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Article ; Online: Spatial Instability: The Paradox of Place Cell Remapping.

Muzzio, Isabel A

2018 Volume 28, Issue 22, Page(s) R1306–R1307

Abstract: How do memories persist stably over time when the spatial maps upon which they are constructed are unstable? New insights resolve this paradox by finding coherent structure in the instability of spatial maps arising from dynamic switches in reference ... ...

Abstract	How do memories persist stably over time when the spatial maps upon which they are constructed are unstable? New insights resolve this paradox by finding coherent structure in the instability of spatial maps arising from dynamic switches in reference frames.
MeSH term(s)	Hippocampus ; Memory ; Place Cells ; Temporal Lobe
Language	English
Publishing date	2018-11-19
Publishing country	England
Document type	Journal Article ; Comment
ZDB-ID	1071731-6
ISSN	1879-0445 ; 0960-9822
ISSN (online)	1879-0445
ISSN	0960-9822
DOI	10.1016/j.cub.2018.10.010
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Article ; Online: Therapeutic Delivery of Soluble Fractalkine Ameliorates Vascular Dysfunction in the Diabetic Retina.

Rodriguez, Derek / Church, Kaira A / Smith, Chelsea T / Vanegas, Difernando / Cardona, Sandra M / Muzzio, Isabel A / Nash, Kevin R / Cardona, Astrid E

International journal of molecular sciences

2024 Volume 25, Issue 3

Abstract: Diabetic retinopathy (DR)-associated vision loss is a devastating disease affecting the working-age population. Retinal pathology is due to leakage of serum components into retinal tissues, activation of resident phagocytes (microglia), and vascular and ... ...

Abstract	Diabetic retinopathy (DR)-associated vision loss is a devastating disease affecting the working-age population. Retinal pathology is due to leakage of serum components into retinal tissues, activation of resident phagocytes (microglia), and vascular and neuronal damage. While short-term interventions are available, they do not revert visual function or halt disease progression. The impact of microglial inflammatory responses on the neurovascular unit remains unknown. In this study, we characterized microglia-vascular interactions in an experimental model of DR. Early diabetes presents activated retinal microglia, vascular permeability, and vascular abnormalities coupled with vascular tortuosity and diminished astrocyte and endothelial cell-associated tight-junction (TJ) and gap-junction (GJ) proteins. Microglia exclusively bind to the neuronal-derived chemokine fractalkine (FKN) via the CX3CR1 receptor to ameliorate microglial activation. Using neuron-specific recombinant adeno-associated viruses (rAAVs), we therapeutically overexpressed soluble (sFKN) or membrane-bound (mFKN) FKN using intra-vitreal delivery at the onset of diabetes. This study highlights the neuroprotective role of rAAV-sFKN, reducing microglial activation, vascular tortuosity, fibrin(ogen) deposition, and astrogliosis and supporting the maintenance of the GJ connexin-43 (Cx43) and TJ zonula occludens-1 (ZO-1) molecules. The results also show that microglia-vascular interactions influence the vascular width upon administration of rAAV-sFKN and rAAV-mFKN. Administration of rAAV-sFKN improved visual function without affecting peripheral immune responses. These findings suggest that overexpression of rAAV-sFKN can mitigate vascular abnormalities by promoting glia-neural signaling. sFKN gene therapy is a promising translational approach to reverse vision loss driven by vascular dysfunction.
MeSH term(s)	Chemokine CX3CL1/pharmacology ; Chemokine CX3CL1/therapeutic use ; Diabetes Mellitus/metabolism ; Diabetic Retinopathy/drug therapy ; Diabetic Retinopathy/metabolism ; Microglia/metabolism ; Retina/metabolism ; Signal Transduction ; Diabetes Complications/drug therapy ; Animals ; Mice
Chemical Substances	Chemokine CX3CL1
Language	English
Publishing date	2024-01-31
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2019364-6
ISSN	1422-0067 ; 1422-0067 ; 1661-6596
ISSN (online)	1422-0067
ISSN	1422-0067 ; 1661-6596
DOI	10.3390/ijms25031727
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Article ; Online: Fractalkine isoforms differentially regulate microglia-mediated inflammation and enhance visual function in the diabetic retina.

