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Article: Dominance hierarchy regulates social behavior during spatial movement.

Lara-Vasquez, Ariel / Espinosa, Nelson / Morales, Cristian / Moran, Constanza / Billeke, Pablo / Gallagher, Joseph / Strohl, Joshua J / Huerta, Patricio T / Fuentealba, Pablo

Frontiers in neuroscience

2024 Volume 18, Page(s) 1237748

Abstract: Rodents establish dominance hierarchy as a social ranking system in which one subject acts as dominant over all the other subordinate individuals. Dominance hierarchy regulates food access and mating opportunities, but little is known about its ... ...

Abstract	Rodents establish dominance hierarchy as a social ranking system in which one subject acts as dominant over all the other subordinate individuals. Dominance hierarchy regulates food access and mating opportunities, but little is known about its significance in other social behaviors, for instance during collective navigation for foraging or migration. Here, we implemented a simplified goal-directed spatial task in mice, in which animals navigated individually or collectively with their littermates foraging for food. We compared between conditions and found that the social condition exerts significant influence on individual displacement patterns, even when efficient navigation rules leading to reward had been previously learned. Thus, movement patterns and consequent task performance were strongly dependent on contingent social interactions arising during collective displacement, yet their influence on individual behavior was determined by dominance hierarchy. Dominant animals did not behave as leaders during collective displacement; conversely, they were most sensitive to the social environment adjusting their performance accordingly. Social ranking in turn was associated with specific spontaneous neural activity patterns in the prefrontal cortex and hippocampus, with dominant mice showing higher firing rates, larger ripple oscillations, and stronger neuronal entrainment by ripples than subordinate animals. Moreover, dominant animals selectively increased their cortical spiking activity during collective movement, while subordinate mice did not modify their firing rates, consistent with dominant animals being more sensitive to the social context. These results suggest that dominance hierarchy influences behavioral performance during contingent social interactions, likely supported by the coordinated activity in the hippocampal-prefrontal circuit.
Language	English
Publishing date	2024-02-07
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2411902-7
ISSN	1662-453X ; 1662-4548
ISSN (online)	1662-453X
ISSN	1662-4548
DOI	10.3389/fnins.2024.1237748
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Article: Intrinsic diving reflex induces potent antioxidative response by activation of NRF2 signaling.

Powell, Keren / Wadolowski, Steven / Tambo, Willians / Strohl, Joshua J / Kim, Daniel / Turpin, Justin / Al-Abed, Yousef / Brines, Michael / Huerta, Patricio T / Li, Chunyan

bioRxiv : the preprint server for biology

2024

Abstract: Aims: This study aims to elucidate the underlying mechanisms of diving reflex, a powerful endogenous mechanism supporting underwater mammalian survival. Antioxidative responses, observed in marine mammals, may be contributing factors. Using a multi- ... ...

Abstract	Aims: This study aims to elucidate the underlying mechanisms of diving reflex, a powerful endogenous mechanism supporting underwater mammalian survival. Antioxidative responses, observed in marine mammals, may be contributing factors. Using a multi-organ approach, this study assesses whether acute and chronic diving reflex activate nuclear factor-erythroid-2-related factor 2 (NRF2) signaling pathways, which regulate cellular antioxidant responses. Methods: Male Sprague-Dawley rats ( Results: Diving reflex increased nuclear NRF2, phosphorylated NRF2, and antioxidative gene expression, in an organ-specific and exposure time-specific manner. Comparing organs, the brain had the highest increase of phosphorylated NRF2 expression, while kidney had the highest degree of nuclear NRF2 expression. Comparing acute and chronic sessions, phosphorylated NRF2 increased the most with chronic diving reflex, but acute diving reflex had the highest antioxidative gene expression. Notably, calcitonin gene-related peptide appears to mediate diving reflex' effects on NRF2 activation. Conclusions: Acute and chronic diving reflex activate potent NRF2 signaling in the brain and peripheral organs. Interestingly, acute diving reflex induces higher expression of downstream antioxidative genes compared to chronic diving reflex. This result contradicts previous assumptions requiring chronic exposure to diving for induction of antioxidative effects and implies that the diving reflex has a strong translational potential during preconditioning and postconditioning therapies. Key points: Diving reflex activates potent NRF2 signaling via multiple mechanisms, including phosphorylation, nuclear translocation, and KEAP1 downregulation with both acute and chronic exposure.Diving reflex activates NRF2 via differential pathways in the brain and other organs; phosphorylated NRF2 increases more in the brain, while nuclear NRF2 increases more in the peripheral organs.Acute diving reflex exposure induces a more pronounced antioxidative effect than chronic diving reflex exposure, indicating that the antioxidative response activated by diving reflex is not dependent upon chronic adaptive responses and supports diving reflex as both a preconditioning and postconditioning treatment.
Language	English
Publishing date	2024-02-13
Publishing country	United States
Document type	Preprint
DOI	10.1101/2024.02.12.579910
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Article: Contributions of Sex Chromosomes and Gonadal Hormones to the Male Bias in a Maternal Antibody-Induced Model of Autism Spectrum Disorder.

