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Book ; Online: Axonopathy in Neurodegenerative Disease

Crish, Samuel D. / Burgess, Robert W. / Inman, Denise M. / Dengler-Crish, Christine M. / Richardson, Jason R. / Schofield, Brett

2019

Keywords	Science: general issues ; Neurosciences ; axon degeneration ; Neuropathy ; Glaucoma ; Mitochondrial dysfunction ; Chemotherapy-induced peripheral neuropathy ; Mitochondria ; tau ; axon transport ; Neuroinflammation
Size	1 electronic resource (248 pages)
Publisher	Frontiers Media SA
Document type	Book ; Online
Note	English ; Open Access
HBZ-ID	HT021230221
ISBN	9782889456802 ; 2889456803
Database	ZB MED Catalogue: Medicine, Health, Nutrition, Environment, Agriculture

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Article: Lineage-tracing reveals an expanded population of NPY neurons in the inferior colliculus.

Silveira, Marina A / Herrera, Yoani N / Beebe, Nichole L / Schofield, Brett R / Roberts, Michael T

bioRxiv : the preprint server for biology

2024

Abstract: Growing evidence suggests that neuropeptide signaling shapes auditory computations. We previously showed that neuropeptide Y (NPY) is expressed in the inferior colliculus (IC) by a population of GABAergic stellate neurons and that NPY regulates the ... ...

Abstract	Growing evidence suggests that neuropeptide signaling shapes auditory computations. We previously showed that neuropeptide Y (NPY) is expressed in the inferior colliculus (IC) by a population of GABAergic stellate neurons and that NPY regulates the strength of local excitatory circuits in the IC. NPY neurons were initially characterized using the NPY-hrGFP reporter mouse, in which hrGFP expression indicates NPY expression at the time of assay, i.e., an expression-tracking approach. However, studies in other brain regions have shown that NPY expression can vary based on a range of factors, suggesting that the NPY-hrGFP mouse might miss NPY neurons not expressing NPY proximal to the experiment date. Here, we hypothesized that neurons with the ability to express NPY represent a larger population of IC GABAergic neurons than previously reported. To test this hypothesis, we used a lineage-tracing approach to irreversibly tag neurons that expressed NPY at any point prior to the experiment date. We then compared the physiological and anatomical features of neurons labeled with this lineage-tracing approach to our prior data set, revealing a larger population of NPY neurons than previously found. In addition, we used optogenetics to test the local connectivity of NPY neurons and found that NPY neurons routinely provide inhibitory synaptic input to other neurons in the ipsilateral IC. Together, our data expand the definition of NPY neurons in the IC, suggest that NPY expression might be dynamically regulated in the IC, and provide functional evidence that NPY neurons form local inhibitory circuits in the IC.
Language	English
Publishing date	2024-03-30
Publishing country	United States
Document type	Preprint
DOI	10.1101/2024.03.27.587042
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Article ; Online: Cholinergic boutons are closely associated with excitatory cells and four subtypes of inhibitory cells in the inferior colliculus.

Beebe, Nichole L / Schofield, Brett R

Journal of chemical neuroanatomy

2021 Volume 116, Page(s) 101998

Abstract: Acetylcholine (ACh) is a neuromodulator that has been implicated in multiple roles across the brain, including the central auditory system, where it sets neuronal excitability and gain and affects plasticity. In the cerebral cortex, subtypes of GABAergic ...

Abstract	Acetylcholine (ACh) is a neuromodulator that has been implicated in multiple roles across the brain, including the central auditory system, where it sets neuronal excitability and gain and affects plasticity. In the cerebral cortex, subtypes of GABAergic interneurons are modulated by ACh in a subtype-specific manner. Subtypes of GABAergic neurons have also begun to be described in the inferior colliculus (IC), a midbrain hub of the auditory system. Here, we used male and female mice (Mus musculus) that express fluorescent protein in cholinergic cells, axons, and boutons to look at the association between ACh and four subtypes of GABAergic IC cells that differ in their associations with extracellular markers, their soma sizes, and their distribution within the IC. We found that most IC cells, including excitatory and inhibitory cells, have cholinergic boutons closely associated with their somas and proximal dendrites. We also found that similar proportions of each of four subtypes of GABAergic cells are closely associated with cholinergic boutons. Whether the different types of GABAergic cells in the IC are differentially regulated remains unclear, as the response of cells to ACh is dependent on which types of ACh receptors are present. Additionally, this study confirms the presence of these four subtypes of GABAergic cells in the mouse IC, as they had previously been identified only in guinea pigs. These results suggest that cholinergic projections to the IC modulate auditory processing via direct effects on a multitude of inhibitory circuits.
MeSH term(s)	Animals ; Cholinergic Neurons/chemistry ; Cholinergic Neurons/metabolism ; Female ; Inferior Colliculi/chemistry ; Inferior Colliculi/cytology ; Inferior Colliculi/metabolism ; Male ; Mice ; Mice, Inbred C57BL ; Mice, Transgenic ; Neural Inhibition/physiology ; Presynaptic Terminals/chemistry ; Presynaptic Terminals/metabolism ; Vesicular Glutamate Transport Protein 2/metabolism
Chemical Substances	Slc17a6 protein, mouse ; Vesicular Glutamate Transport Protein 2
Language	English
Publishing date	2021-06-26
Publishing country	Netherlands
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	639443-7
ISSN	1873-6300 ; 0891-0618
ISSN (online)	1873-6300
ISSN	0891-0618
DOI	10.1016/j.jchemneu.2021.101998
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Article ; Online: Characterization of three cholinergic inputs to the cochlear nucleus.

