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Open accessJournal ArticleDOI: 10.3389/FPHYS.2021.638695

Phasic Neuronal Firing in the Rodent Nucleus of the Solitary Tract ex vivo.

02 Mar 2021-Frontiers in Physiology (Frontiers Media SA)-Vol. 12, pp 638695-638695
Abstract: Phasic pattern of neuronal activity has been previously described in detail for magnocellular vasopressin neurons in the hypothalamic paraventricular and supraoptic nuclei. This characteristic bistable pattern consists of alternating periods of electrical silence and elevated neuronal firing, implicated in neuropeptide release. Here, with the use of multi-electrode array recordings ex vivo, we aimed to study the firing pattern of neurons in the nucleus of the solitary tract (NTS) - the brainstem hub for homeostatic, cardio-vascular, and metabolic processes. Our recordings from the mouse and rat hindbrain slices reveal the phasic activity pattern to be displayed by a subset of neurons in the dorsomedial NTS subjacent to the area postrema (AP), with the inter-spike interval distribution closely resembling that reported for phasic magnocellular vasopressin cells. Additionally, we provide interspecies comparison, showing higher phasic frequency and firing rate of phasic NTS cells in mice compared to rats. Further, we describe daily changes in their firing rate and pattern, peaking at the middle of the night. Last, we reveal these phasic cells to be sensitive to α 2 adrenergic receptors activation and to respond to electrical stimulation of the AP. This study provides a comprehensive description of the phasic neuronal activity in the rodent NTS and identifies it as a potential downstream target of the AP noradrenergic system.

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Topics: Solitary tract (55%), Premovement neuronal activity (55%), Neuropeptide (52%) ... read more
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8 results found


Journal ArticleDOI: 10.1113/JP281596
Abstract: Recently, we found the dorsal vagal complex to display autonomous circadian timekeeping properties The dorsal motor nucleus of the vagus (DMV) is an executory part of this complex - a source of parasympathetic innervation of the gastrointestinal tract Here, we reveal daily changes in the neuronal activities of the rat DMV, including firing rate, intrinsic excitability and synaptic input - all of these peaking at the late day Additionally, we establish that short term high-fat diet disrupts these daily rhythms, boosting the variability in the firing rate, but blunting the DMV responsiveness to ingestive cues These results help us better understand daily control over parasympathetic outflow and provide evidence on their dependence on the high-fat diet ABSTRACT: The suprachiasmatic nuclei (SCN) of the hypothalamus functions as the brain's primary circadian clock, but circadian clock genes are also rhythmically expressed in several extra-SCN brain sites where they can exert local temporal control over physiology and behaviour. Recently, we found that the hindbrain dorsal vagal complex possesses strong daily timekeeping capabilities, with the area postrema and nucleus of the solitary tract exhibiting the most robust clock properties. The possibility that the executory part of this complex - the dorsal motor nucleus of the vagus (DMV), also exhibits daily changes has not been extensively studied. The DMV is the source of vagal efferent motoneurons that regulate gastric motility and emptying and consequently influence meal size and energy homeostasis. We used a combination of multi-channel electrophysiology and patch clamp recordings to gain insight into effects of time of day and diet on these DMV cells. We found that DMV neurons increase their spontaneous activity, excitability and responsiveness to metabolic neuromodulators at late day and this was paralleled with an enhanced synaptic input to these neurons. A high-fat diet typically damps circadian rhythms, but we found that consumption of a high-fat diet paradoxically amplified daily variation of DMV neuronal activity, while blunting their responsiveness to metabolic neuromodulators. In summary, we show for the first time that DMV neural activity changes with time of day with this temporal variation modulated by diet. These findings have clear implications for our understanding of the daily control of vagal efferents and parasympathetic outflow. This article is protected by copyright. All rights reserved.

