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Article ; Online: Nonbinary 2D Distribution Tool Maps Autonomic Nerve Fiber Clustering in Lumbosacral Ventral Roots of Rhesus Macaques.

Bartmeyer, Petra M / Biscola, Natalia P / Havton, Leif A

2024 Volume 11, Issue 4

Abstract: Neuromodulation of the peripheral nervous system (PNS) by electrical stimulation may augment autonomic function after injury or in neurodegenerative disorders. Nerve fiber size, myelination, and distance between individual fibers and the stimulation ... ...

Abstract	Neuromodulation of the peripheral nervous system (PNS) by electrical stimulation may augment autonomic function after injury or in neurodegenerative disorders. Nerve fiber size, myelination, and distance between individual fibers and the stimulation electrode may influence response thresholds to electrical stimulation. However, information on the spatial distribution of nerve fibers within the PNS is sparse. We developed a new two-dimensional (2D) morphological mapping tool to assess spatial heterogeneity and clustering of nerve fibers. The L6-S3 ventral roots (VRs) in rhesus macaques were used as a model system to map preganglionic parasympathetic, γ-motor, and α-motor fibers. Random and ground truth distributions of nerve fiber centroids were determined for each VR by light microscopy. The proposed tool allows for nonbinary determinations of fiber heterogeneity by defining the minimum distance between nerve fibers for cluster inclusion and comparisons with random fiber distributions for each VR. There was extensive variability in the relative composition of nerve fiber types and degree of 2D fiber heterogeneity between different L6-S3 VR levels within and across different animals. There was a positive correlation between the proportion of autonomic fibers and the degree of nerve fiber clustering. Nerve fiber cluster heterogeneity between VRs may contribute to varied functional outcomes from neuromodulation.
MeSH term(s)	Animals ; Macaca mulatta ; Spinal Nerve Roots ; Autonomic Pathways ; Cluster Analysis
Language	English
Publishing date	2024-04-12
Publishing country	United States
Document type	Journal Article
ZDB-ID	2800598-3
ISSN	2373-2822 ; 2373-2822
ISSN (online)	2373-2822
ISSN	2373-2822
DOI	10.1523/ENEURO.0009-23.2024
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Article ; Online: Detrusor underactivity is associated with metabolic syndrome in aged primates.

Biscola, Natalia P / Bartmeyer, Petra M / Christe, Kari L / Colman, Ricki J / Havton, Leif A

Scientific reports

2023 Volume 13, Issue 1, Page(s) 6716

Abstract: Lower urinary tract (LUT) dysfunction is prevalent in the elderly population, and clinical manifestations include urinary retention, incontinence, and recurrent urinary tract infections. Age-associated LUT dysfunction is responsible for significant ... ...

Abstract	Lower urinary tract (LUT) dysfunction is prevalent in the elderly population, and clinical manifestations include urinary retention, incontinence, and recurrent urinary tract infections. Age-associated LUT dysfunction is responsible for significant morbidity, compromised quality of life, and rising healthcare costs in older adults, but its pathophysiology is not well understood. We aimed to investigate the effects of aging on LUT function by urodynamic studies and metabolic markers in non-human primates. Adult (n = 27) and aged (n = 20) female rhesus macaques were evaluated by urodynamic and metabolic studies. Cystometry showed detrusor underactivity (DU) with increased bladder capacity and compliance in aged subjects. Metabolic syndrome indicators were present in the aged subjects, including increased weight, triglycerides, lactate dehydrogenase (LDH), alanine aminotransferase (ALT), and high sensitivity C-reactive protein (hsCRP), whereas aspartate aminotransferase (AST) was unaffected and the AST/ALT ratio reduced. Principal component analysis and paired correlations showed a strong association between DU and metabolic syndrome markers in aged primates with DU but not in aged primates without DU. The findings were unaffected by prior pregnancies, parity, and menopause. Our findings provide insights into possible mechanisms for age-associated DU and may guide new strategies to prevent and treat LUT dysfunction in older adults.
MeSH term(s)	Aged ; Animals ; Female ; Humans ; Urinary Bladder, Underactive ; Metabolic Syndrome/complications ; Macaca mulatta ; Quality of Life ; Urinary Bladder ; Urodynamics/physiology
Language	English
Publishing date	2023-04-25
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S. ; Research Support, N.I.H., Extramural
ZDB-ID	2615211-3
ISSN	2045-2322 ; 2045-2322
ISSN (online)	2045-2322
ISSN	2045-2322
DOI	10.1038/s41598-023-33112-3
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Article ; Online: A shape-adjusted ellipse approach corrects for varied axonal dispersion angles and myelination in primate nerve roots.

