its effects, with neuronal loss within the hippocampus during acute infection and protracted synapse loss during recovery, which is associated with cognitive deficits. The effects of ZIKV on cortical networks have not been evaluated. Although animal behavior assays have been used previously to model cognitive impairment, in vivo brain imaging can provide orthogonal information regarding the health of brain networks in real time, providing a tool to translate findings in animal models to humans. In this study, we use widefield optical imaging to measure cortical functional connectivity (FC) in mice during acute infection with, and recovery from, intracranial infection with a mouse-adapted strain of ZIKV. Acute ZIKV infection leads to high levels of myeloid cell activation, with loss of neurons and presynaptic termini in the cerebral cortex and associated loss of FC primarily within the somatosensory cortex. During recovery, neuron numbers, synapses and FC recover to levels near those of healthy mice. However, hippocampal injury and impaired spatial cognition persist. The magnitude of activated myeloid cells during acute infection predicted both recovery of synapses and the degree of FC recovery after recovery from ZIKV infection. These findings suggest that a robust inflammatory response may contribute to the health of functional brain networks after recovery from infection.
Language	English
Publishing date	2023-07-06
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.07.06.547991
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Article ; Online: Oxytocin-induced birth causes sex-specific behavioral and brain connectivity changes in developing rat offspring.

Giri, Tusar / Maloney, Susan E / Giri, Saswat / Goo, Young Ah / Song, Jong Hee / Son, Minsoo / Tycksen, Eric / Conyers, Sara B / Bice, Annie / Ge, Xia / Garbow, Joel R / Quirk, James D / Bauer, Adam Q / Palanisamy, Arvind

iScience

2024 Volume 27, Issue 2, Page(s) 108960

Abstract: Despite six decades of the use of exogenous oxytocin for management of labor, little is known about its effects on the developing brain. Motivated by controversial reports suggesting a link between oxytocin use during labor and autism spectrum disorders ( ...

Abstract	Despite six decades of the use of exogenous oxytocin for management of labor, little is known about its effects on the developing brain. Motivated by controversial reports suggesting a link between oxytocin use during labor and autism spectrum disorders (ASDs), we employed our recently validated rat model for labor induction with oxytocin to address this important concern. Using a combination of molecular biological, behavioral, and neuroimaging assays, we show that induced birth with oxytocin leads to sex-specific disruption of oxytocinergic signaling in the developing brain, decreased communicative ability of pups, reduced empathy-like behaviors especially in male offspring, and widespread sex-dependent changes in functional cortical connectivity. Contrary to our hypothesis, social behavior, typically impaired in ASDs, was largely preserved. Collectively, our foundational studies provide nuanced insights into the neurodevelopmental impact of birth induction with oxytocin and set the stage for mechanistic investigations in animal models and prospective longitudinal clinical studies.
Language	English
Publishing date	2024-01-22
Publishing country	United States
Document type	Journal Article
ISSN	2589-0042
ISSN (online)	2589-0042
DOI	10.1016/j.isci.2024.108960
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Article ; Online: Visual Deprivation during Mouse Critical Period Reorganizes Network-Level Functional Connectivity.

Chen, Siyu / Rahn, Rachel M / Bice, Annie R / Bice, Seana H / Padawer-Curry, Jonah A / Hengen, Keith B / Dougherty, Joseph D / Culver, Joseph P

The Journal of neuroscience : the official journal of the Society for Neuroscience

2024 Volume 44, Issue 19

Abstract: A classic example of experience-dependent plasticity is ocular dominance (OD) shift, in which the responsiveness of neurons in the visual cortex is profoundly altered following monocular deprivation (MD). It has been postulated that OD shifts also modify ...

