Comparisons of Neuronal and Excitatory Network Properties between the Rat Brainstem Nuclei that Participate in Vertical and Horizontal Gaze Holding

Saito, Yasuhiko; Sugimura, Tomoko; Yanagawa, Yuchio

doi:10.1523/eneuro.0180-17.2017

Cited by 6 publications

(5 citation statements)

References 83 publications

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“…Therefore, the sustained activity responsible for horizontal and vertical eye position signals may be maintained by reciprocal loops in the PHN-VN and INC-VN networks, respectively (Evinger et al, 1977;Cannon and Robinson, 1987;McFarland and Fuchs, 1992;Sylvestre et al, 2003). Our present and previous studies demonstrated that sustained EPSC responses, indicating local excitatory networks, occurred in reduced preparations in which the connections to the VNs were discontinued (Saito and Yanagawa, 2010;Saito et al, 2017). These findings suggest that recurrent excitatory networks that produce sustained EPSC responses are deployed within the PHN and the INC.…”

Section: Discussionsupporting

confidence: 64%

“…All experimental procedures were approved by the Animal Care Committee of Nara Medical University, and the experiments were conducted in accordance with the guidelines outlined by the US National Institutes of Health regarding the care and use of animals for experimental research. Although our previous studies were performed in slice preparations obtained from Wistar rats (Saito and Yanagawa, 2010;Saito et al, 2017), we used slices obtained from Long-Evans rats of either sex in this study because pigmented rats have higher visual acuity than albino rats (Birch and Jacobs, 1979;Prusky et al, 2002). A total of 30 Long-Evans rats (18 -21 postnatal days old) were used in this study.…”

Section: Methodsmentioning

confidence: 99%

“…The slice preparation and whole-cell patch-clamp recording procedures were similar to those described previously (Saito and Yanagawa, 2010;Saito et al, 2017). Briefly, the rat was deeply anesthetized with isoflurane and decapitated.…”

Section: Slice Preparation and Whole-cell Recordingmentioning

confidence: 99%

“…In contrast to the accumulating findings regarding the PHN, there has been no report regarding the local networks in the INC. In our recent study (Saito et al, 2017), we examined excitatory networks in the INC by using the same experimental procedure used in the PHN study and found that the sustained EPSC responses also occurred in the INC. However, the effect of a CP-AMPA receptor antagonist on the sustained EPSC response was significantly smaller in the INC than in the PHN.…”

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Different Activation Mechanisms of Excitatory Networks in the Rat Oculomotor Integrators for Vertical and Horizontal Gaze Holding

Saito

Sugimura

2019

eNeuro

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Gaze holding in the horizontal and vertical directions is separately controlled via the oculomotor neural integrators, the prepositus hypoglossi nucleus (PHN) and the interstitial nucleus of Cajal (INC), respectively. Our previous in vitro studies demonstrated that transient, high-frequency local stimulation of the PHN and the INC increased Significance Statement Position signals necessary for gaze holding are produced from velocity signals by mathematical integration via brainstem oculomotor integrators, which are separated into horizontal and vertical integrators. Although excitatory networks in the integrators are essential for their functions, the mechanisms of sustained activation in their networks have not been clarified. This study reports that the activation of excitatory networks in the horizontal integrator is mediated predominantly via Ca 2ϩ-permeable AMPA receptors and Ca 2ϩ-activated nonselective cation channels, while their activation in the vertical integrator is mediated predominantly via NMDA receptors. This result strongly suggests that excitatory networks are activated via different synaptic mechanisms between horizontal and vertical integrators.

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Section: Discussionsupporting

confidence: 64%

Section: Methodsmentioning

confidence: 99%

Section: Slice Preparation and Whole-cell Recordingmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Different Activation Mechanisms of Excitatory Networks in the Rat Oculomotor Integrators for Vertical and Horizontal Gaze Holding

Saito

Sugimura

2019

eNeuro

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“…The analysis of the relationship between the firing rate before ATP application and the effects of ATP on the firing rate revealed that the firing rate of neurons that exhibited a decrease to zero was significantly smaller than the firing rate of neurons that exhibited an increase or decrease (Figure c2). Although we did not identify the neuronal types in this study, PHN neurons that exhibit a firing pattern with few spikes during the 400‐ms current injection show a low spontaneous firing rate (Saito, Sugimura, & Yanagawa, ; Saito et al., ; Shino, Ozawa, Furuya, & Saito, ; Shino et al., ; Zhang et al., ). Therefore, ATP may completely inhibit the firing of this type of PHN neuron.…”