Bartmeyer, Petra M / Biscola, Natalia P / Havton, Leif A

Scientific reports

2021 Volume 11, Issue 1, Page(s) 3150

Abstract: Segmentation of axons in light and electron micrographs allows for quantitative high-resolution analysis of nervous tissues, but varied axonal dispersion angles result in over-estimates of fiber sizes. To overcome this technical challenge, we developed a ...

Abstract	Segmentation of axons in light and electron micrographs allows for quantitative high-resolution analysis of nervous tissues, but varied axonal dispersion angles result in over-estimates of fiber sizes. To overcome this technical challenge, we developed a novel shape-adjusted ellipse (SAE) determination of axonal size and myelination as an all-inclusive and non-biased tool to correct for oblique nerve fiber presentations. Our new resource was validated by light and electron microscopy against traditional methods of determining nerve fiber size and myelination in rhesus macaques as a model system. We performed detailed segmental mapping and characterized the morphological signatures of autonomic and motor fibers in primate lumbosacral ventral roots (VRs). An en bloc inter-subject variability for the preganglionic parasympathetic fibers within the L7-S2 VRs was determined. The SAE approach allows for morphological ground truth data collection and assignment of individual axons to functional phenotypes with direct implications for fiber mapping and neuromodulation studies.
MeSH term(s)	Animals ; Axons/physiology ; Axons/ultrastructure ; Female ; Fixatives ; Formaldehyde ; Glutaral ; Lumbosacral Region/innervation ; Macaca mulatta ; Microscopy, Electron/methods ; Microscopy, Electron/standards ; Nerve Fibers, Myelinated/physiology ; Nerve Fibers, Myelinated/ultrastructure ; Polymers ; Spinal Nerve Roots/physiology ; Spinal Nerve Roots/ultrastructure ; Tissue Fixation/methods
Chemical Substances	Fixatives ; Polymers ; Formaldehyde (1HG84L3525) ; Glutaral (T3C89M417N) ; paraform (Y19UC83H8E)
Language	English
Publishing date	2021-02-04
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2615211-3
ISSN	2045-2322 ; 2045-2322
ISSN (online)	2045-2322
ISSN	2045-2322
DOI	10.1038/s41598-021-82575-9
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Article: Comparative specialization of intrinsic cardiac neurons in humans, mice, and pigs.

Tompkins, John D / Hoover, Donald B / Havton, Leif A / Patel, Janaki C / Cho, Youngjin / Smith, Elizabeth H / Biscola, Natalia P / Ajijola, Olujimi A / Shivkumar, Kalyanam / Ardell, Jeffrey L

bioRxiv : the preprint server for biology

2024

Abstract: Intrinsic cardiac neurons (ICNs) play a crucial role in the proper functioning of the heart; yet a paucity of data pertaining to human ICNs exists. We took a multidisciplinary approach to complete a detailed cellular comparison of the structure and ... ...