Abstract	A classic example of experience-dependent plasticity is ocular dominance (OD) shift, in which the responsiveness of neurons in the visual cortex is profoundly altered following monocular deprivation (MD). It has been postulated that OD shifts also modify global neural networks, but such effects have never been demonstrated. Here, we use wide-field fluorescence optical imaging (WFOI) to characterize calcium-based resting-state functional connectivity during acute (3 d) MD in female and male mice with genetically encoded calcium indicators (
MeSH term(s)	Animals ; Mice ; Male ; Female ; Sensory Deprivation/physiology ; Visual Cortex/physiology ; Nerve Net/physiology ; Mice, Inbred C57BL ; Neuronal Plasticity/physiology ; Dominance, Ocular/physiology ; Critical Period, Psychological ; Visual Pathways/physiology
Language	English
Publishing date	2024-05-08
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	604637-x
ISSN	1529-2401 ; 0270-6474
ISSN (online)	1529-2401
ISSN	0270-6474
DOI	10.1523/JNEUROSCI.1019-23.2024
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Zs.A 1668: Show issues

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Article ; Online: Functional network disorganization and cognitive decline following fractionated whole-brain radiation in mice.

Seitzman, Benjamin A / Reynoso, Francisco J / Mitchell, Timothy J / Bice, Annie R / Jarang, Anmol / Wang, Xiaodan / Mpoy, Cedric / Strong, Lori / Rogers, Buck E / Yuede, Carla M / Rubin, Joshua B / Perkins, Stephanie M / Bauer, Adam Q

GeroScience

2023 Volume 46, Issue 1, Page(s) 543–562

Abstract: Cognitive dysfunction following radiotherapy (RT) is one of the most common complications associated with RT delivered to the brain, but the precise mechanisms behind this dysfunction are not well understood, and to date, there are no preventative ... ...

Abstract	Cognitive dysfunction following radiotherapy (RT) is one of the most common complications associated with RT delivered to the brain, but the precise mechanisms behind this dysfunction are not well understood, and to date, there are no preventative measures or effective treatments. To improve patient outcomes, a better understanding of the effects of radiation on the brain's functional systems is required. Functional magnetic resonance imaging (fMRI) has shown promise in this regard, however, compared to neural activity, hemodynamic measures of brain function are slow and indirect. Understanding how RT acutely and chronically affects functional brain organization requires more direct examination of temporally evolving neural dynamics as they relate to cerebral hemodynamics for bridging with human studies. In order to adequately study the underlying mechanisms of RT-induced cognitive dysfunction, the development of clinically mimetic RT protocols in animal models is needed. To address these challenges, we developed a fractionated whole-brain RT protocol (3Gy/day for 10 days) and applied longitudinal wide field optical imaging (WFOI) of neural and hemodynamic brain activity at 1, 2, and 3 months post RT. At each time point, mice were subject to repeated behavioral testing across a variety of sensorimotor and cognitive domains. Disruptions in cortical neuronal and hemodynamic activity observed 1 month post RT were significantly worsened by 3 months. While broad changes were observed in functional brain organization post RT, brain regions most impacted by RT occurred within those overlapping with the mouse default mode network and other association areas similar to prior reports in human subjects. Further, significant cognitive deficits were observed following tests of novel object investigation and responses to auditory and contextual cues after fear conditioning. Our results fill a much-needed gap in understanding the effects of whole-brain RT on systems level brain organization and how RT affects neuronal versus hemodynamic signaling in the cortex. Having established a clinically-relevant injury model, future studies can examine therapeutic interventions designed to reduce neuroinflammation-based injury following RT. Given the overlap of sequelae that occur following RT with and without chemotherapy, these tools can also be easily incorporated to examine chemotherapy-related cognitive impairment.
MeSH term(s)	Humans ; Mice ; Animals ; Brain/pathology ; Cognitive Dysfunction ; Brain Mapping ; Magnetic Resonance Imaging/methods ; Cognition Disorders/etiology
Language	English
Publishing date	2023-09-25
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2886586-8
ISSN	2509-2723 ; 2509-2715
ISSN (online)	2509-2723
ISSN	2509-2715
DOI	10.1007/s11357-023-00944-w
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Zs.A 1502: Show issues

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Article ; Online: Mecp2 deletion results in profound alterations of developmental and adult functional connectivity.

