Chem. Senses 24: 655-664,
1999
© Oxford University Press 1999
Intramedullary Projections of the Rostral Nucleus of the Solitary Tract in the Rat: Gustatory Influences on Autonomic Output
Department of Animal Physiology, Groningen Graduate School for Behavioral and Cognitive Neurosciences (BCN), University of Groningen, The Netherlands 1 Department of Behavioral Biology,Groningen Graduate School for Behavioral and Cognitive Neurosciences (BCN), University of Groningen, The Netherlands
Correspondence to be sent to: C. Streefland, Department of Neurology, PO Box 30001, 9700 RB Groningen, The Netherlands. e-mail:c.streefland{at}neuro.azg.nl
 |
Abstract |
|---|
 Top Abstract IntroductionMaterials and methodsResultsDiscussionReferences |
|---|
The efferent connections of the rostral nucleus of the solitary tract (NTS) in the rat were studied by anterograde transport of Phaseolus vulgaris leucoagglutinin. Rostral to the injection site, fibers travel through the rostral parvocellular reticular formation and deflect medially or laterally around the motor trigeminal nucleus, giving off few terminals in these nuclei and terminate in the parabrachial nucleus. Moderate projections to the peritrigeminal zone, including the intertrigeminal nucleus and the dorsal subcoeruleus nucleus, were observed. Caudally to the injection site, dense innervations from the rostral nucleus of the solitary tract were detected in the parvocellular reticular formation ventral and caudal to the injection site and in the intermediate and ventral medullary reticular formation. The rostral central and ventral subdivisions of the NTS up to the level where the nucleus of the solitary tract abuts the fourth ventricle and the hypoglossal nucleus, receive moderate input from the rostral nucleus of the solitary tract. In general, the projections from the rostral nucleus of the solitary tract were bilateral with an ipsilateral predominance. The caudal part of the nucleus of the solitary tract, the dorsal motor nucleus of the vagus and the facial nucleus were not labeled. It is concluded that medullary rNTS projections participate in oral motor behavior and autonomic control of abdominal organs.
|
Introduction |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
The nucleus of the solitary tract (NTS) is the major integrative visceral sensory relay nucleus in the brainstem. It is the principal recipient of first-order gustatory afferents and visceral afferents from gut, hepatic and pancreatic receptors.
Gustatory information synapses in the rostral NTS (rNTS) and is disseminated by the rNTS
along
two major pathways. An ascending pathway projects in rodents via the parabrachial nucleus
(PBN) to
several forebrain nuclei, including the thalamus, gustatory neocortex, lateral hypothalamus,
amygdala
and bed nucleus of the stria terminalis (Ricardo and Koh, 1978
; Ter Horst et al., 1989; Herbert et al., 1990; Ter Horst and Streefland, 1993). The second major pathway
is locally
directed and largely confined to the medulla. These intramedullary connections link oral afferent
nerves
to the orofacial motor nuclei involved in ingestive behavior and rejection responses (Norgren, 1978; Travers, 1988; Beckman and
Whitehead, 1991; Ter Horst et al., 1991; Ergene et al., 1994).
Apart from ascending and local projections, the NTS subserves a major visceral efferent
function
via regulation of autonomic mechanisms (Norgren, 1981, 1985; Strack et al., 1989; Cechetto, 1991; Loewy and Haxhiu, 1993; Streefland et al.,
1998) (C. Streefland et al., submitted for publication), including vagal
parasympathetic and sympathoadrenal control. Within the NTS, gustatory information may be
integrated with incoming visceral afferent responses and thereby influence general autonomic
responses.
Gustatory stimulation can induce a number of autonomic changes, such as pancreatic insulin
release (Strubbe and Steffens, 1975; Strubbe and Bouman,
1978). It is obvious that the neuroanatomical architecture of gustatorily induced and
vagally
mediated responses involves the rNTS and the dorsal motor nucleus of the vagus (DMnX).
Furthermore, it is confined to the medulla, since decerebration does not significantly alter these
mechanisms in decerebrated animals (Flynn et al., 1986; Mark et al., 1988). Retrograde transneuronal viral tracing
experiments did not
substantiate a direct connection between the rNTS and the DMnX and suggested the involvement
of
intra-NTS connections or the reticular formation (Streefland et al., 1998).
