Thalamic- and cerebellar-projecting interpolaris neuron responses to afferent inputs

Ohya, Atsushi; Tsuruoka, Masayoshi; Imai, Eiichi; Fukunaga, Hideki; Shinya, Akiyuki; Furuya, Ryoichi; Kawawa, Tadaharu; Matsui, Yoichiro

doi:10.1016/0361-9230(93)90163-6

Cited by 22 publications

(8 citation statements)

References 31 publications

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“…Previous studies have shown that some neurons in Vi can be activated from the masseter muscle. In the rat, Ohya and coworkers (Ohya, 1992;Ohya et al, 1993) have shown that some neurons in Vi can be activated by light brushing of the masseter muscle and that some of these neurons project to the thalamus. In the cat, neurons located in Vi and the border of Vi with the reticular formation have been reported that respond to electrical stimulation of the masseter nerve and stretching of the masticatory muscles (Hayashi et al, 1984;Capra et al, 1994).…”

Section: Discussionmentioning

confidence: 99%

Inputs from identified jaw‐muscle spindle afferents to trigeminothalamic neurons in the rat: A double‐labeling study using retrograde HRP and intracellular biotinamide

Luo

Dessem

1995

J of Comparative Neurology

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Projections from physiologically identified jaw-muscle spindle afferents onto trigeminothalamic neurons were studied in the rat. Trigeminothalamic neurons were identified by means of retrograde transport of horseradish peroxidase from the ventroposteromedial nucleus of the thalamus. Labeled neurons were found contralaterally in the supratrigeminal region (Vsup), the trigeminal principal sensory nucleus, the ventrolateral part of the trigeminal subnucleus oralis, the spinal trigeminal subnuclei interpolaris and caudalis, the reticular formation, and an area ventral to the trigeminal motor nucleus (Vmo) and medial to the trigeminal principal sensory nucleus (AVM). Jaw-muscle spindle afferents were physiologically identified by their increased firing during stretching of the jaw muscles and intracellularly injected with biotinamide. Axon collaterals and boutons from jaw-muscle spindle afferents were found in Vmo; Vsup; the dorsomedial part of the trigeminal principal sensory nucleus (Vpdm); the dorsomedial part of the spinal trigeminal subnuclei oralis, interpolaris (Vidm) and caudalis; the parvicellular reticular formation (PCRt); and the mesencephalic trigeminal nucleus. Trigeminothalamic neurons in Vsup, Vpdm, Vidm, PCRt, and AVM were associated with axon collaterals and boutons from intracellularly stained jaw-muscle spindle afferents. Trigeminothalamic neurons in Vsup, Vpdm, Vidm, and PCRt were closely apposed by one to 14 intracellularly labeled boutons from jaw-muscle spindle afferents, suggesting a powerful input to some trigeminothalamic neurons. These data demonstrate that muscle length and velocity feedback from jaw-muscle spindle afferents is projected to the contralateral thalamus via multiple regions of the trigeminal system and implicates these pathways in the projection of trigeminal proprioceptive information to the cerebral cortex.

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Section: Discussionmentioning

confidence: 99%

Inputs from identified jaw‐muscle spindle afferents to trigeminothalamic neurons in the rat: A double‐labeling study using retrograde HRP and intracellular biotinamide

Luo

Dessem

1995

J of Comparative Neurology

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“…Single units in the region of Vi that respond to electrical stimulation of the masseter nerve or stretching of the jaw-elevator muscles have been reported in cats (Hayashi et al, 1984;Capra et al, 1994). In rats, Ohya and coworkers (Ohya, 1992;Ohya et al, 1993) reported that some units in this region respond to light brushing of the masseter muscle. Although the responses described in these studies are consistent with a projection of masticatory muscle afferents to Vi, these studies failed to characterize the neuronal responses sufficiently to identify them as originating from jaw-muscle spindles.…”

Section: The Projection Of Jaw-muscle Spindle Afferents To the Caudalmentioning

confidence: 99%

“…Anatomical studies have demonstrated that many neurons in Vi project to the contralateral ventroposterior thalamus (Fukushima and Kerr, 1979;Erzurumlu et al, 1980). Electrophysiological studies (Ohya, 1992;Ohya et al, 1993) and combined anatomical and electrophysiological studies (Luo and Dessem, 1995) provide evidence that some neurons in Vi receive jaw-muscle spindle input and project to the contralateral thalamus in the rat. Neurons distributed throughout Vi also project to orofacial regions of the cerebellum (Watson and Switzer, 1978;Phelan and Falls, 1991), creating the possibility of a relay of spindle information from Vi to the cerebellum.…”

Section: The Projection Of Jaw-muscle Spindle Afferents To the Caudalmentioning

confidence: 99%

Projection of jaw‐muscle spindle afferents to the caudal brainstem in rats demonstrated using intracellular biotinamide