Gata-Garcia, Adriana / Porat, Amit / Brimberg, Lior / Volpe, Bruce T / Huerta, Patricio T / Diamond, Betty

Frontiers in neurology

2021 Volume 12, Page(s) 721108

Abstract: Autism Spectrum Disorder (ASD) is a group of neurodevelopmental conditions that is four times more commonly diagnosed in males than females. While susceptibility genes located in the sex chromosomes have been identified in ASD, it is unclear whether they ...

Abstract	Autism Spectrum Disorder (ASD) is a group of neurodevelopmental conditions that is four times more commonly diagnosed in males than females. While susceptibility genes located in the sex chromosomes have been identified in ASD, it is unclear whether they are sufficient to explain the male bias or whether gonadal hormones also play a key role. We evaluated the sex chromosomal and hormonal influences on the male bias in a murine model of ASD, in which mice are exposed
Language	English
Publishing date	2021-10-13
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2564214-5
ISSN	1664-2295
ISSN	1664-2295
DOI	10.3389/fneur.2021.721108
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Article ; Online: Framework for automated sorting of neural spikes from Neuralynx-acquired tetrode recordings in freely-moving mice.

Strohl, Joshua J / Gallagher, Joseph T / Gómez, Pedro N / Glynn, Joshua M / Huerta, Patricio T

Bioelectronic medicine

2021 Volume 7, Issue 1, Page(s) 17

Abstract: ... from the prelimbic cortex, a region of the medial prefrontal cortex, while the mice are tested in a T maze ...

Abstract	Background: Extracellular recording represents a crucial electrophysiological technique in neuroscience for studying the activity of single neurons and neuronal populations. The electrodes capture voltage traces that, with the help of analytical tools, reveal action potentials ('spikes') as well as local field potentials. The process of spike sorting is used for the extraction of action potentials generated by individual neurons. Until recently, spike sorting was performed with manual techniques, which are laborious and unreliable due to inherent operator bias. As neuroscientists add multiple electrodes to their probes, the high-density devices can record hundreds to thousands of neurons simultaneously, making the manual spike sorting process increasingly difficult. The advent of automated spike sorting software has offered a compelling solution to this issue and, in this study, we present a simple-to-execute framework for running an automated spike sorter. Methods: Tetrode recordings of freely-moving mice are obtained from the CA1 region of the hippocampus as they navigate a linear track. Tetrode recordings are also acquired from the prelimbic cortex, a region of the medial prefrontal cortex, while the mice are tested in a T maze. All animals are implanted with custom-designed, 3D-printed microdrives that carry 16 electrodes, which are bundled in a 4-tetrode geometry. Results: We provide an overview of a framework for analyzing single-unit data in which we have concatenated the acquisition system (Cheetah, Neuralynx) with analytical software (MATLAB) and an automated spike sorting pipeline (MountainSort). We give precise instructions on how to implement the different steps of the framework, as well as explanations of our design logic. We validate this framework by comparing manually-sorted spikes against automatically-sorted spikes, using neural recordings of the hippocampus and prelimbic cortex in freely-moving mice. Conclusions: We have efficiently integrated the MountainSort spike sorter with Neuralynx-acquired neural recordings. Our framework is easy to implement and provides a high-throughput solution. We predict that within the broad field of bioelectronic medicine, those teams that incorporate high-density neural recording devices to their armamentarium might find our framework quite valuable as they expand their analytical footprint.
Language	English
Publishing date	2021-11-23
Publishing country	England
Document type	Journal Article
ZDB-ID	2929561-0
ISSN	2332-8886 ; 2332-8886
ISSN (online)	2332-8886
ISSN	2332-8886
DOI	10.1186/s42234-021-00079-3
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Article: Neurobehavioral impairments predict specific cerebral damage in rat model of subarachnoid hemorrhage.