Therefore, in this study efferent projections from the rNTS within the NTS and within the brainstem were traced with the anterograde tracer Phaseolus vulgaris leucoagglutinin (Pha-L). Pha-L was applied iontophoretically in small sites within the rNTS and in the parvocellular reticular formation (PCRt) and the vestibular nucleus (Ve) nucleus which surround the rNTS. Efferent axons from the injection sites were traced and attributed to the rNTS or the nuclei that surround the rostral tip of the NTS.
|
Materials and methods |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
All procedures used in this study were approved by the Committee on Animal Bioethics of the University of Groningen.
Pha-L procedure
The anterograde tracing experiments were carried out on 12 male Wistar rats (of our own
breeding) between 3 and 4 months of age. For injecting Pha-L, the animals were anesthetized
with a
combination of sodium pentobarbital (i.p., 30 mg/kg body wt), Hypnorm (i.m., 0.5 ml/kg,
Janssen
Pharmaceutica Pharmaceuticals) and atropine sulphate (i.p., 0.125 mg/kg) and mounted in a
stereotactic frame. Pha-L was delivered iontophoretically through beveled glass micropipettes
with tip
diameters of 15–20 µm, which were positioned in the rNTS, the parvocellular
reticular
formation situated rostrally and ventrally to the rNTS and in the vestibular nuclei situated
dorsally to the
rNTS. Brain areas were defined by the coordinate system of Paxinos and Watson (Paxinos
and Watson, 1986). The micropipettes were filled with a solution of 2.5% Pha-L
(Brunschwig) in 0.01 M phosphate buffered saline (PBS, pH 7.4) and connected to the positive
pole of
a Midgard CS3 constant current source. Iontophoretic delivery was achieved with a 5–7
µA current for 30 min in a 7 s on–off cycle. After completion of the iontophoresis,
the glass
pipette was left in its position for 10 min to prevent leakage of tracer in the track during
retraction.
Immunocytochemical staining procedure
Following a postoperative survival time of 7 days, the animals were deeply anesthetized with an i.p. injection of sodium pentobarbital (70 mg/kg body wt) and perfused transcardially with 400 ml of fixative [2.5% glutaraldehyde, 0.5% paraformaldehyde in 0.1 M phosphate buffer (PB), pH 7.4], preceded by a short prerinse with a 0.9% heparinized saline solution. Brains were removed and were cryoprotected by overnight storage at 4°C in 30% sucrose in 0.1 M PB. Transverse or longitudinal sections were cut at 20 µm thickness on a cryostat microtome. The sections were collected in PBS.
Pha-L was visualized with an immunocytochemical avidin–biotin staining technique. Prior to the first antibody incubation, sections were immersed for 10 min in 0.3% H2O2 in 0.01M PBS to exhaust endogenous peroxidase activity. The sections were then incubated for 1 h at room temperature (RT) in 10% normal goat serum (NGS) to suppress non-specific antibody binding, followed by an incubation for 24 h at 4°C in a rabbit anti-Pha-L primary antibody solution (1:2000; Brunschwig, 0.5% Triton X-100, 5% NGS). Subsequently, the sections were incubated in 5% NGS for 1 h at RT, in a goat-anti-rabbit IgG biotinylated secondary antibody solution (1:200; Zymed, 0.5% Triton X-100, 2.5% NGS) for 90 min at RT. Thereafter, a 90 min. incubation in Streptavidin–horseradish peroxidase (1:200; Zymed) was carried out. Between all steps, the sections were rinsed thoroughly with 0.01 M PBS. Finally, the sections were rinsed in 0.1 M Tris–HCl (pH 7.6) and processed by the diaminobenzidine (DAB)–H2O2 reaction (30 mg DAB and 0.01 % H2O2/100 ml 0.1 M Tris–HCl, pH 7.6).
After the immunocytochemical staining, the sections were mounted, air dried, counterstained with cresyl violet, dehydrated, cleared in xylene and coverslipped with DPX mountant (BDH-Pool, UK).