Beebe, Nichole L / Herrera, Yoani N / Noftz, William A / Roberts, Michael T / Schofield, Brett R

Journal of chemical neuroanatomy

2023 Volume 131, Page(s) 102284

Abstract: Acetylcholine modulates responses throughout the auditory system, including at the earliest brain level, the cochlear nucleus (CN). Previous studies have shown multiple sources of cholinergic input to the CN but information about their relative ... ...

Abstract	Acetylcholine modulates responses throughout the auditory system, including at the earliest brain level, the cochlear nucleus (CN). Previous studies have shown multiple sources of cholinergic input to the CN but information about their relative contributions and the distribution of inputs from each source is lacking. Here, we used staining for cholinergic axons and boutons, retrograde tract tracing, and acetylcholine-selective anterograde tracing to characterize three sources of acetylcholine input to the CN in mice. Staining for cholinergic axons showed heavy cholinergic inputs to granule cell areas and the dorsal CN with lighter input to the ventral CN. Retrograde tract tracing revealed that cholinergic cells from the superior olivary complex, pontomesencephalic tegmentum, and lateral paragigantocellular nucleus send projections to the CN. When we selectively labeled cholinergic axons from each source to the CN, we found surprising similarities in their terminal distributions, with patterns that were overlapping rather than complementary. Each source heavily targeted granule cell areas and the dorsal CN (especially the deep dorsal CN) and sent light input into the ventral CN. Our results demonstrate convergence of cholinergic inputs from multiple sources in most regions of the CN and raise the possibility of convergence onto single CN cells. Linking sources of acetylcholine and their patterns of activity to modulation of specific cell types in the CN will be an important next step in understanding cholinergic modulation of early auditory processing.
MeSH term(s)	Mice ; Animals ; Cochlear Nucleus/metabolism ; Acetylcholine/metabolism ; Cholinergic Agents ; Tegmentum Mesencephali ; Axons/metabolism
Chemical Substances	Acetylcholine (N9YNS0M02X) ; Cholinergic Agents
Language	English
Publishing date	2023-05-08
Publishing country	Netherlands
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	639443-7
ISSN	1873-6300 ; 0891-0618
ISSN (online)	1873-6300
ISSN	0891-0618
DOI	10.1016/j.jchemneu.2023.102284
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Article ; Online: Multiple Sources of Cholinergic Input to the Superior Olivary Complex.

Beebe, Nichole L / Zhang, Chao / Burger, R Michael / Schofield, Brett R

Frontiers in neural circuits

2021 Volume 15, Page(s) 715369

Abstract: The superior olivary complex (SOC) is a major computation center in the brainstem auditory system. Despite previous reports of high expression levels of cholinergic receptors in the SOC, few studies have addressed the functional role of acetylcholine in ... ...