Rodriguez, Derek / Church, Kaira A / Pietramale, Alicia N / Cardona, Sandra M / Vanegas, Difernando / Rorex, Colin / Leary, Micah C / Muzzio, Isabel A / Nash, Kevin R / Cardona, Astrid E

Journal of neuroinflammation

2024 Volume 21, Issue 1, Page(s) 42

Abstract: Diabetic retinopathy (DR) affects about 200 million people worldwide, causing leakage of blood components into retinal tissues, leading to activation of microglia, the resident phagocytes of the retina, promoting neuronal and vascular damage. The ... ...

Abstract	Diabetic retinopathy (DR) affects about 200 million people worldwide, causing leakage of blood components into retinal tissues, leading to activation of microglia, the resident phagocytes of the retina, promoting neuronal and vascular damage. The microglial receptor, CX3CR1, binds to fractalkine (FKN), an anti-inflammatory chemokine that is expressed on neuronal membranes (mFKN), and undergoes constitutive cleavage to release a soluble domain (sFKN). Deficiencies in CX3CR1 or FKN showed increased microglial activation, inflammation, vascular damage, and neuronal loss in experimental mouse models. To understand the mechanism that regulates microglia function, recombinant adeno-associated viral vectors (rAAV) expressing mFKN or sFKN were delivered to intact retinas prior to diabetes. High-resolution confocal imaging and mRNA-seq were used to analyze microglia morphology and markers of expression, neuronal and vascular health, and inflammatory mediators. We confirmed that prophylactic intra-vitreal administration of rAAV expressing sFKN (rAAV-sFKN), but not mFKN (rAAV-mFKN), in FKN
MeSH term(s)	Animals ; Humans ; Mice ; Chemokine CX3CL1/genetics ; Chemokine CX3CL1/metabolism ; CX3C Chemokine Receptor 1/genetics ; CX3C Chemokine Receptor 1/metabolism ; Diabetes Mellitus/metabolism ; Immunologic Factors ; Inflammation/metabolism ; Microglia/metabolism ; Protein Isoforms ; Retina/metabolism
Chemical Substances	Chemokine CX3CL1 ; CX3C Chemokine Receptor 1 ; Immunologic Factors ; Protein Isoforms ; Cx3cr1 protein, mouse ; Cx3cl1 protein, mouse
Language	English
Publishing date	2024-02-04
Publishing country	England
Document type	Journal Article
ZDB-ID	2156455-3
ISSN	1742-2094 ; 1742-2094
ISSN (online)	1742-2094
ISSN	1742-2094
DOI	10.1186/s12974-023-02983-8
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Article: Distinct neural mechanisms for heading retrieval and context recognition in the hippocampus during spatial reorientation.

Gagliardi, Celia M / Normandin, Marc E / Keinath, Alexandra T / Julian, Joshua B / Lopez, Matthew R / Ramos-Alvarez, Manuel-Miguel / Epstein, Russell A / Muzzio, Isabel A

Research square

2023

Abstract: Reorientation, the process of regaining one's bearings after becoming lost, requires identification of a spatial context (context recognition) and recovery of heading direction within that context (heading retrieval). We previously showed that these ... ...

Abstract	Reorientation, the process of regaining one's bearings after becoming lost, requires identification of a spatial context (context recognition) and recovery of heading direction within that context (heading retrieval). We previously showed that these processes rely on the use of features and geometry, respectively. Here, we examine reorientation behavior in a task that creates contextual ambiguity over a long timescale to demonstrate that mice learn to combine both featural and geometric cues to recover heading with experience. At the neural level, most CA1 neurons persistently align to geometry, and this alignment predicts heading behavior. However, a small subset of cells shows feature-sensitive place field remapping, which serves to predict context. Efficient heading retrieval and context recognition require integration of featural and geometric information in the active network through rate changes. These data illustrate how context recognition and heading retrieval are coded in CA1 and how these processes change with experience.
Language	English
Publishing date	2023-03-31
Publishing country	United States
Document type	Preprint
DOI	10.21203/rs.3.rs-2724785/v1
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Article ; Online: Navigable Space and Traversable Edges Differentially Influence Reorientation in Sighted and Blind Mice.