Analysis
The atlas of the rat brain, according to Paxinos and Watson (Paxinos and Watson,
1986), was used to localize Pha-L labeled neurons, axons and terminals. Tracing
results
were analyzed by light microscopic examination and visualized by camera lucida drawings.
|
Results |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Cytoarchitecture of the rNTS
The NTS can be divided into three rostro-caudal levels (Figure 1A). The
rostral level extends from the point at which the NTS buds off from the dorsomedial edge of the
spinal
trigeminal nucleus to the level where the NTS first touches the fourth ventricle. The intermediate
NTS
extends further caudally to the obex. The caudal NTS extends caudally into the medulla to the
junction
with the spinal cord. The rNTS is composed of four subdivisions (Travers, 1988; Beckman and Whitehead, 1991; Becker, 1992; Halsell et al., 1996): medial (m), rostral central
(rc),
rostral lateral (rl) and ventral (v) (Figure 1B). The mNTS occupies the
medial
quarter of the rNTS, the v subdivision is positioned ventral to the rc and rl subdivisions of the
nucleus.
|
Injection sites
The NTS was injected at bregma (B) –11.4, at the level where its lateral subnucleus touches the dorsal tip of the dorsomedial spinal trigeminal nucleus. The effective site of the tracer injection is defined by the presence of neurons filled with tracer. In general, the effective injection sites were spherical and their diameter ranged from 400 to 700 µm. Outside these boundaries, filled neurons were occasionally found. Due to the small area of the rNTS at the level of the injection site, several injections comprise both the rNTS and the surrounding area, including the rostral and caudal parvocellular reticular formation (rPCRt and cPCRt) and the vestibular nucleus (Ve), situated rostrally, ventrally and dorsally to the rNTS. Control injections in which the tracer is confined to these surrounding nuclei were made to distinguish between projections originating within and outside the boundaries of the rNTS. The locations of the injection sites are depicted in Figure 2. Injection areas 1–4 represent individual cases (as described below), while injection areas 5 and 6 are a summary of three cases each.
|
Pha-L tracing results
An injection site largely confined to the rNTS is exemplified by the case summarized in Figure 3 (case no. 1). The injection was largely confined to the rc and v subnuclei of the rNTS (B –11.4). The majority of the labeled axons that emanated from the injection site showed a characteristic rostrolateral and caudal trajectory. The ascending axons traversed in a dorsolateral direction through the rPCRt and gave rise to few terminal boutons in the rPCRt, the motor trigeminal nucleus (Mo5) and the principal sensory trigeminal nucleus (Pr5). Most fibers deflect medially or laterally around the Mo5 with terminals in the peritrigeminal zone, the intertrigeminal nucleus and the dorsal subcoeruleus nucleus. Although the more rostral levels were not analyzed, it appeared that most of the axons passing around and through the Mo5 ended as swellings in the medial and lateral subdivisions of the PBN. Before reaching the Mo5, dorsally to the genu facial nerve, part of the ascending axons branched of laterally and crossed the midline, forming swellings in the contralateral Mo5, Pr5 and surrounding areas to a lesser extent as compared to the ipsilateral site. Furthermore, labeled axons and their varicosities were found in the medial longitudinal fasciculus, within the mesencephalic trigeminal tract and in the superior cerebellar peduncle.
|
Most of the descending axons leave the rNTS ventrally and course in a caudal direction through the parvocellular and intermediate (Irt) medullary reticular formation, giving rise to numerous terminal boutons. The heaviest projection to the PCRt was directly ventral to the injection site (rPCRt) and diminished in ventral direction (cPCRt). At the level of the hypoglossal nucleus (12n), axons form swellings in the dorsal medullary reticular formation (MdV) lateral to 12n. In the caudal medulla the axons coursed to the spinal cord, without the presence of terminal boutons. This labeling pattern was bilateral with an ipsilateral predominance.
A relatively small part of the descending rNTS projections travels through the NTS, mainly in the horizontal plane of the injection site. Pha-L labeling was detectable down to the level where the NTS abuts the fourth ventricle. Within the NTS the sparse descending axons and swellings were mainly located along the medial border of the NTS in the medial and rostral subnuclei of the medial subdivision. Occasionally some anterogradely labeled fibers were found in the tractus. The labeling at the contralateral NTS showed the same pattern and was less numerous as compared to the ipsilateral side.