Abstract	The superior olivary complex (SOC) is a major computation center in the brainstem auditory system. Despite previous reports of high expression levels of cholinergic receptors in the SOC, few studies have addressed the functional role of acetylcholine in the region. The source of the cholinergic innervation is unknown for all but one of the nuclei of the SOC, limiting our understanding of cholinergic modulation. The medial nucleus of the trapezoid body, a key inhibitory link in monaural and binaural circuits, receives cholinergic input from other SOC nuclei and also from the pontomesencephalic tegmentum. Here, we investigate whether these same regions are sources of cholinergic input to other SOC nuclei. We also investigate whether individual cholinergic cells can send collateral projections bilaterally (i.e., into both SOCs), as has been shown at other levels of the subcortical auditory system. We injected retrograde tract tracers into the SOC in gerbils, then identified retrogradely-labeled cells that were also immunolabeled for choline acetyltransferase, a marker for cholinergic cells. We found that both the SOC and the pontomesencephalic tegmentum (PMT) send cholinergic projections into the SOC, and these projections appear to innervate all major SOC nuclei. We also observed a small cholinergic projection into the SOC from the lateral paragigantocellular nucleus of the reticular formation. These various sources likely serve different functions; e.g., the PMT has been associated with things such as arousal and sensory gating whereas the SOC may provide feedback more closely tuned to specific auditory stimuli. Further, individual cholinergic neurons in each of these regions can send branching projections into both SOCs. Such projections present an opportunity for cholinergic modulation to be coordinated across the auditory brainstem.
MeSH term(s)	Acoustic Stimulation/methods ; Animals ; Auditory Pathways/chemistry ; Auditory Pathways/enzymology ; Auditory Pathways/physiology ; Choline O-Acetyltransferase/metabolism ; Cholinergic Neurons/chemistry ; Cholinergic Neurons/enzymology ; Cholinergic Neurons/physiology ; Female ; Gerbillinae ; Male ; Olivary Nucleus/chemistry ; Olivary Nucleus/enzymology ; Olivary Nucleus/physiology ; Superior Olivary Complex/chemistry ; Superior Olivary Complex/enzymology ; Superior Olivary Complex/physiology
Chemical Substances	Choline O-Acetyltransferase (EC 2.3.1.6)
Language	English
Publishing date	2021-07-15
Publishing country	Switzerland
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2452968-0
ISSN	1662-5110 ; 1662-5110
ISSN (online)	1662-5110
ISSN	1662-5110
DOI	10.3389/fncir.2021.715369
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Article ; Online: Subtypes of GABAergic cells in the inferior colliculus.

Schofield, Brett R / Beebe, Nichole L

Hearing research

2018 Volume 376, Page(s) 1–10

Abstract: The inferior colliculus occupies a central position in ascending and descending auditory pathways. A substantial proportion of its neurons are GABAergic, and these neurons contribute to intracollicular circuits as well as to extrinsic projections to ... ...

Abstract	The inferior colliculus occupies a central position in ascending and descending auditory pathways. A substantial proportion of its neurons are GABAergic, and these neurons contribute to intracollicular circuits as well as to extrinsic projections to numerous targets. A variety of types of evidence - morphology, physiology, molecular markers - indicate that the GABAergic cells can be divided into at least four subtypes that serve different functions. However, there has yet to emerge a unified scheme for distinguishing these subtypes. The present review discusses these criteria and, where possible, relates the different properties. In contrast to GABAergic cells in cerebral cortex, where subtypes are much more thoroughly characterized, those in the inferior colliculus contribute substantially to numerous long range extrinsic projections. At present, the best characterized subtype is a GABAergic cell with a large soma, dense perisomatic synaptic inputs and a large axon that provides rapid auditory input to the thalamus. This large GABAergic subtype projects to additional targets, and other subtypes also project to the thalamus. The eventual characterization of these subtypes can be expected to reveal multiple functions of these inhibitory cells and the many circuits to which they contribute.
MeSH term(s)	Animals ; Auditory Pathways/cytology ; Auditory Pathways/physiology ; Calcium-Binding Proteins/physiology ; Cell Surface Extensions/physiology ; Cell Surface Extensions/ultrastructure ; GABAergic Neurons/classification ; GABAergic Neurons/cytology ; GABAergic Neurons/physiology ; Inferior Colliculi/cytology ; Inferior Colliculi/physiology ; Models, Neurological ; Receptors, Neurotransmitter/physiology ; Vesicular Glutamate Transport Protein 2/physiology
Chemical Substances	Calcium-Binding Proteins ; Receptors, Neurotransmitter ; Vesicular Glutamate Transport Protein 2
Language	English
Publishing date	2018-10-04
Publishing country	Netherlands
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Review
ZDB-ID	282629-x
ISSN	1878-5891 ; 0378-5955
ISSN (online)	1878-5891
ISSN	0378-5955
DOI	10.1016/j.heares.2018.10.001
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Article ; Online: Perineuronal nets in subcortical auditory nuclei of four rodent species with differing hearing ranges.