Normandin, Marc E / Garza, Maria C / Ramos-Alvarez, Manuel Miguel / Julian, Joshua B / Eresanara, Tuoyo / Punjaala, Nishanth / Vasquez, Juan H / Lopez, Matthew R / Muzzio, Isabel A

Psychological science

2022 Volume 33, Issue 6, Page(s) 925–947

Abstract: Reorientation enables navigators to regain their bearings after becoming lost. Disoriented individuals primarily reorient themselves using the geometry of a layout, even when other informative cues, such as landmarks, are present. Yet the specific ... ...

Abstract	Reorientation enables navigators to regain their bearings after becoming lost. Disoriented individuals primarily reorient themselves using the geometry of a layout, even when other informative cues, such as landmarks, are present. Yet the specific strategies that animals use to determine geometry are unclear. Moreover, because vision allows subjects to rapidly form precise representations of objects and background, it is unknown whether it has a deterministic role in the use of geometry. In this study, we tested sighted and congenitally blind mice (
MeSH term(s)	Animals ; Blindness ; Cues ; Humans ; Mathematics ; Mice ; Orientation ; Space Perception
Language	English
Publishing date	2022-05-10
Publishing country	United States
Document type	Journal Article ; Research Support, U.S. Gov't, Non-P.H.S. ; Research Support, N.I.H., Extramural
ZDB-ID	2022256-7
ISSN	1467-9280 ; 0956-7976
ISSN (online)	1467-9280
ISSN	0956-7976
DOI	10.1177/09567976211055373
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Article ; Online: Defibrinogenation Ameliorates Retinal Microgliosis and Inflammation in A CX3CR1-Independent Manner.

Sarker, Borna / Cardona, Sandra M / Church, Kaira A / Vanegas, Difernando / Velazquez, Priscila / Rorex, Colin / Rodriguez, Derek / Mendiola, Andrew S / Kern, Timothy S / Domingo, Nadia D / Stephens, Robin / Muzzio, Isabel A / Cardona, Astrid E

ASN neuro

2022 Volume 14, Page(s) 17590914221131446

Abstract: Summary statement: Diabetic human and murine retinas revealed pronounced microglial morphological activation and vascular abnormalities associated with inflammation. Pharmacological fibrinogen depletion using ancrod dampened microglial morphology ... ...

Abstract	Summary statement: Diabetic human and murine retinas revealed pronounced microglial morphological activation and vascular abnormalities associated with inflammation. Pharmacological fibrinogen depletion using ancrod dampened microglial morphology alterations, resolved fibrinogen accumulation, rescued axonal integrity, and reduced inflammation in the diabetic murine retina.
MeSH term(s)	Ancrod ; Animals ; CX3C Chemokine Receptor 1/genetics ; Fibrinogen ; Humans ; Inflammation/drug therapy ; Mice ; Microglia ; Retina/physiology
Chemical Substances	CX3C Chemokine Receptor 1 ; CX3CR1 protein, human ; Cx3cr1 protein, mouse ; Fibrinogen (9001-32-5) ; Ancrod (EC 3.4.21.-)
Language	English
Publishing date	2022-10-12
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	2485467-0
ISSN	1759-0914 ; 1759-0914
ISSN (online)	1759-0914
ISSN	1759-0914
DOI	10.1177/17590914221131446
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Article ; Online: Environmental Geometry Aligns the Hippocampal Map during Spatial Reorientation.

Keinath, Alex T / Julian, Joshua B / Epstein, Russell A / Muzzio, Isabel A

Current biology : CB

2017 Volume 27, Issue 3, Page(s) 309–317

Abstract: When a navigator's internal sense of direction is disrupted, she must rely on external cues to regain her bearings, a process termed spatial reorientation. Extensive research has demonstrated that the geometric shape of the environment exerts powerful ... ...