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Topics: Dorsal motor nucleus (60%), Area postrema (53%), Premovement neuronal activity (52%) ... read more

3 Citations


Open accessJournal ArticleDOI: 10.1016/J.BRAINRES.2021.147603
Lukasz Chrobok1, Anna Alwani1, Kamil Pradel1, Jasmin Daniela Klich1  +1 moreInstitutions (1)
13 May 2021-Brain Research
Abstract: Pronounced environmental changes between the day and night led to evolution of specialised mechanisms organising their daily physiology, named circadian clocks. Currently, it has become clear that the master clock in the suprachiasmatic nuclei of the hypothalamus is not an exclusive brain site to generate daily rhythms. Indeed, several brain areas, including the subcortical visual system have been recently shown to change their neuronal activity across the daily cycle. Here we focus our investigation on the olivary pretectal nucleus (OPN) – a retinorecipient structure primarily involved in the pupillary light reflex. Using the multi-electrode array technology ex vivo we provide evidence for OPN neurons to elevate their firing during the behaviourally quiescent light phase. Additionally, we report the robust responsivity to orexin A via the identified OX2 receptor in this pretectal centre, with higher responsiveness noted during the night. Interestingly, we likewise report a daily variation in the response to PAC1 receptor activation, with implications for the convergence of orexinergic and visual input on the same OPN neurons. Altogether, our report is first to suggest a daily modulation of the OPN activity via intrinsic and extrinsic mechanisms, organising its temporal physiology.

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Topics: Orexin-A (54%), Orexin (52%), Premovement neuronal activity (51%) ... read more

2 Citations


Open accessPosted ContentDOI: 10.1002/JNR.24973
Lukasz Chrobok1, Kamil Pradel1, Marcelina Janik1, Anna M Sanetra1  +7 moreInstitutions (2)
Abstract: Circadian rhythmicity in mammals is sustained by the central brain clock-the suprachiasmatic nucleus of the hypothalamus (SCN), entrained to the ambient light-dark conditions through a dense retinal input. However, recent discoveries of autonomous clock gene expression cast doubt on the supremacy of the SCN and suggest circadian timekeeping mechanisms devolve to local brain clocks. Here, we use a combination of molecular, electrophysiological, and optogenetic tools to evaluate intrinsic clock properties of the main retinorecipient thalamic center-the lateral geniculate nucleus (LGN) in male rats and mice. We identify the dorsolateral geniculate nucleus as a slave oscillator, which exhibits core clock gene expression exclusively in vivo. Additionally, we provide compelling evidence for intrinsic clock gene expression accompanied by circadian variation in neuronal activity in the intergeniculate leaflet and ventrolateral geniculate nucleus (VLG). Finally, our optogenetic experiments propose the VLG as a light-entrainable oscillator, whose phase may be advanced by retinal input at the beginning of the projected night. Altogether, this study for the first time demonstrates autonomous timekeeping mechanisms shaping circadian physiology of the LGN.

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Topics: Suprachiasmatic nucleus (62%), Circadian clock (58%), Lateral geniculate nucleus (57%) ... read more

2 Citations


Open accessJournal ArticleDOI: 10.1113/JP281838
Abstract: Temporal partitioning of daily food intake is crucial for survival and involves the integration of internal circadian states and external influences such as the light-dark cycle and dietary composition. These intrinsic and extrinsic factors are interdependent with misalignment of circadian rhythms promoting body weight gain, while consumption of a calorie-dense diet elevates the risk of obesity and blunts circadian rhythms. Recently, we defined the circadian properties of the dorsal vagal complex of the brainstem, a structure implicated in the control of food intake and autonomic tone, but whether and how 24 h rhythms in this area are influenced by diet remains unresolved. Here we focused on a key structure of this complex, the nucleus of the solitary tract (NTS). We used a combination of immunohistochemical and electrophysiological approaches together with daily monitoring of body weight and food intake to interrogate how the neuronal rhythms of the NTS are affected by a high-fat diet. We report that short-term consumption of a high-fat diet increases food intake during the day and blunts NTS daily rhythms in neuronal discharge. Additionally, we found that a high-fat diet dampens NTS responsiveness to metabolic neuropeptides, and decreases orexin immunoreactive fibres in this structure. These alterations occur without prominent body weight gain, suggesting that a high-fat diet acts initially to reduce activity in the NTS to disinhibit mechanisms that suppress daytime feeding. KEY POINTS: The dorsal vagal complex of the rodent hindbrain possesses intrinsic circadian timekeeping mechanisms In particular, the nucleus of the solitary tract (NTS) is a robust circadian oscillator, independent of the master suprachiasmatic clock Here, we reveal that rat NTS neurons display timed daily rhythms in their neuronal activity and responsiveness to ingestive cues These daily rhythms are blunted or eliminated by a short-term high-fat diet, together with increased consumption of calories during the behaviourally quiescent day Our results help us better understand the circadian control of satiety by the brainstem and its malfunctioning under a high-fat diet.