Lynch, Daniel G / Shah, Kevin A / Powell, Keren / Wadolowski, Steven / Ayol, Willians Tambo / Strohl, Joshua J / Unadkat, Prashin / Eidelberg, David / Huerta, Patricio T / Li, Chunyan

Research square

2023

Abstract: Subarachnoid hemorrhage (SAH) is a severe form of stroke that can cause unpredictable and diffuse cerebral damage, which is difficult to detect until it becomes irreversible. Therefore, there is a need for a reliable method to identify dysfunctional ... ...

Abstract	Subarachnoid hemorrhage (SAH) is a severe form of stroke that can cause unpredictable and diffuse cerebral damage, which is difficult to detect until it becomes irreversible. Therefore, there is a need for a reliable method to identify dysfunctional regions and initiate treatment before permanent damage occurs. Neurobehavioral assessments have been suggested as a possible tool to detect and approximately localize dysfunctional cerebral regions. In this study, we hypothesized that a neurobehavioral assessment battery could be a sensitive and specific early warning for damage in discrete cerebral regions following SAH. To test this hypothesis, a behavioral battery was employed at multiple time points after SAH induced via an endovascular perforation, and brain damage was confirmed via postmortem histopathological analysis. Our results demonstrate that impairment of sensorimotor function accurately predict damage in the cerebral cortex (AUC: 0.905; sensitivity: 81.8%; specificity: 90.9%) and striatum (AUC: 0.913; sensitivity: 90.1%; specificity: 100%), while impaired novel object recognition is a more accurate indicator of damage to the hippocampus (AUC: 0.902; sensitivity: 74.1%; specificity: 83.3%) than impaired reference memory (AUC: 0.746; sensitivity: 72.2%; specificity: 58.0%). Tests for anxiety-like and depression-like behaviors predict damage to the amygdala (AUC: 0.900; sensitivity: 77.0%; specificity: 81.7%) and thalamus (AUC: 0.963; sensitivity: 86.3%; specificity: 87.8%), respectively. This study suggests that recurring behavioral testing can accurately predict damage in specific brain regions, which could be developed into a clinical battery for early detection of SAH damage in humans, potentially improving early treatment and outcomes.
Language	English
Publishing date	2023-05-19
Publishing country	United States
Document type	Preprint
DOI	10.21203/rs.3.rs-2943917/v1
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Article ; Online: Neurobehavioral Impairments Predict Specific Cerebral Damage in Rat Model of Subarachnoid Hemorrhage.

Lynch, Daniel G / Shah, Kevin A / Powell, Keren / Wadolowski, Steven / Tambo, Willians / Strohl, Joshua J / Unadkat, Prashin / Eidelberg, David / Huerta, Patricio T / Li, Chunyan