Rahn, Rachel M / Yen, Allen / Chen, Siyu / Gaines, Seana H / Bice, Annie R / Brier, Lindsey M / Swift, Raylynn G / Lee, LeiLani / Maloney, Susan E / Culver, Joseph P / Dougherty, Joseph D

Cerebral cortex (New York, N.Y. : 1991)

2023 Volume 33, Issue 12, Page(s) 7436–7453

Abstract: As a regressive neurodevelopmental disorder with a well-established genetic cause, Rett syndrome and its Mecp2 loss-of-function mouse model provide an excellent opportunity to define potentially translatable functional signatures of disease progression, ... ...

Abstract	As a regressive neurodevelopmental disorder with a well-established genetic cause, Rett syndrome and its Mecp2 loss-of-function mouse model provide an excellent opportunity to define potentially translatable functional signatures of disease progression, as well as offer insight into the role of Mecp2 in functional circuit development. Thus, we applied widefield optical fluorescence imaging to assess mesoscale calcium functional connectivity (FC) in the Mecp2 cortex both at postnatal day (P)35 in development and during the disease-related decline. We found that FC between numerous cortical regions was disrupted in Mecp2 mutant males both in juvenile development and early adulthood. Female Mecp2 mice displayed an increase in homotopic contralateral FC in the motor cortex at P35 but not in adulthood, where instead more posterior parietal regions were implicated. An increase in the amplitude of connection strength, both with more positive correlations and more negative anticorrelations, was observed across the male cortex in numerous functional regions. Widespread rescue of MeCP2 protein in GABAergic neurons rescued none of these functional deficits, nor, surprisingly, the expected male lifespan. Altogether, the female results identify early signs of disease progression, while the results in males indicate MeCP2 protein is required for typical FC in the brain.
MeSH term(s)	Male ; Female ; Mice ; Animals ; Methyl-CpG-Binding Protein 2/genetics ; Rett Syndrome/genetics ; Rett Syndrome/metabolism ; Brain ; GABAergic Neurons/physiology ; Disease Models, Animal ; Mice, Inbred C57BL
Chemical Substances	Methyl-CpG-Binding Protein 2 ; Mecp2 protein, mouse
Language	English
Publishing date	2023-03-10
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	1077450-6
ISSN	1460-2199 ; 1047-3211
ISSN (online)	1460-2199
ISSN	1047-3211
DOI	10.1093/cercor/bhad050
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Zs.A 3235: Show issues

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Article: Visual deprivation during mouse critical period reorganizes network-level functional connectivity.

Chen, Siyu / Rahn, Rachel M / Bice, Annie R / Bice, Seana H / Padawer-Curry, Jonah A / Hengen, Keith B / Dougherty, Joseph D / Culver, Joseph P

bioRxiv : the preprint server for biology

2023

Abstract	A classic example of experience-dependent plasticity is ocular dominance (OD) shift, in which the responsiveness of neurons in the visual cortex is profoundly altered following monocular deprivation (MD). It has been postulated that OD shifts also modify global neural networks, but such effects have never been demonstrated. Here, we used longitudinal wide-field optical calcium imaging to measure resting-state functional connectivity during acute (3-day) MD in mice. First, delta GCaMP6 power in the deprived visual cortex decreased, suggesting that excitatory activity was reduced in the region. In parallel, interhemispheric visual homotopic functional connectivity was rapidly reduced by the disruption of visual drive through MD and was sustained significantly below baseline state. This reduction of visual homotopic connectivity was accompanied by a reduction in parietal and motor homotopic connectivity. Finally, we observed enhanced internetwork connectivity between visual and parietal cortex that peaked at MD2. Together, these findings support the hypothesis that early MD induces dynamic reorganization of disparate functional networks including association cortices.
Language	English
Publishing date	2023-12-09
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.05.30.542957
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Article ; Online: Functional Connectivity of the Developing Mouse Cortex.