Some rNTS injections comprised part of the ventrally located PCRt [for ~30% in case no. 2 (Figure 4) and 50% in case no. 3 (Figure 5)]. The ascending and descending projection patterns (case no. 3, not shown) are very similar to those that can be observed in case no. 1 (Figure 3), where the axons arise solely from the rNTS. However, additional labeling originating from anterograde transport of Pha-L by PCRt neurons is present. First, a higher number of labeled axons and swellings was found in the hypoglossal nucleus, especially at its most caudal level in the ventral part, in close vicinity to the DMnX. Furthermore, more terminal labeling was found in the Mo5 and axons and their varicosities were observed to enter the 7n. A considerably higher number of labeled axons and swellings was detected in the medullary reticular formation (MRF), including cPCRt, Irt and MdV. Small fibers and terminals were observed in the dorsal DMnX that seemed to emanate from the densely labeled ventral hypoglossal area. DMnX labeling was sparse and confined to its dorsal border. Concerning the intra-NTS labeling, small axons and swellings were detected entering the ventrolateral part of the cNTS from the MdV.
|
|
Control injections
Control injections with Pha-L were positioned in the rPCRt situated rostrally (n= 3), the cPCRt oriented ventrally (n= 3) and in the Ve oriented dorsally (n = 3) to the rNTS.
Injections confined to the spinal vestibular nucleus, situated dorsally to the rNTS, did not reveal projections to the rNTS.
Injections confined to the rPCRt located rostrally to the rNTS (represented by case no. 4, Figure 6) showed extensive projections to the 12n, Mo5 and 7n; the density of the labeling decreased in this order. Projections to the DMnX were present but sparse. Furthermore, axonal projections and terminal boutons were found in the cPCRt and the more caudally located MRF. Projections to the NTS were also observed in the horizontal plane of the injection site. Axons and terminals directly entered the rNTS. At the remaining horizontal levels where the NTS is present (and no injection site was present), the fibers and their varicosities mainly entered the rNTS at its medial and rostral subnuclei and occasionally in and around the tractus. In caudal direction, NTS labeling was still present, but less extensive and more scattered throughout the medial part. The labeling was bilateral with an ipsilateral predominance.
|
Injections confined to the cPCRt also revealed projections to all oromotor nuclei. The density of the projections to and innervation of these nuclei decreased in the order 12n, Mo5, 7n, nucleus ambiguus (Amb), DMnX. The innervation of the Amb was sparse, but fibers and boutons were clearly visible. Very few fibers were detected at the area postrema (AP) level, in a small strip at the dorsal border between the DMnX and the NTS, from the central canal up to the medial DMnX. A comparable labeling pattern was observed at the contralateral side, although the number of labeled axons and terminals was lower. cPCRt injections also gave rise to NTS projections, although less compared to the rPCRt. Within the rNTS, sparse Pha-L labeled terminals were detected in the medioventral subdivision in the so-called C2 area (adrenergic cells). In the caudal direction, an occasional fiber with terminals was found in the medial part of the NTS. At the level of the AP up to the obex, axons and their boutons were found in the ventral part of the lNTS, emanating from the ventrolaterally orientated MdV.
|
Discussion |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
In the present study we describe the efferent projections from the rNTS to brainstem nuclei and NTS subnuclei. The rNTS neurons contribute to both an ascending and a descending pathway. Ascending axons travel through the rPCRt, around the Mo5 and terminate in the PBN. The descending pathway is confined to the brainstem. The rNTS efferents appear to terminate mainly in the parvocellular and intermediate parts of the MRF and the 12n and, to a lesser extent, in more caudally oriented NTS subnuclei.
Anatomical aspects
The results of the present study confirm the main conclusions of previous reports about rNTS
efferent projections (Norgren, 1978; Travers, 1988; Herbert et al., 1990; Beckman and
Whitehead, 1991; Halsell et al., 1996). These
studies were the result of
anterograde tracing with [3H]leucine and HRP or retrograde tracing with HRP.
However,
these tracing techniques bear several limitations. A disadvantage of autoradiographic
identification of
tritiated amino acids is the relatively poor resolution, which rules out discrimination between
fibers and
presynaptic endings. Furthermore, in both autoradiographic and HRP tracing techniques, tracer
always
spreads or leaks to nearby regions. In most of the rNTS tracing studies, the injection sites were
contaminated with tracer spillage to the surrounding reticular formation.
Since our interest lies in the medullary projections of the rNTS, we will not further discuss ascending projections.
Oromotor nuclei
The most substantial medullary projection after Pha-L injection into the rNTS was to the
12n. The
other oromotor nuclei received light (Mo5) or no (7n) and (Amb) rNTS input. Other anterograde
tracing studies inconsistently report light rNTS projections to the Mo5 and 7n, but usually not to
the
Amb (Norgren, 1978; Travers, 1988; Beckman and Whitehead, 1991; Becker, 1992). Additionally,
Travers and Norgren (Travers and Norgren, 1983) failed to show direct
projections from the rNTS to the 7n and Amb after retrograde HRP deposits in these oromotor
nuclei.