Beebe, Nichole L / Schofield, Brett R

The Journal of comparative neurology

2018 Volume 526, Issue 6, Page(s) 972–989

Abstract: Perineuronal nets (PNs) are aggregates of extracellular matrix molecules that surround some neurons in the brain. While PNs occur widely across many cortical areas, subcortical PNs are especially associated with motor and auditory systems. The auditory ... ...

Abstract	Perineuronal nets (PNs) are aggregates of extracellular matrix molecules that surround some neurons in the brain. While PNs occur widely across many cortical areas, subcortical PNs are especially associated with motor and auditory systems. The auditory system has recently been suggested as an ideal model system for studying PNs and their functions. However, descriptions of PNs in subcortical auditory areas vary, and it is unclear whether the variation reflects species differences or differences in staining techniques. Here, we used two staining techniques (one lectin stain and one antibody stain) to examine PN distribution in the subcortical auditory system of four different species: guinea pigs (Cavia porcellus), mice (Mus musculus, CBA/CaJ strain), Long-Evans rats (Rattus norvegicus), and naked mole-rats (Heterocephalus glaber). We found that some auditory nuclei exhibit dramatic differences in PN distribution among species while other nuclei have consistent PN distributions. We also found that PNs exhibit molecular heterogeneity, and can stain with either marker individually or with both. PNs within a given nucleus can be heterogeneous or homogenous in their staining patterns. We compared PN staining across the frequency axes of tonotopically organized nuclei and among species with different hearing ranges. PNs were distributed non-uniformly across some nuclei, but only rarely did this appear related to the tonotopic axis. PNs were prominent in all four species; we found no systematic relationship between the hearing range and the number, staining patterns or distribution of PNs in the auditory nuclei.
MeSH term(s)	Acetylgalactosamine/metabolism ; Animals ; Auditory Cortex/physiology ; Auditory Pathways/physiology ; Guinea Pigs ; Hearing/physiology ; Male ; Mice ; Moles ; Nerve Net/physiology ; Rats ; Rats, Long-Evans ; Rodentia ; Species Specificity
Chemical Substances	Acetylgalactosamine (KM15WK8O5T)
Language	English
Publishing date	2018-01-17
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	3086-7
ISSN	1096-9861 ; 0021-9967 ; 0092-7317
ISSN (online)	1096-9861
ISSN	0021-9967 ; 0092-7317
DOI	10.1002/cne.24383
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Article ; Online: Perineuronal nets and subtypes of GABAergic cells differentiate auditory and multisensory nuclei in the intercollicular area of the midbrain.

Beebe, Nichole L / Noftz, William A / Schofield, Brett R

The Journal of comparative neurology

2020 Volume 528, Issue 16, Page(s) 2695–2707

Abstract: The intercollicular region, which lies between the inferior and superior colliculi in the midbrain, contains neurons that respond to auditory, visual, and somatosensory stimuli. Golgi studies have been used to parse this region into three distinct nuclei: ...

Abstract	The intercollicular region, which lies between the inferior and superior colliculi in the midbrain, contains neurons that respond to auditory, visual, and somatosensory stimuli. Golgi studies have been used to parse this region into three distinct nuclei: the intercollicular tegmentum (ICt), the rostral pole of the inferior colliculus (ICrp), and the nucleus of the brachium of the IC (NBIC). Few reports have focused on these nuclei, especially the ICt and the ICrp, possibly due to lack of a marker that distinguishes these areas and is compatible with modern methods. Here, we found that staining for GABAergic cells and perineuronal nets differentiates these intercollicular nuclei in guinea pigs. Further, we found that the proportions of four subtypes of GABAergic cells differentiate intercollicular nuclei from each other and from adjacent inferior collicular subdivisions. Our results support earlier studies that suggest distinct morphology and functions for intercollicular nuclei, and provide staining methods that differentiate intercollicular nuclei and are compatible with most modern techniques. We hope that this will help future studies to further characterize the intercollicular region.
MeSH term(s)	Afferent Pathways/anatomy & histology ; Afferent Pathways/physiology ; Animals ; Fluorescent Antibody Technique ; GABAergic Neurons/cytology ; Glutamate Decarboxylase/immunology ; Guinea Pigs ; Mesencephalon/anatomy & histology ; Neural Pathways/anatomy & histology ; Oligodendroglia/cytology ; Tegmentum Mesencephali/anatomy & histology ; Tegmentum Mesencephali/physiology
Chemical Substances	Glutamate Decarboxylase (EC 4.1.1.15) ; glutamate decarboxylase 1 (EC 4.1.1.15)
Language	English
Publishing date	2020-04-28
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	3086-7
ISSN	1096-9861 ; 0021-9967 ; 0092-7317
ISSN (online)	1096-9861
ISSN	0021-9967 ; 0092-7317
DOI	10.1002/cne.24926
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Article ; Online: Dense cholinergic projections to auditory and multisensory nuclei of the intercollicular midbrain.