Translational stroke research

2023

Abstract	Subarachnoid hemorrhage (SAH) is a severe form of stroke that can cause unpredictable and diffuse cerebral damage, which is difficult to detect until it becomes irreversible. Therefore, there is a need for a reliable method to identify dysfunctional regions and initiate treatment before permanent damage occurs. Neurobehavioral assessments have been suggested as a possible tool to detect and approximately localize dysfunctional cerebral regions. In this study, we hypothesized that a neurobehavioral assessment battery could be a sensitive and specific method for detecting damage in discrete cerebral regions following SAH. To test this hypothesis, a behavioral battery was employed at multiple time points after SAH induced via an endovascular perforation, and brain damage was confirmed via postmortem histopathological analysis. Our results demonstrate that impairment of sensorimotor function accurately predict damage in the cerebral cortex (AUC 0.905; sensitivity 81.8%; specificity 90.9%) and striatum (AUC 0.913; sensitivity 90.1%; specificity 100%), while impaired novel object recognition is a more accurate indicator of damage to the hippocampus (AUC 0.902; sensitivity 74.1%; specificity 83.3%) than impaired reference memory (AUC 0.746; sensitivity 72.2%; specificity 58.0%). Tests for anxiety-like and depression-like behaviors predict damage to the amygdala (AUC 0.900; sensitivity 77.0%; specificity 81.7%) and thalamus (AUC 0.963; sensitivity 86.3%; specificity 87.8%), respectively. This study suggests that recurring behavioral testing can accurately predict damage in specific brain regions, which could be developed into a clinical battery for early detection of SAH damage in humans, potentially improving early treatment and outcomes.
Language	English
Publishing date	2023-07-26
Publishing country	United States
Document type	Journal Article
ZDB-ID	2541897-X
ISSN	1868-601X ; 1868-4483
ISSN (online)	1868-601X
ISSN	1868-4483
DOI	10.1007/s12975-023-01180-2
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Article ; Online: Assessment of glutamatergic synaptic transmission and plasticity in brain slices: relevance to bioelectronic approaches.

Chang, Eric H / Carreiro, Samantha T / Frattini, Stephen A / Huerta, Patricio T

Bioelectronic medicine

2019 Volume 5, Page(s) 6

Abstract: Background: Glutamatergic neurons represent the largest neuronal class in the brain and are responsible for the bulk of excitatory synaptic transmission and plasticity. Abnormalities in glutamatergic neurons are linked to several brain disorders and ... ...

Abstract	Background: Glutamatergic neurons represent the largest neuronal class in the brain and are responsible for the bulk of excitatory synaptic transmission and plasticity. Abnormalities in glutamatergic neurons are linked to several brain disorders and their modulation represents a potential opportunity for emerging bioelectronic medicine (BEM) approaches. Here, we have used a set of electrophysiological assays to identify the effect of the pyrimidine nucleoside uridine on glutamatergic systems in ex vivo brain slices. An improved understanding of glutamatergic synaptic transmission and plasticity, through this type of examination, is critical to the development of potential neuromodulation strategies. Methods: Ex vivo hippocampal slices (400 μm thick) were prepared from mouse brain. We recorded field excitatory postsynaptic potentials (fEPSP) in the CA1's stratum radiatum by stimulation of the CA3 Schaeffer collateral/commissural axons. Uridine was applied at concentrations (3, 30, 300 μM) representing the physiological range present in brain tissue. Synaptic function was studied with input-output (I-O) functions, as well as paired-pulse facilitation (PPF). Synaptic plasticity was studied by applying tetanic stimulation to induce post-tetanic potentiation (PTP), short-term potentiation (STP) and long-term potentiation (LTP). Additionally, we determined whether uridine affected synaptic responses carried solely by n-methyl-d-aspartate receptors (NMDARs), particularly during the oxygen-glucose deprivation (OGD) paradigm. Results: The presence of uridine altered glutamatergic synaptic transmission and plasticity. We found that uridine affected STP and LTP in a concentration-dependent manner. Low-dose uridine (3 μM) had no effect, but higher doses (30 and 300 μM) impaired STP and LTP. Moreover, uridine (300 μM) decreased NMDAR-mediated synaptic responses. Conversely, uridine (at all concentrations tested) had a negligible effect on PPF and basal synaptic transmission, which is mediated primarily by α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptors (AMPARs). In addition, uridine (100 μM) exerted a protective effect when the hippocampal slices were challenged with OGD, a widely used model of cerebral ischemia. Conclusions: Using a wide set of electrophysiological assays, we identify that uridine interacts with glutamatergic neurons to alter NMDAR-mediated responses, impair synaptic STP and LTP in a dose-dependent manner, and has a protective effect against OGD insult. This work outlines a strategy to identify deficits in glutamatergic mechanisms for signaling and plasticity that may be critical for targeting these same systems with BEM device-based approaches. To improve the efficacy of potential neuromodulation approaches for treating brain dysfunction, we need to improve our understanding of glutamatergic systems in the brain, including the effects of modulators such as uridine.
Language	English
Publishing date	2019-06-10
Publishing country	England
Document type	Journal Article
ZDB-ID	2929561-0
ISSN	2332-8886 ; 2332-8886
ISSN (online)	2332-8886
ISSN	2332-8886
DOI	10.1186/s42234-019-0022-2
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Article ; Online: Reversible dysregulation of renal circadian rhythm in lupus nephritis.