Abstract	Intrinsic cardiac neurons (ICNs) play a crucial role in the proper functioning of the heart; yet a paucity of data pertaining to human ICNs exists. We took a multidisciplinary approach to complete a detailed cellular comparison of the structure and function of ICNs from mice, pigs, and humans. Immunohistochemistry of whole and sectioned ganglia, transmission electron microscopy, intracellular microelectrode recording and dye filling for quantitative morphometry were used to define the neurophysiology, histochemistry, and ultrastructure of these cells across species. The densely packed, smaller ICNs of mouse lacked dendrites, formed axosomatic connections, and had high synaptic efficacy constituting an obligatory synapse. At Pig ICNs, a convergence of subthreshold cholinergic inputs onto extensive dendritic arbors supported greater summation and integration of synaptic input. Human ICNs were tonically firing, with synaptic stimulation evoking large suprathreshold excitatory postsynaptic potentials like mouse, and subthreshold potentials like pig. Ultrastructural examination of synaptic terminals revealed conserved architecture, yet small clear vesicles (SCVs) were larger in pigs and humans. The presence and localization of ganglionic neuropeptides was distinct, with abundant VIP observed in human but not pig or mouse ganglia, and little SP or CGRP in pig ganglia. Action potential waveforms were similar, but human ICNs had larger after-hyperpolarizations. Intrinsic excitability differed; 93% of human cells were tonic, all pig neurons were phasic, and both phasic and tonic phenotypes were observed in mouse. In combination, this publicly accessible, multimodal atlas of ICNs from mice, pigs, and humans identifies similarities and differences in the evolution of ICNs.
Language	English
Publishing date	2024-04-08
Publishing country	United States
Document type	Preprint
DOI	10.1101/2024.04.04.588174
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Article ; Online: Ketamine-induced neuromuscular reactivity is associated with aging in female rhesus macaques.

Havton, Leif A / Biscola, Natalia P / Christe, Kari L / Colman, Ricki J

PloS one

2020 Volume 15, Issue 9, Page(s) e0236430

Abstract: Rhesus macaques represent an important species for translational and pre-clinical research studies across a multitude of disease and injury models, including aging. Ketamine anesthesia is used in humans and non-human primates but may be associated with ... ...

Abstract	Rhesus macaques represent an important species for translational and pre-clinical research studies across a multitude of disease and injury models, including aging. Ketamine anesthesia is used in humans and non-human primates but may be associated with adverse effects, including neuromuscular reactions. The effects of aging on ketamine adverse effects is not well characterized. Urodynamic recordings and electromyography (EMG) studies were performed in aged (>20 years old) and adult (3.9-14.9 years old) female rhesus macaques under an equal and light plane of sedation by constant rate infusion (CRI) of ketamine. A total of 4 of 41 adult subjects (9.7%) showed clinical signs of ketamine-induced abnormal neuromuscular reactivity, whereas a larger portion of 14 of 26 aged subjects showed similar ketamine-induced neuromuscular reactivity (53.8%; P< 0.001). The ketamine CRI rate was 19.8±0.9 mg/kg/h in adults and lower in aged subjects at 16.5±1.4 mg/kg/h (P<0.05). The ketamine CRI rate was negatively correlated with age (r = -0.30, P<0.05, n = 64). The incidence of ketamine reactivity or CRI rate was not different between aged pre-and post-menopausal females. EMG recordings during neuromuscular reactivity showed coordinated activation of multiple muscles, suggesting a central nervous system (CNS) mechanism for ketamine-associated neuromuscular reactivity. The incidence of ketamine-induced neuromuscular reactivity is age related but not affected by the estrous cycle in female rhesus macaques. A coordinated activation of multiple muscles, innervated by different peripheral nerves, suggests that ketamine-induced neuromuscular reactivity originates in the CNS.
MeSH term(s)	Aging/drug effects ; Anesthetics, Dissociative/adverse effects ; Animals ; Electromyography ; Female ; Ketamine/adverse effects ; Macaca mulatta/physiology ; Muscles/drug effects ; Muscles/innervation ; Muscles/physiology
Chemical Substances	Anesthetics, Dissociative ; Ketamine (690G0D6V8H)
Language	English
Publishing date	2020-09-21
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ISSN	1932-6203
ISSN (online)	1932-6203
DOI	10.1371/journal.pone.0236430
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Article ; Online: Bortezomib-induced neuropathy is in part mediated by the sensitization of TRPV1 channels.