When our injection comprised both the rNTS and the ventrally located PCRt (which belongs to
the
rPCRt), a greater number of labeled axons and swellings was observed in the Mo5 and 12n.
Additional
labeling was detected in the 7n, while sparse Pha-L deposits were seen in the DMnX (Figures 4 and 5). cPCRt control injections showed a
resembling
projection pattern to the oromotor nuclei and also to the Amb. These results partially agree with
former
tracing studies. Anterograde tracing results have shown that the cPCRt innervates the oromotor
nuclei,
the Amb and DMnX (Rogers et al., 1980; Travers
and
Norgren, 1983; Ter Horst et al., 1984; Luiten et al., 1987; Beckman and Whitehead, 1991).
However, a detailed anterograde Pha-L tracer study (Ter Horst et al., 1991) showed that caudal and rostral parts of the PCRt project to the Amb, DMnX and
intermediolateral cell column (IML), and to the Mo5, 7n and 12n respectively. Taken together,
these
results indicate that the rNTS solely projects to the 12n and to a lesser extent to the Mo5. Tracer
leakage to the ventrally or rostrally located rPCRt and the cPCRt probably account for the
inconsistent
results reported so far, concerning the presence and density of 12n, Mo5, 7n, DMnX and Amb
labeling.
Medullary reticular formation
Projections from the rNTS to the MRF (cPCRt, IRt, MdV) extended over a relatively large
area.
The heaviest projection was to the PCRt immediately ventral to the injection site. Again,
injections that
comprised the rPCRt rostral and ventral to the rNTS and the cPCRt showed a higher amount of
Pha-L
within the MRF. Intra-PCRt projections (rostral to caudal) probably cause this increase in MRF
Pha-L
labeling (Ter Horst et al., 1991).
Intra-NTS projections
Several studies have shown that within the rNTS, ascending and descending projections
originate
from different subdivisions (Travers, 1988; Halsell et al.,
1996). The rc division is the major recipient of the chorda tympani and
glossopharyngeal
nerves and mainly projects to the PBN. The v subdivision of the rNTS projects heavily to the
MRF (Beckman and Whitehead, 1991; Halsell et al.,
1996) and receives afferent input from the rc subdivision. Since our injection sites
within the
rNTS comprise both the rc and v subdivisions, attribution of efferent projections to either of
these
subdivisions is not possible. Rostral to caudal NTS projections were found down to the level
were the
NTS abuts the fourth ventricle, in the horizontal plane of the injection site, mainly along the
medial
border of the NTS. This finding is in agreement with some tracing studies (Travers,
1988; Beckman and Whitehead, 1991). Others mention
Pha-L labeling
in the cNTS as well (Norgren, 1978; Becker, 1992),
which might be the result of spilling of the tracer into the PCRt, since our injection sites that
comprised
both the rNTS and the surrounding PCRt showed projection to cNTS subdivisions.
Functional considerations
The functional significance of intramedullary projections from the rNTS is still not
elucidated.
However, it is likely that these projections convey both gustatory and somatosensory information
that
regulates or influences oral motor behavior. Furthermore, the rNTS is involved in the
maintenance of
metabolic homeostasis through autonomic control of abdominal organs (Norgren,
1983).
Gustatory stimuli can elicit a number of behavioral and physiological responses to feeding,
such as
licking, swallowing and active rejection (Travers et al., 1987a).
Behavioral experiments (Travers et al., 1987b) showed that taste
nerve section can disrupt the patterns of motor activity associated with licking, gaping and
swallowing.
This study gives neuroanatomical evidence for taste influence on oral motor behavior through its
projections on the oromotor nuclei. Our results show that the hypoglossal motoneurons
innervating the
tongue musculature (Travers, 1988, 1995) are
directly innervated by the rNTS. The facial and trigeminal motor nuclei, responsible for control
of the
muscles of face, lips and jaw (Travers, 1988, 1995),
receive indirect rNTS input via rNTS efferents to the MRF. These ‘premotor’
cells are
concentrated in the PCRt ventral to the rNTS (rPCRt) and the reticular formation lateral to the
12n
(MdV). The rPCRt projects heavily onto the oromotor nuclei (this study) (Travers and
Norgren, 1983; Ter Horst et al., 1991). Furthermore,
electrophysiological studies showed that the MdV contains neurons that are active during licking
and
swallowing (Jean, 1984; Amri and Car, 1988; Travers and Jackson, 1989; Travers and Dinardo, 1992).