Mishra, Rakesh / Bethunaickan, Ramalingam / Berthier, Celine C / Yi, Zhengzi / Strohl, Joshua J / Huerta, Patricio T / Zhang, Weijia / Davidson, Anne

Molecular medicine (Cambridge, Mass.)

2021 Volume 27, Issue 1, Page(s) 99

Abstract: Background: We have found disruption of expression of major transcriptional regulators of circadian rhythm in the kidneys of several mouse models of lupus nephritis. Here we define the consequence of this disturbance with respect to circadian gene ... ...

Abstract	Background: We have found disruption of expression of major transcriptional regulators of circadian rhythm in the kidneys of several mouse models of lupus nephritis. Here we define the consequence of this disturbance with respect to circadian gene expression and renal homeostatic function in a mouse model of lupus nephritis. Methods: Molecular profiling of kidneys from 47 young and 41 nephritic female NZB/W F1 mice was performed at 4 hourly intervals over a 24 h period. Disruption of major circadian transcriptional regulators was confirmed by qPCR. Molecular data was normalized and analyzed for rhythmicity using RAIN analysis. Serum aldosterone and glucose and urine sodium and potassium were measured at 4 hourly intervals in pre-nephritic and nephritic mice and blood pressure was measured every 4 h. Analyses were repeated after induction of complete remission of nephritis using combination cyclophosphamide and costimulatory blockade. Results: We show a profound alteration of renal circadian rhythms in mice with lupus nephritis affecting multiple renal pathways. Using Cosinor analysis we identified consequent alterations of renal homeostasis and metabolism as well as blood pressure dipper status. This circadian dysregulation was partially reversed by remission induction therapy. Conclusions: Our studies indicate the role of inflammation in causing the circadian disruption and suggest that screening for loss of normal blood pressure dipping should be incorporated into LN management. The data also suggest a potential role for circadian agonists in the treatment of lupus nephritis.
MeSH term(s)	Animals ; Biomarkers ; Circadian Rhythm/genetics ; Computational Biology/methods ; Disease Models, Animal ; Disease Susceptibility ; Female ; Gene Expression Profiling ; Gene Expression Regulation ; Lupus Nephritis/etiology ; Lupus Nephritis/metabolism ; Lupus Nephritis/pathology ; Mice ; Transcriptome
Chemical Substances	Biomarkers
Language	English
Publishing date	2021-09-06
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	1283676-x
ISSN	1528-3658 ; 1076-1551
ISSN (online)	1528-3658
ISSN	1076-1551
DOI	10.1186/s10020-021-00361-9
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Article ; Online: Integrative neuroscience approach to neuropsychiatric lupus.

Huerta, Patricio T / Gibson, Elizabeth L / Rey, Carson / Huerta, Tomás S

Immunologic research

2015 Volume 63, Issue 1-3, Page(s) 11–17

Abstract: We present a succinct review of our approach to study the interactions between the DNA-reactive antibodies that cross-react with the GluN2A and GluN2B subunits of the N-methyl-D-aspartate receptor, denoted DNRABs, and their brain targets in subjects with ...