Sprague, Jared M / Yekkirala, Ajay S / Singh, Bhagat / Tochitsky, Ivan / Stephens, Michael / Viramontes, Octavio / Ivanis, Jelena / Biscola, Natalia P / Havton, Leif A / Woolf, Clifford J / Latremoliere, Alban

Communications biology

2023 Volume 6, Issue 1, Page(s) 1228

Abstract: TRPV1 is an ion channel that transduces noxious heat and chemical stimuli and is expressed in small fiber primary sensory neurons that represent almost half of skin nerve terminals. Tissue injury and inflammation result in the sensitization of TRPV1 and ... ...

Abstract	TRPV1 is an ion channel that transduces noxious heat and chemical stimuli and is expressed in small fiber primary sensory neurons that represent almost half of skin nerve terminals. Tissue injury and inflammation result in the sensitization of TRPV1 and sustained activation of TRPV1 can lead to cellular toxicity though calcium influx. To identify signals that trigger TRPV1 sensitization after a 24-h exposure, we developed a phenotypic assay in mouse primary sensory neurons and performed an unbiased screen with a compound library of 480 diverse bioactive compounds. Chemotherapeutic agents, calcium ion deregulators and protein synthesis inhibitors were long-acting TRPV1 sensitizers. Amongst the strongest TRPV1 sensitizers were proteasome inhibitors, a class that includes bortezomib, a chemotherapeutic agent that causes small fiber neuropathy in 30-50% of patients. Prolonged exposure of bortezomib produced a TRPV1 sensitization that lasted several days and neurite retraction in vitro and histological and behavioral changes in male mice in vivo. TRPV1 knockout mice were protected from epidermal nerve fiber loss and a loss of sensory discrimination after bortezomib treatment. We conclude that long-term TRPV1 sensitization contributes to the development of bortezomib-induced neuropathy and the consequent loss of sensation, major deficits experienced by patients under this chemotherapeutic agent.
MeSH term(s)	Humans ; Mice ; Male ; Animals ; Bortezomib/adverse effects ; Bortezomib/metabolism ; TRPV Cation Channels/genetics ; TRPV Cation Channels/metabolism ; Calcium/metabolism ; Skin/metabolism ; Mice, Knockout
Chemical Substances	Bortezomib (69G8BD63PP) ; TRPV Cation Channels ; Calcium (SY7Q814VUP) ; TRPV1 protein, human ; TRPV1 protein, mouse
Language	English
Publishing date	2023-12-05
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ISSN	2399-3642
ISSN (online)	2399-3642
DOI	10.1038/s42003-023-05624-1
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Article ; Online: Sexual dimorphism of detrusor function demonstrated by urodynamic studies in rhesus macaques.

Biscola, Natalia P / Christe, Kari L / Rosenzweig, Ephron S / Tuszynski, Mark H / Havton, Leif A

Scientific reports

2020 Volume 10, Issue 1, Page(s) 16170

Abstract: The lower urinary tract (LUT) and micturition reflexes are sexually dimorphic across mammals. Sex as a biological variable is also of critical importance for the development and translation of new medical treatments and therapeutics interventions ... ...

Abstract	The lower urinary tract (LUT) and micturition reflexes are sexually dimorphic across mammals. Sex as a biological variable is also of critical importance for the development and translation of new medical treatments and therapeutics interventions affecting pelvic organs, including the LUT. However, studies of LUT function with comparisons between the sexes have remained sparse, especially for larger mammals. Detrusor function was investigated by filling cystometry and pressure flow studies in 16 male and 22 female rhesus macaques. By filling cystometry, male subjects exhibited a significantly larger bladder capacity and compliance compared to females. Pressure flow studies showed a significantly higher bladder pressure at voiding onset, peak pressure, and elevation in detrusor-activated bladder pressure from the end of bladder filling to peak pressure in the male subjects. The activation of reflex micturition, with associated detrusor contractions, resulted in voiding in a significantly larger proportion of female compared to male subjects. A higher urethral outlet resistance is suggested in the male subjects. We conclude that sexual dimorphism of detrusor function is prominent in rhesus macaques, shares many features with the human, and merits consideration in translational and pre-clinical research studies of micturition and LUT function in non-human primates.
MeSH term(s)	Animals ; Female ; Macaca mulatta ; Male ; Reflex/physiology ; Sex Characteristics ; Urethra/physiology ; Urinary Bladder/physiology ; Urination/physiology ; Urodynamics/physiology
Language	English
Publishing date	2020-09-30
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	2615211-3
ISSN	2045-2322 ; 2045-2322
ISSN (online)	2045-2322
ISSN	2045-2322
DOI	10.1038/s41598-020-73016-0
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Article: A novel statistical methodology for quantifying the spatial arrangements of axons in peripheral nerves.