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Topics: Circadian rhythm (56%), Circadian clock (56%), Solitary tract (52%)

2 Citations


Open accessPosted ContentDOI: 10.1101/2021.05.11.443625
Lukasz Chrobok1, Anna Alwani1, Kamil Pradel1, Jasmin Daniela Klich1  +1 moreInstitutions (1)
13 May 2021-bioRxiv
Abstract: Pronounced environmental changes between the day and night forced living organisms to evolve specialised mechanisms organising their daily physiology, named circadian clocks. Currently, it has become clear that the master clock in the suprachiasmatic nuclei of the hypothalamus is not an exclusive brain site to generate daily rhythms. Indeed, several brain areas, including the subcortical visual system have been recently shown to change their neuronal activity across the daily cycle. Here we focus our investigation on the olivary pretectal nucleus (OPN) - a retinorecipient structure primarily involved in the pupillary light reflex. Using the multi-electrode array technology ex vivo we provide evidence for OPN neurons to elevate their firing during the behaviourally quiescent light phase. Additionally, we report the robust sensitivity to orexin A via the identified OX2 receptor in this pretectal centre, with higher responsiveness noted during the night. Interestingly, we likewise report a daily variation in the response to PAC1 receptor activation, with implications for the convergence of orexinergic and visual input on the same OPN neurons. Altogether, our report is first to suggest a daily modulation of the OPN activity via intrinsic and extrinsic mechanisms, organising its temporal physiology.

... read more

Topics: Orexin-A (54%), Premovement neuronal activity (51%)

References
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53 results found


Journal ArticleDOI: 10.1002/CNE.902340306
Abstract: We applied the neuroanatomical tracers cholera toxin-horseradish peroxidase and wheat germ agglutinin-horseradish peroxidase to investigate the neural connections of the area postrema (AP) in the rat. We find that the AP projects to the nucleus of the solitary tract (NTS) and dorsal motor nucleus of the vagus bilaterally both rostral and caudal to obex; the nucleus ambiguus; the dorsal aspect of the spinal trigeminal tract and nucelus and the paratrigeminal nucleus; the region of the ventrolateral medullary catecholaminergic column; the cerebellar vermis; and a cluster of structures in the dorsolateral pons which prominently include a discrete set of subnuclei in the lateral parabrachial nucleus. The major central afferent input to the area postrema is provided by a group of neurons in the paraventricular and dorsomedial hypothalamic nuclei whose collective dendrites describe a horizontally oriented plexus which encircles the parvocellular nucleus of the hypothalamus bilaterally. In addition, the caudal NTS may project lightly to the AP. The lateral parabrachial nucleus provides a very light input as well. These connections, when considered in the context of the known vagal afferent input and reduced blood-brain barrier of AP, place this structure in a unique position to receive and modulate ascending interoceptive information and to influence autonomic outflow as well.

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Topics: Dorsal motor nucleus (66%), Lateral parabrachial nucleus (65%), Parabrachial Nucleus (64%) ... read more