Abstract	We present a succinct review of our approach to study the interactions between the DNA-reactive antibodies that cross-react with the GluN2A and GluN2B subunits of the N-methyl-D-aspartate receptor, denoted DNRABs, and their brain targets in subjects with neuropsychiatric systemic lupus erythematosus (NPSLE). We have analyzed the DNRAB-based brain symptomatology in mouse models of NPSLE by using an integrative neuroscience approach, which includes behavioral assessment coupled with electrophysiological studies of neural networks and synaptic connections in target brain regions, such as the CA1 region of the hippocampus. Our results suggest a framework for understanding the interactions between immune factors and neural networks.
MeSH term(s)	Animals ; Antibodies, Antinuclear/metabolism ; CA1 Region, Hippocampal/physiology ; Cognition Disorders/immunology ; Cross Reactions ; Humans ; Lupus Erythematosus, Systemic/immunology ; Mice ; Nerve Net/physiology ; Neuroimmunomodulation ; Receptors, N-Methyl-D-Aspartate/immunology ; Receptors, N-Methyl-D-Aspartate/metabolism
Chemical Substances	Antibodies, Antinuclear ; N-methyl D-aspartate receptor subtype 2A ; NR2B NMDA receptor ; Receptors, N-Methyl-D-Aspartate
Language	English
Publishing date	2015-12
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Review
ZDB-ID	632857-x
ISSN	1559-0755 ; 0257-277X
ISSN (online)	1559-0755
ISSN	0257-277X
DOI	10.1007/s12026-015-8713-6
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Zs.A 1755: Show issues

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Jg. 1995 - 2021: Lesesall (1.OG)
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Article: Large-Scale Validation of the Paddling Pool Task in the Clockmaze for Studying Hippocampus-Based Spatial Cognition in Mice.

Sankowski, Roman / Huerta, Tomás S / Kalra, Rishi / Klein, Toby J / Strohl, Joshua J / Al-Abed, Yousef / Robbiati, Sergio / Huerta, Patricio T

Frontiers in behavioral neuroscience

2019 Volume 13, Page(s) 121

Abstract: Rationally designed behavioral tests are important tools to assess the function of specific brain regions. The hippocampus is a crucial neural substrate for spatial cognition, and many studies have linked hippocampal dysfunction with defects on spatial ... ...

Abstract	Rationally designed behavioral tests are important tools to assess the function of specific brain regions. The hippocampus is a crucial neural substrate for spatial cognition, and many studies have linked hippocampal dysfunction with defects on spatial learning and memory in neurological conditions ranging from Alzheimer's disease to autoimmune syndromes, such as neuropsychiatric lupus. While our understanding of hippocampal function, from the molecular to the system levels, has increased dramatically over the last decades, this effort has not yet translated into efficacious therapies for cognitive impairment. We think that the availability of highly validated behavioral paradigms to measure cognition in mouse models is likely to enhance the potential success of preclinical therapeutic modalities. Here, we present an extensive study of the paddling pool task (PPT), first reported by Deacon and Rawlins, in which mice learn to escape from shallow water through a peripheral exit in a circular arena dubbed the clockmaze. We show that the PPT provides highly reliable results when assaying spatial cognition in C57/BL6 mice (120 males, 40 females) and BALB/c mice (40 males, 90 females). Additionally, we develop a robust algorithm for the assessment of escape strategies with clearly quantifiable readouts, enabling fine-granular phenotyping. Notably, the use of spatial strategy increases linearly across trials in the PPT. In a separate cohort of mice, we apply muscimol injections to silence the dorsal CA1 region of the hippocampus and show that the use of the spatial strategy in the PPT relies on the integrity of the dorsal hippocampus. Additionally, we compare directly the PPT and the Morris water maze (MWM) task in C57/BL6 mice (20 males, 20 females) and BALB/c mice (20 males, 20 females) and we find that the PPT induces significantly lower anxiety, exhaustion and hypothermia than the MWM. We conclude that the PPT provides a robust assessment of spatial cognition in mice, which can be applied in conjunction with other tests, to facilitate hypothesis testing and drug development to combat cognitive impairment.
Language	English
Publishing date	2019-06-07
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2452960-6
ISSN	1662-5153
ISSN	1662-5153
DOI	10.3389/fnbeh.2019.00121
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