Rahn, Rachel M / Brier, Lindsey M / Bice, Annie R / Reisman, Matthew D / Dougherty, Joseph D / Culver, Joseph P

Cerebral cortex (New York, N.Y. : 1991)

2021 Volume 32, Issue 8, Page(s) 1755–1768

Abstract: Cross-sectional studies have established a variety of structural, synaptic, and cell physiological changes corresponding to critical periods in cortical development. However, the emergence of functional connectivity (FC) in development has not been fully ...

Abstract	Cross-sectional studies have established a variety of structural, synaptic, and cell physiological changes corresponding to critical periods in cortical development. However, the emergence of functional connectivity (FC) in development has not been fully characterized, and hemodynamic-based measures are vulnerable to any neurovascular coupling changes occurring in parallel. We therefore used optical fluorescence imaging to trace longitudinal calcium FC in the awake, resting-state mouse cortex at 5 developmental timepoints beginning at postnatal day 15 (P15) and ending in early adulthood at P60. Calcium FC displayed coherent functional maps as early as P15, and FC significantly varied in connections between many regions across development, with the developmental trajectory's shape specific to the functional region. Evaluating 325 seed-seed connections, we found that there was a significant increase in FC between P15 and P22 over the majority of the cortex as well as bilateral connectivity and node degree differences in frontal, motor, and retrosplenial cortices after P22. A rebalancing of inter- and intrahemispheric FC and local-distal FC dominance was also observed during development. This longitudinal developmental calcium FC study therefore provides a resource dataset to the field and identifies periods of dynamic change which cross-sectional studies may target for examination of disease states.
MeSH term(s)	Animals ; Calcium ; Cerebral Cortex/diagnostic imaging ; Cross-Sectional Studies ; Gyrus Cinguli ; Magnetic Resonance Imaging ; Mice ; Neurovascular Coupling/physiology
Chemical Substances	Calcium (SY7Q814VUP)
Language	English
Publishing date	2021-09-01
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	1077450-6
ISSN	1460-2199 ; 1047-3211
ISSN (online)	1460-2199
ISSN	1047-3211
DOI	10.1093/cercor/bhab312
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Zs.A 3235: Show issues

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Article ; Online: A Multivariate Functional Connectivity Approach to Mapping Brain Networks and Imputing Neural Activity in Mice.

Brier, Lindsey M / Zhang, Xiaohui / Bice, Annie R / Gaines, Seana H / Landsness, Eric C / Lee, Jin-Moo / Anastasio, Mark A / Culver, Joseph P

Cerebral cortex (New York, N.Y. : 1991)

2021 Volume 32, Issue 8, Page(s) 1593–1607

Abstract: Temporal correlation analysis of spontaneous brain activity (e.g., Pearson "functional connectivity," FC) has provided insights into the functional organization of the human brain. However, bivariate analysis techniques such as this are often susceptible ...

Abstract	Temporal correlation analysis of spontaneous brain activity (e.g., Pearson "functional connectivity," FC) has provided insights into the functional organization of the human brain. However, bivariate analysis techniques such as this are often susceptible to confounding physiological processes (e.g., sleep, Mayer-waves, breathing, motion), which makes it difficult to accurately map connectivity in health and disease as these physiological processes affect FC. In contrast, a multivariate approach to imputing individual neural networks from spontaneous neuroimaging data could be influential to our conceptual understanding of FC and provide performance advantages. Therefore, we analyzed neural calcium imaging data from Thy1-GCaMP6f mice while either awake, asleep, anesthetized, during low and high bouts of motion, or before and after photothrombotic stroke. A linear support vector regression approach was used to determine the optimal weights for integrating the signals from the remaining pixels to accurately predict neural activity in a region of interest (ROI). The resultant weight maps for each ROI were interpreted as multivariate functional connectivity (MFC), resembled anatomical connectivity, and demonstrated a sparser set of strong focused positive connections than traditional FC. While global variations in data have large effects on standard correlation FC analysis, the MFC mapping methods were mostly impervious. Lastly, MFC analysis provided a more powerful connectivity deficit detection following stroke compared to traditional FC.
MeSH term(s)	Animals ; Brain/diagnostic imaging ; Brain/physiology ; Brain Mapping/methods ; Magnetic Resonance Imaging/methods ; Mice ; Neural Pathways/diagnostic imaging ; Neural Pathways/physiology ; Stroke/diagnostic imaging ; Wakefulness
Language	English
Publishing date	2021-09-15
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural
ZDB-ID	1077450-6
ISSN	1460-2199 ; 1047-3211
ISSN (online)	1460-2199
ISSN	1047-3211
DOI	10.1093/cercor/bhab282
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Article: Evaluation of gliovascular functions of Aqp4 readthrough isoforms.