493 Citations


Open accessJournal ArticleDOI: 10.1113/JPHYSIOL.1979.SP012781
Abstract: 1. Isolated rat neural lobes were incubated in vitro and electrically stimulated to release vasopressin. The released vasopressin was assayed using a radioimmunoassay and there was a reasonably good correlation (r = 0.81) between results obtained with this assay and those obtained by bioassay with the rat blood pressure method. 2. Regular stimulation at frequencies of 5, 10 and 20 Hz released progressively more vasopressin and the release could be blocked by addition of tetrodotoxin to the incubation medium. 3. Stimulation with pulse patterns derived from tape recordings of phasically firing units in the supraoptic nucleus of dehydrated rats released more vasopressin than the same number of pulses regularly spaced in time. In the range 2-8 pulses/sec vasopressin release was related to the pulse frequency within the bursts (r = 0.90) and the number of short (< 100 msec) interpulse intervals (r = 0.92). Vasopressin released per pulse increased over the frequency range 3-6 pulses/sec, but above 6 pulses/sec vasopressin release per pulse tended to diminish. 4. We conclude that phasic firing of vasopressin neurosecretory cells may enhance vasopressin release in vivo and that an important factor in determining release is the number of short interspike intervals.

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Topics: Vasopressin (61%), Supraoptic nucleus (56%)

340 Citations


Journal ArticleDOI: 10.1002/CNE.901300402
D. K. Morest1Institutions (1)
Abstract: Projections from the area postrema and adjacent parts of the medial solitary nucleus are demonstrated with the Nauta method following lesions limited exclusively to these structures. Experiments are controlled with lesions involving adjacent bulbar regions, cerebellum, and spinal cord. Ascending pathways in the dorsal and lateral columns of the spinal cord project ipsilaterally to the area postrema and bilaterally to a para-alar nucleus in the ventral periphery of the nucleus gracilis. Neurons in the area postrema project mainly inspilaterally to the dorsal and medial regions of the medial solitary nucleus. Neurons in the posterior half of the medical solitary nucleus project ipsilaterally to the lateral solitary nucleus, dorsal vagal nucleus, ambigus, retrofacial nucleus, and dorsal and lateral bulbar reticular formation. Projections to nuclei intercalatus and prepositus hypoglossi, bilaterally, and to the ipsilateral dorsal tegmental nucleus by way of the dorsal longitudinal fasciculus are also shown. No direct projections to the diencephalon are demonstrated. Control lesions in the dorsal column nuclei reveal projections to the contralateral inferior olive and thalamic reticular and ventrobasal nuclei, but not to the projection sites of the solitary nucleus. Evidence is given to support the hypothesis that ascening visceral pathways are interruped in the bulbar reticular formation and dorsal tegmental nucleus before reaching the diencephalon. Correlations are suggested with functional aspects of the central autonomic and reticular activating systems.

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335 Citations


Open accessJournal ArticleDOI: 10.1016/J.CMET.2012.06.015
Harvey J. Grill1, Matthew R. Hayes1Institutions (1)
05 Sep 2012-Cell Metabolism
Abstract: This Review highlights the processing and integration performed by hindbrain nuclei, focusing on the inputs received by nucleus tractus solitarius (NTS) neurons. These inputs include vagally mediated gastrointestinal satiation signals, blood-borne energy-related hormonal and nutrient signals, and descending neural signals from the forebrain. We propose that NTS (and hindbrain neurons, more broadly) integrate these multiple energy status signals and issue-output commands controlling the behavioral, autonomic, and endocrine responses that collectively govern energy balance. These hindbrain-mediated controls are neuroanatomically distributed; they involve endemic hindbrain neurons and circuits, hindbrain projections to peripheral circuits, and projections to and from midbrain and forebrain nuclei.

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Topics: Forebrain (60%), Hindbrain (57%), Midbrain (51%)

307 Citations


Journal ArticleDOI: 10.1016/S0301-0082(98)00072-0
Abstract: Magnocellular oxytocin and vasopressin cells are among the most extensively studied neurons in the brain; their large size and high synthetic capacity, their discrete, homogeneous distribution and the anatomical separation of their terminals from their cell bodies, and the ability to determine their neuronal output readily by measurements of hormone concentration in the plasma, combine to make these systems amenable to a wide range of fundamental investigations. While vasopressin cells have intrinsic burst-generating properties, oxytocin cells are organized within local pattern-generating networks. In this review we consider the role played by particular afferent pathways in the regulation of the activity of oxytocin and vasopressin cells. For both cell types, the effects of changes in the activity of synaptic input can be complex.

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Topics: Vasopressin (56%), Oxytocin (54%), Cell type (51%)

299 Citations


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