Noftz, William A / Beebe, Nichole L / Mellott, Jeffrey G / Schofield, Brett R

Hearing research

2021 Volume 411, Page(s) 108352

Abstract: Cholinergic axons from the pedunculopontine tegmental nucleus (PPT) innervate the inferior colliculus where they are positioned to modulate both excitatory and inhibitory circuits across the central nucleus and adjacent cortical regions. More rostral ... ...

Abstract	Cholinergic axons from the pedunculopontine tegmental nucleus (PPT) innervate the inferior colliculus where they are positioned to modulate both excitatory and inhibitory circuits across the central nucleus and adjacent cortical regions. More rostral regions of the auditory midbrain include the nucleus of the brachium of the inferior colliculus (NBIC), the intercollicular tegmentum (ICt) and the rostral pole of the inferior colliculus (ICrp). These regions appear especially important for multisensory integration and contribute to orienting behavior and many aspects of auditory perception. These regions appear to receive cholinergic innervation but little is known about the distribution of cholinergic axons in these regions or the cells that they contact. The present study used immunostaining to examine the distribution of cholinergic axons and then used chemically-specific viral tracing to examine cholinergic projections from the PPT to the intercollicular areas in male and female transgenic rats. Staining with antibodies against vesicular acetylcholine transporter revealed dense cholinergic innervation throughout the NBIC, ICt and ICrp. Deposits of viral vector into the PPT labeled cholinergic axons bilaterally in the NBIC, ICt and ICrp. In each area, the projections were denser on the ipsilateral side. The axons appeared morphologically similar across the three areas. In each area, en passant and terminal boutons from these axons appeared in the neuropil and also in close apposition to cell bodies. Immunostaining with a marker for GABAergic cells suggested that the cholinergic axons likely contact both GABAergic and non-GABAergic cells in the NBIC, ICt and ICrp. Thus, the cholinergic axons could affect multisensory processing by modulating excitatory and inhibitory circuits in the NBIC, ICt and ICrp. The similarity of axons and their targets suggests there may be a common function for cholinergic innervation across the three areas. Given what is known about the PPT, such functions could be associated with arousal, sleep-wake cycle, reward and plasticity.
MeSH term(s)	Animals ; Axons ; Cholinergic Agents ; Female ; Inferior Colliculi ; Male ; Mesencephalon ; Rats ; Tegmentum Mesencephali
Chemical Substances	Cholinergic Agents
Language	English
Publishing date	2021-09-20
Publishing country	Netherlands
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	282629-x
ISSN	1878-5891 ; 0378-5955
ISSN (online)	1878-5891
ISSN	0378-5955
DOI	10.1016/j.heares.2021.108352
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Article ; Online: Anterograde Tract Tracing for Assaying Axonopathy and Transport Deficits in Glaucoma.

Crish, Samuel D / Schofield, Brett R

Methods in molecular biology (Clifton, N.J.)

2017 Volume 1695, Page(s) 171–185

Abstract: Whether to stage degeneration or investigate early pathology in glaucoma, examination of axonal structure and function is essential. There are a wide variety of methods available to investigators using animal models of glaucoma, with varying utilities ... ...

Abstract	Whether to stage degeneration or investigate early pathology in glaucoma, examination of axonal structure and function is essential. There are a wide variety of methods available to investigators using animal models of glaucoma, with varying utilities depending on the questions asked. Here, we describe the use of anterograde neuronal tract tracing using cholera toxin B (CTB) for the determination of axon transport integrity of the retinofugal projection. This method reveals the structure of the retinal axons as well as the functional integrity of anterograde transport systems.
MeSH term(s)	Animals ; Axonal Transport ; Axons/metabolism ; Axons/pathology ; Axons/physiology ; Cholera Toxin/metabolism ; Disease Models, Animal ; Glaucoma/diagnostic imaging ; Glaucoma/metabolism ; Glaucoma/physiopathology ; Humans ; Mice ; Microscopy, Confocal ; Rats ; Visual Pathways
Chemical Substances	Cholera Toxin (9012-63-9)
Language	English
Publishing date	2017-11-29
Publishing country	United States
Document type	Journal Article
ISSN	1940-6029
ISSN (online)	1940-6029
DOI	10.1007/978-1-4939-7407-8_15
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