Mueller, Shayna M / White, Kelli McFarland / Fass, Stuart B / Chen, Siyu / Shi, Zhan / Ge, Xia / Engelbach, John A / Gaines, Seana H / Bice, Annie R / Vasek, Michael J / Garbow, Joel R / Culver, Joseph P / Zila Martinez-Lozada / Cohen-Salmon, Martine / Dougherty, Joseph D / Sapkota, Darshan

bioRxiv : the preprint server for biology

2023

Abstract: Aquaporin-4 (AQP4) is a water channel protein that links astrocytic endfeet to the blood-brain barrier (BBB) and regulates water and potassium homeostasis in the brain, as well as the glymphatic clearance of waste products that would otherwise potentiate ...

Abstract	Aquaporin-4 (AQP4) is a water channel protein that links astrocytic endfeet to the blood-brain barrier (BBB) and regulates water and potassium homeostasis in the brain, as well as the glymphatic clearance of waste products that would otherwise potentiate neurological diseases. Recently, translational readthrough was shown to generate a C-terminally extended variant of AQP4, known as AQP4x, that preferentially localizes around the BBB through interaction with the scaffolding protein α-syntrophin, and loss of AQP4x disrupts waste clearance from the brain. To investigate the function of AQP4x, we generated a novel mouse AQP4 line (AllX) to increase relative levels of the readthrough variant above the ~15% of AQP4 in the brain of wildtype (WT) mice. We validated the line and assessed characteristics that are affected by the presence of AQP4x, including AQP4 and α-syntrophin localization, integrity of the BBB, and neurovascular coupling. We compared AllX
Language	English
Publishing date	2023-07-25
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.07.21.549379
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Article: Evaluation of gliovascular functions of AQP4 readthrough isoforms.

Mueller, Shayna M / McFarland White, Kelli / Fass, Stuart B / Chen, Siyu / Shi, Zhan / Ge, Xia / Engelbach, John A / Gaines, Seana H / Bice, Annie R / Vasek, Michael J / Garbow, Joel R / Culver, Joseph P / Martinez-Lozada, Zila / Cohen-Salmon, Martine / Dougherty, Joseph D / Sapkota, Darshan

Frontiers in cellular neuroscience

2023 Volume 17, Page(s) 1272391

Abstract: Aquaporin-4 (AQP4) is a water channel protein that links the astrocytic endfeet to the blood-brain barrier (BBB) and regulates water and potassium homeostasis in the brain, as well as the glymphatic clearance of waste products that would otherwise ... ...

Abstract	Aquaporin-4 (AQP4) is a water channel protein that links the astrocytic endfeet to the blood-brain barrier (BBB) and regulates water and potassium homeostasis in the brain, as well as the glymphatic clearance of waste products that would otherwise potentiate neurological diseases. Recently, translational readthrough was shown to generate a C-terminally extended variant of AQP4, known as AQP4x, which preferentially localizes around the BBB through interaction with the scaffolding protein α-syntrophin, and loss of AQP4x disrupts waste clearance from the brain. To investigate the function of AQP4x, we generated a novel AQP4 mouse line (AllX) to increase relative levels of the readthrough variant above the ~15% of AQP4 in the brain of wild-type (WT) mice. We validated the line and assessed characteristics that are affected by the presence of AQP4x, including AQP4 and α-syntrophin localization, integrity of the BBB, and neurovascular coupling. We compared AllX
Language	English
Publishing date	2023-11-23
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2452963-1
ISSN	1662-5102
ISSN	1662-5102
DOI	10.3389/fncel.2023.1272391
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