Abstract	When a navigator's internal sense of direction is disrupted, she must rely on external cues to regain her bearings, a process termed spatial reorientation. Extensive research has demonstrated that the geometric shape of the environment exerts powerful control over reorientation behavior, but the neural and cognitive mechanisms underlying this phenomenon are not well understood. Whereas some theories claim that geometry controls behavior through an allocentric mechanism potentially tied to the hippocampus, others postulate that disoriented navigators reach their goals by using an egocentric view-matching strategy. To resolve this debate, we characterized hippocampal representations during reorientation. We first recorded from CA1 cells as disoriented mice foraged in chambers of various shapes. We found that the alignment of the recovered hippocampal map was determined by the geometry of the chamber, but not by nongeometric cues, even when these cues could be used to disambiguate geometric ambiguities. We then recorded hippocampal activity as disoriented mice performed a classical goal-directed spatial memory task in a rectangular chamber. Again, we found that the recovered hippocampal map aligned solely to the chamber geometry. Critically, we also found a strong correspondence between the hippocampal map alignment and the animal's behavior, making it possible to predict the search location of the animal from neural responses on a trial-by-trial basis. Together, these results demonstrate that spatial reorientation involves the alignment of the hippocampal map to local geometry. We hypothesize that geometry may be an especially salient cue for reorientation because it is an inherently stable aspect of the environment.
MeSH term(s)	Animals ; Behavior, Animal/physiology ; CA1 Region, Hippocampal/anatomy & histology ; CA1 Region, Hippocampal/physiology ; Cues ; Discrimination (Psychology) ; Environment ; Mental Recall/physiology ; Mice ; Orientation/physiology ; Space Perception/physiology
Language	English
Publishing date	2017-01-12
Publishing country	England
Document type	Journal Article
ZDB-ID	1071731-6
ISSN	1879-0445 ; 0960-9822
ISSN (online)	1879-0445
ISSN	0960-9822
DOI	10.1016/j.cub.2016.11.046
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Article ; Online: Differential effect of sleep deprivation on place cell representations, sleep architecture, and memory in young and old mice.

Yuan, Robin K / Lopez, Matthew R / Ramos-Alvarez, Manuel-Miguel / Normandin, Marc E / Thomas, Arthur S / Uygun, David S / Cerda, Vanessa R / Grenier, Amandine E / Wood, Matthew T / Gagliardi, Celia M / Guajardo, Herminio / Muzzio, Isabel A

Cell reports

2021 Volume 35, Issue 11, Page(s) 109234

Abstract: Poor sleep quality is associated with age-related cognitive decline, and whether reversal of these alterations is possible is unknown. In this study, we report how sleep deprivation (SD) affects hippocampal representations, sleep patterns, and memory in ... ...

Abstract	Poor sleep quality is associated with age-related cognitive decline, and whether reversal of these alterations is possible is unknown. In this study, we report how sleep deprivation (SD) affects hippocampal representations, sleep patterns, and memory in young and old mice. After training in a hippocampus-dependent object-place recognition (OPR) task, control animals sleep ad libitum, although experimental animals undergo 5 h of SD, followed by recovery sleep. Young controls and old SD mice exhibit successful OPR memory, whereas young SD and old control mice are impaired. Successful performance is associated with two cellular phenotypes: (1) "context" cells, which remain stable throughout training and testing, and (2) "object configuration" cells, which remap when objects are introduced to the context and during testing. Additionally, effective memory correlates with spindle counts during non-rapid eye movement (NREM)/rapid eye movement (REM) sigma transitions. These results suggest SD may serve to ameliorate age-related memory deficits and allow hippocampal representations to adapt to changing environments.
MeSH term(s)	Aging/pathology ; Animals ; Bayes Theorem ; Behavior, Animal ; Corticosterone/blood ; Delta Rhythm/physiology ; Hippocampus/pathology ; Hippocampus/physiopathology ; Male ; Memory/physiology ; Mice, Inbred C57BL ; Place Cells/pathology ; Sleep/physiology ; Sleep Deprivation/blood ; Sleep Deprivation/physiopathology ; Task Performance and Analysis ; Theta Rhythm/physiology ; Mice
Chemical Substances	Corticosterone (W980KJ009P)
Language	English
Publishing date	2021-06-15
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	2649101-1
ISSN	2211-1247 ; 2211-1247
ISSN (online)	2211-1247
ISSN	2211-1247
DOI	10.1016/j.celrep.2021.109234
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Article ; Online: Role of the hippocampus in goal-oriented tasks requiring retrieval of spatial versus non-spatial information.