Luo

Wong

Dessem

1995

J of Comparative Neurology

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Intracellular staining with biotinamide was used to study the axonal projection and synaptic morphology of rat jaw-muscle spindle afferents. Intracellular recordings in the mesencephalic trigeminal nucleus (Vme) were identified as spindle afferent responses by their increased firing during stretching of the jaw-elevator muscles. Biotinamide-stained axon collaterals with boutons were found in the trigeminal motor nucleus (Vmo), Vme, the region dorsal to Vmo including the supratrigeminal region, the dorsomedial portion of the trigeminal principal sensory nucleus, and the dorsomedial part of the rostral spinal trigeminal subnucleus oralis. Additional, previously undescribed projections of jaw-muscle spindle afferents were found to the dorsomedial portion of the caudal spinal trigeminal subnucleus oralis (Vodm), the dorsomedial part of the spinal trigeminal subnucleus interpolaris (Vidm), the caudal parvicellular reticular formation, laminae IV and V of the spinal trigeminal subnucleus caudalis (Vc), and the dorsal division of the medullary reticular field. Labeled spindle boutons in Vodm formed predominately axodendritic synapses. Some of these boutons received presynaptic inputs from unlabeled P-type boutons containing clear, spherical, or flattened vesicles. In Vidm, labeled collaterals and boutons were densely clustered into glomerular-like structures. Labeled boutons in Vidm made axodendritic, axosomatic, and axoaxonic synapses and received synaptic contacts from unlabeled boutons containing clear, spherical, or flat and pleomorphic vesicles. Unlabeled presynaptic boutons in Vidm occasionally contained dense core vesicles. Labeled boutons in Vc mainly formed synaptic contacts with large diameter dendrites. This projection of jaw-muscle spindle afferents to caudal brainstem regions may play a significant role in masticatory-muscle stretch reflexes and in the integration of trigeminal proprioceptive information and its transmission to higher centers.

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“…The trigeminal nuclear complex is a major relay in the processing of orofacial nociceptive information. Although Vc has been most extensively studied (for review, see Sessle and Greenwood, 1976;Hu et al, 1981;Dubner and Bennett, 1983), the more rostral subnuclei interpolaris and oralis are also involved (Greenwood and Sessle, 1976;Sessle and Greenwood, 1976;Nord and Young, 1979;Hu et al, 1981Hu et al, , 1992Hayashi et al, 1984;Hu and Sessle, 1984;Hayashi and Tabata, 1989;Dallel et al, 1990Dallel et al, , 1996Jacquin and Rhoades, 1990;Raboisson et al, 1991;Ohya, 1992;Ohya et al, 1993). Vc processes information from mechanosensitive, proprioceptive, thermosensitive, and nociceptive fibers originating in the orofacial region (Hu et al, 1981;Sessle et al, 1981;Bushnell et al, 1984;Hu, 1990;Chiang et al, 1994;McHaffie et al, 1994;Raboisson et al, 1995), including the oral cavity (Kruger and Michel, 1962;Yokota, 1975;Amano et al, 1986;Strassman and Voss, 1993;C arstens et al, 1995, nasal sinus (Cain and Murphy, 1980;Garcia Medina and C ain, 1982;Cometto-Muñiz and Noriega, 1985;Stevens and C ain, 1986;Anton et al, 1991aAnton et al, ,b, 1992Thürauf et al, 1991…”

Section: Activation Of Vc Neurons By Carbonated Watermentioning

confidence: 99%

Neurobiological and Psychophysical Mechanisms Underlying the Oral Sensation Produced by Carbonated Water

Simons

Dessirier

Carstens³

et al. 1999

J. Neurosci.

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Carbonated drinks elicit a sensation that is highly sought after, yet the underlying neural mechanisms are ill-defined. We hypothesize that CO(2) is converted via carbonic anhydrase into carbonic acid, which excites lingual nociceptors that project to the trigeminal nuclei. We investigated this hypothesis using three methodological approaches. Electrophysiological methods were used to record responses of single units located in superficial laminae of the dorsomedial aspect of trigeminal subnucleus caudalis (Vc) evoked by lingual application of carbonated water in anesthetized rats. After pretreatment of the tongue with the carbonic anhydrase inhibitor dorzolamide, neuronal responses to carbonated water were significantly attenuated, followed by recovery. Using c-Fos immunohistochemistry, we investigated the distribution of brainstem neurons activated by intraoral carbonated water. Fos-like immunoreactivity (FLI) was significantly higher in the superficial laminae of dorsomedial and ventrolateral Vc in animals treated with carbonated water versus controls. Dorzolamide pretreatment significantly reduced FLI in dorsomedial Vc. We also examined the sensation elicited by carbonated water in human psychophysical studies. When one side of the tongue was pretreated with dorzolamide, followed by bilateral application of carbonated water, a significant majority of subjects chose the untreated side as having a stronger sensation and assigned significantly higher intensity ratings to that side. Dorzolamide did not reduce irritation elicited by pentanoic acid. The present data support the hypothesis that carbonated water excites lingual nociceptors via a carbonic anhydrase-dependent process, in turn exciting neurons in Vc that are presumably involved in signaling oral irritant sensations.

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Thalamic- and cerebellar-projecting interpolaris neuron responses to afferent inputs

Cited by 22 publications

References 31 publications

Inputs from identified jaw‐muscle spindle afferents to trigeminothalamic neurons in the rat: A double‐labeling study using retrograde HRP and intracellular biotinamide

Inputs from identified jaw‐muscle spindle afferents to trigeminothalamic neurons in the rat: A double‐labeling study using retrograde HRP and intracellular biotinamide

Projection of jaw‐muscle spindle afferents to the caudal brainstem in rats demonstrated using intracellular biotinamide

Neurobiological and Psychophysical Mechanisms Underlying the Oral Sensation Produced by Carbonated Water

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