Section: Discussionmentioning

confidence: 97%

Purinergic modulation of neuronal activity in the rat prepositus hypoglossi nucleus

Sugioka

Saito

2018

Eur J of Neuroscience

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In the nervous system, adenosine 5′‐trisphosphate (ATP) functions as a neurotransmitter and binds to ionotropic P2X receptors and metabotropic P2Y receptors. Although ATP receptors are expressed in the prepositus hypoglossi nucleus (PHN), which is a brainstem structure involved in controlling horizontal gaze, it is unclear whether ATP indeed affects the activity of PHN neurons. In this study, we investigated the effects of ATP on spontaneous firing of PHN neurons using whole‐cell recordings in rat brainstem slices. Bath application of ATP increased or decreased the spontaneous firing rate of the neurons in a dose‐dependent manner, indicating that ATP indeed affects PHN neuronal activity. To clarify the mechanisms of the ATP effects, we investigated the current responses of PHN neurons to a local application of ATP. The ATP application induced a fast inward (FI) current, a slow inward (SI) current, and/or a slow outward (SO) current in the neurons. The agonists of P2X and P2Y receptors induced FI and SI currents, respectively. The SO currents were not induced by the ATP agonists but were induced by adenosine, which may be extracellularly converted from ATP by ectonucleotidases. An antagonist of adenosine P1 (A1) receptors abolished the adenosine‐induced SO currents and bath application of adenosine decreased the spontaneous firing rate of all PHN neurons tested. These results indicate that PHN neurons express functional purinoceptors and show that the FI, SI, and SO currents were mediated via P2X, P2Y, and A1 receptors, respectively.

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Noradrenergic current responses of neurons in rat oculomotor neural integrators

Saito,

Sugimura

2024

Journal of Neurophysiology

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The prepositus hypoglossi nucleus (PHN) and the interstitial nucleus of Cajal (INC) are involved in the control of horizontal and vertical gaze, respectively. A previous study showed that PHN neurons exhibit depolarized or hyperpolarized responses to noradrenaline (NA). However, the adrenoceptor types that participate in NA-induced responses and the effects of NA on INC neurons have not yet been investigated. Furthermore, the relationship between NA-induced responses and neuron types defined by neurotransmitter phenotypes has not been determined. In this study, we investigated NA-induced current responses in PHN and INC neurons and the relationships between these responses and neuron types using whole-cell recordings in wild-type and transgenic rat brainstem slices. Local application of NA to the cell soma induced slow inward (SI) and slow outward (SO) currents that were mainly mediated by α1 and α2 adrenoceptors, respectively. These current responses were observed in both PHN and INC neurons, although the proportion of INC neurons that responded to NA was low. Analyses of the distributions of the current responses revealed that in the PHN, all fluorescently identified inhibitory neurons exhibited SI currents, whereas glutamatergic and cholinergic neurons exhibited both SI and SO currents. In the INC, glutamatergic and inhibitory neurons preferentially exhibited SI and SO currents, respectively. When the PHN and INC neurons were characterized by their firing pattern, we found that the proportions of the currents depended on their firing pattern. These results suggest that various modes of noradrenergic modulation in horizontal and vertical neural integrators are dependent on neuron type.

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Comparisons of Neuronal and Excitatory Network Properties between the Rat Brainstem Nuclei that Participate in Vertical and Horizontal Gaze Holding

Abstract: Visual Abstract

Cited by 6 publications

References 83 publications

Different Activation Mechanisms of Excitatory Networks in the Rat Oculomotor Integrators for Vertical and Horizontal Gaze Holding

Different Activation Mechanisms of Excitatory Networks in the Rat Oculomotor Integrators for Vertical and Horizontal Gaze Holding

Purinergic modulation of neuronal activity in the rat prepositus hypoglossi nucleus

Noradrenergic current responses of neurons in rat oculomotor neural integrators

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