Shemonti, Abida Sanjana / Plebani, Emanuele / Biscola, Natalia P / Jaffey, Deborah M / Havton, Leif A / Keast, Janet R / Pothen, Alex / Dundar, M Murat / Powley, Terry L / Rajwa, Bartek

Frontiers in neuroscience

2023 Volume 17, Page(s) 1072779

Abstract: A thorough understanding of the neuroanatomy of peripheral nerves is required for a better insight into their function and the development of neuromodulation tools and strategies. In biophysical modeling, it is commonly assumed that the complex spatial ... ...

Abstract	A thorough understanding of the neuroanatomy of peripheral nerves is required for a better insight into their function and the development of neuromodulation tools and strategies. In biophysical modeling, it is commonly assumed that the complex spatial arrangement of myelinated and unmyelinated axons in peripheral nerves is random, however, in reality the axonal organization is inhomogeneous and anisotropic. Present quantitative neuroanatomy methods analyze peripheral nerves in terms of the number of axons and the morphometric characteristics of the axons, such as area and diameter. In this study, we employed spatial statistics and point process models to describe the spatial arrangement of axons and Sinkhorn distances to compute the similarities between these arrangements (in terms of first- and second-order statistics) in various vagus and pelvic nerve cross-sections. We utilized high-resolution transmission electron microscopy (TEM) images that have been segmented using a custom-built high-throughput deep learning system based on a highly modified U-Net architecture. Our findings show a novel and innovative approach to quantifying similarities between spatial point patterns using metrics derived from the solution to the optimal transport problem. We also present a generalizable pipeline for quantitative analysis of peripheral nerve architecture. Our data demonstrate differences between male- and female-originating samples and similarities between the pelvic and abdominal vagus nerves.
Language	English
Publishing date	2023-03-09
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.2023.1072779
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Article ; Online: Computational modelling of nerve stimulation and recording with peripheral visceral neural interfaces.

Eiber, Calvin D / Payne, Sophie C / Biscola, Natalia P / Havton, Leif A / Keast, Janet R / Osborne, Peregrine B / Fallon, James B

Journal of neural engineering

2021 Volume 18, Issue 6

Abstract: Objective. ...

Abstract	Objective.
MeSH term(s)	Action Potentials/physiology ; Animals ; Axons/physiology ; Computer Simulation ; Electric Stimulation/methods ; Nerve Tissue ; Peripheral Nerves/physiology ; Rats
Language	English
Publishing date	2021-11-25
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2170901-4
ISSN	1741-2552 ; 1741-2560
ISSN (online)	1741-2552
ISSN	1741-2560
DOI	10.1088/1741-2552/ac36e2
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Article: Sarm1 is not necessary for activation of neuron-intrinsic growth programs yet required for the Schwann cell repair response and peripheral nerve regeneration.

bioRxiv : the preprint server for biology

2024

Abstract: Upon peripheral nervous system (PNS) injury, severed axons undergo rapid SARM1-dependent Wallerian degeneration (WD). In mammals, the role of SARM1 in PNS regeneration, however, is unknown. Here we demonstrate ... ...

Abstract	Upon peripheral nervous system (PNS) injury, severed axons undergo rapid SARM1-dependent Wallerian degeneration (WD). In mammals, the role of SARM1 in PNS regeneration, however, is unknown. Here we demonstrate that
Language	English
Publishing date	2024-04-17
Publishing country	United States
Document type	Preprint
DOI	10.1101/2024.03.04.583374
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