Levita, Liat / Muzzio, Isabel A

Neurobiology of learning and memory

2010 Volume 93, Issue 4, Page(s) 581–588

Abstract: The role of the hippocampus in non-spatial memory has been issue of some controversy. To investigate the nature of dorsal hippocampus engagement in spatial and non-spatial memory we performed discrete excitotoxic lesions of this region before mice (C57/ ... ...

Abstract	The role of the hippocampus in non-spatial memory has been issue of some controversy. To investigate the nature of dorsal hippocampus engagement in spatial and non-spatial memory we performed discrete excitotoxic lesions of this region before mice (C57/BL6) were trained in one of two tasks that required the animals to retrieve a hidden food reward. In the visuospatial task animals had to remember a particular spatial location, independent of odor cues. In contrast, in a non-spatial olfactory task animals had to remember a particular odor, independent of spatial location. The mice were trained in one of these tasks over a period of three days. We found that lesions restricted to the dorsal hippocampus affected performance only in the spatial task. In contrast, lesions that also encompassed a larger portion of the ventral hippocampus caused a moderate deficit in the olfactory task. These results are consistent with the role of the dorsal hippocampus in long-term spatial episodic memory, and support the involvement of larger portions of the hippocampus on the encoding of non-spatial olfactory representations.
MeSH term(s)	Animals ; Cues ; Executive Function/physiology ; Goals ; Hippocampus/drug effects ; Hippocampus/injuries ; Hippocampus/physiology ; Male ; Mental Recall/physiology ; Mice ; Mice, Inbred C57BL ; N-Methylaspartate/toxicity ; Neuropsychological Tests ; Neurotoxins/toxicity ; Olfactory Perception/physiology ; Reward ; Space Perception/physiology ; Visual Perception/physiology
Chemical Substances	Neurotoxins ; N-Methylaspartate (6384-92-5)
Language	English
Publishing date	2010-05
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	1223366-3
ISSN	1095-9564 ; 1074-7427
ISSN (online)	1095-9564
ISSN	1074-7427
DOI	10.1016/j.nlm.2010.02.006
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Article ; Online: Place recognition and heading retrieval are mediated by dissociable cognitive systems in mice.

Julian, Joshua B / Keinath, Alexander T / Muzzio, Isabel A / Epstein, Russell A

Proceedings of the National Academy of Sciences of the United States of America

2015 Volume 112, Issue 20, Page(s) 6503–6508

Abstract: A lost navigator must identify its current location and recover its facing direction to restore its bearings. We tested the idea that these two tasks--place recognition and heading retrieval--might be mediated by distinct cognitive systems in mice. ... ...

Abstract	A lost navigator must identify its current location and recover its facing direction to restore its bearings. We tested the idea that these two tasks--place recognition and heading retrieval--might be mediated by distinct cognitive systems in mice. Previous work has shown that numerous species, including young children and rodents, use the geometric shape of local space to regain their sense of direction after disorientation, often ignoring nongeometric cues even when they are informative. Notably, these experiments have almost always been performed in single-chamber environments in which there is no ambiguity about place identity. We examined the navigational behavior of mice in a two-chamber paradigm in which animals had to both recognize the chamber in which they were located (place recognition) and recover their facing direction within that chamber (heading retrieval). In two experiments, we found that mice used nongeometric features for place recognition, but simultaneously failed to use these same features for heading retrieval, instead relying exclusively on spatial geometry. These results suggest the existence of separate systems for place recognition and heading retrieval in mice that are differentially sensitive to geometric and nongeometric cues. We speculate that a similar cognitive architecture may underlie human navigational behavior.
MeSH term(s)	Analysis of Variance ; Animals ; Cognition/physiology ; Cues ; Male ; Mice ; Mice, Inbred C57BL ; Models, Psychological ; Orientation/physiology ; Recognition (Psychology)/physiology ; Spatial Navigation/physiology
Language	English
Publishing date	2015-05-19
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	209104-5
ISSN	1091-6490 ; 0027-8424
ISSN (online)	1091-6490
ISSN	0027-8424
DOI	10.1073/pnas.1424194112
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