The influence of gustatory information on autonomic responses, such as salivation or the
cephalic
phase insulin response, always seems to be indirect. The rNTS projections to the MRF may
indirectly
influence salivation. Preganglionic parasympathetic neurons from the superior salivatory nucleus
are
found in the rPCRt, which is located ventral to and receives input from the rNTS (Hiura,
1977; Nicholson and Severin, 1981; Whitehead
and
Frank, 1983). Furthermore, the medullary reticular formation (cPCRt, IRt, MdV) that
receives input from the rNTS, directly projects to the preganglionic paraand orthosympathetic
neurons
of the DMnX, Amb and IML (Rogers et al., 1980; Ter
Horst et al., 1984; Ter Horst, 1986;Luiten et al., 1987; Cunningham and Sawchenko, 1989).
The
hypothalamus, playing an important role in metabolic homeostasis, projects to the caudally
located
PCRt. The descending efferents from hypothalamic nuclei that regulate the motivational aspects
of food
intake mainly innervate the cPCRt (Ter Horst et al., 1984; Luiten et al., 1985, 1987; Ter
Horst, 1986).
Since our results also show rNTS projections to the iNTS at the level of the fourth ventricle,
the
descending gustatory pathway may reach the DMnX through the MRF or through more caudally
located NTS subnuclei. This study provides no direct evidence that rNTS neurons projecting to
the
MRF and the iNTS have a gustatory function. Although the DMnX receives input from both the
cPCRt
(Rogers et al., 1980; Ter Horst et al., 1984) and iNTS (Ross et al., 1985; Cunningham
and Sawchenko, 1989; Otake et al., 1992), there is
little
evidence for gustatory responses in the MRF and iNTS. In an intracellular recording Renehan
and
colleagues (Renehan et al., 1994) observed taste responsive
neurons
in the rNTS that projected to the RF after filling with neurobiotin. Halsell et al. (Halsell et al., 1996) report that they often tried to record taste
responsive neurons
in the RF, but found only few extracellularly recorded gustatory responses in the RF. They
suggested
that the influence of taste may be ‘modulatory or refractory to observation under
anesthesia’. This may also be true for taste responsive neurons in the NTS at fourth
ventricle
level (i.e. iNTS), since we were not able to record single-unit responses to whole-mouth
gustatory
stimulation in this region (unpublished results). In an earlier study, where c-fos
expression was
used to localize neuronal activity caused by gustatory stimulation, no PCRt labeling was found (Streefland et al., 1998) (C. Streefland et al., submitted
for
publication). However, we did observe Fos protein within the iNTS. This could be an indication
that
descending gustatory information reaches the DMnX through the iNTS.
In conclusion, the anatomical evidence shows that, in the rat, medullary rNTS projections mainly relay in the rPCRt ventral to the rNTS and in the MRF caudal to the rNTS (including the cPCRt, IRt and MdV). A small portion of rNTS efferents appears to synapse in the 12n and in more caudally situated NTS subdivisions. Medullary rNTS projections seem to play a role in oral motor behavior and autonomic control of abdominal organs.
|
Acknowledgments |
|---|
The helpful comments of Ms E. Farkas, Dr F.W. Maes and Professor Dr B. Bohus are gratefully acknowledged.
|
References |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Amri, M. and Car, A. (1988) Projections from the medullary swallowing center to the hypoglossal motor nucleus: a neuroanatomical and electrophysiological study in sheep. Brain Res., 441 , 119–126.[Web of Science][Medline]
Becker, D.C. (1992) Efferent projections of electrophysiologically identified regions of the rostral nucleus of the solitary tract in the rat. Thesis, Graduate School of the Ohio State University.
Beckman, M.E. and Whitehead, M.C. (1991) Intramedullary connections of the rostral nucleus of the solitary tract in the hamster. Brain Res. , 557, 265–279.[Web of Science][Medline]
Cechetto, D.F. (1991) Central nervous system pathways and mechanisms integrating taste and the autonomic nervous system. In Friedman, M.I., Tordoff, M.G. and Kare, M.R. (eds), Chemical Senses: Appetite and Nutrition. M. Dekker, New York, pp. 427–443.
Cunningham, E.T. and Sawchenko, P.E. (1989) A circumscribed projection from the nucleus of the solitary tract to the nucleus ambiguus in the rat: anatomical evidence for somatostatin-28-immunoreactive interneurons subserving reflex control of esophageal motility. J. Neurosci., 9, 1668–1682.[Abstract]
Ergene, E., Dunbar, J.C. and Barraco, I.R.A. (1994) Role of NTS in nutrient homeostasis and ingestive behavior. In Barraco, I.R.A. (ed.), Nucleus of the Solitary Tract. CRC Press, Boca Raton, FL, pp. 341–348.
Flynn, F.W., Berridge, K.C. and Grill, H.J. (1986) Preand postabsorptive insulin secretion in chronic decerebrate rats. Am. J. Physiol., 250, R539–R548.
Halsell, C.B., Travers, S.P. and Travers, J.B. (1996) Ascending and descending projections from the rostral nucleus of the solitary tract originate from separate neuronal populations. Neuroscience,72, 185–197.[Web of Science][Medline]
Herbert, H., Moga, M.M. and Saper, C.B. (1990) Connections of the parabrachial nucleus with the nucleus of the solitary tract and the medullary reticular formation in the rat. J. Comp. Neurol.,293, 540–580.[Web of Science][Medline]
Hiura, T. (1977) Salivatory neurons innervate the submandibular and sublingual glands in the rat: a horseradish peroxidase study. Brain Res.,137, 145–149.[Web of Science][Medline]
Jean, A. (1984) Brainstem organization of the swallowing network. Brain Behav. Evol., 25, 109–116.[Web of Science][Medline]
Loewy, A.D. and Haxhiu, M.A. (1993) CNS cell groups projecting to pancreas parasympathetic preganglionic neurons. Brain Res., 620, 323–330.[Web of Science][Medline]
Luiten, P.G.M., Ter Horst, G.J., Karst, H. and Steffens, A.B. (1985) The course of paraventricular hypothalamic efferents to autonomic structures in medulla and spinal cord. Brain Res., 329, 374–378.[Web of Science][Medline]
Luiten, P.G.M., Ter Horst, G.J. and Steffens, A.B. (1987) The hypothalamus, intrinsic connections and outflow pathways to the endocrine system in relation to the control of feeding and metabolism. Prog. Neurobiol., 28, 1–54.[Medline]
Mark, G.P., Scott, T.R., Chang, T.F.C. and Grill, H.J. (1988) Taste responses in the nucleus tractus solitarius of the chronic decerebrate rat. Brain Res., 443, 137–148.[Web of Science][Medline]
Nicholson, J.E. and Severin, C.N. (1981) The superior and inferior salivatory nuclei in the rat. Neurosci. Lett., 21, 127–132.
Norgren, R. (1978) Projections from the nucleus of the solitary tract in the rat. Neuroscience, 3, 207–218.[Web of Science][Medline]
Norgren, R. (1981) The central organization of the gustatory and visceral afferent systems in the nucleus of the solitary tract. In Katsuki, Y., Norgren, R. and Sato, M. (eds), Brain Mechanisms of Sensation. Wiley, New York, pp. 143–160.
Norgren, R. (1985) Taste and the autonomic
nervous system. Chem. Senses, 10, 143–165.
Otake, K., Ezure, K., Lipsky, J. and Wong-She, R.B. (1992) Projections from the commissural subnucleus of the nucleus of the solitary tract: an anterograde tracing study in the cat. J. Comp. Neurol., 324, 365–378.[Web of Science][Medline]
Paxinos, G. and Watson, C. (1986) The Rat Brain in Stereotaxic Coordinates. Academic Press, New York.
Renehan, W.E., Jin, Z., Zhang, X. and Schweitzer, L. (1994) Structure and function of gustatory neurons in the nucleus of the solitary tract. I. A classification of neurons based on morphological features. J. Comp. Neurol., 347, 531–544.[Web of Science][Medline]
Ricardo, J.A. and Koh, E.T. (1978) Anatomical evidence of direct projections from the nucleus of the solitary tract to the hypothalamus, amygdala, and other forebrain stuctures in the rat. Brain Res., 153, 1–26.[Web of Science][Medline]
Rogers, R.C., Kita, H., Butcher, H. and Novin, D. (1980) Efferent projections to the dorsal motor nucleus of the vagus. Brain Res. Bull., 5, 365–373.[Web of Science][Medline]
Ross, C.A., Ruggiero, D.A. and Reis, D.J. (1985) Projections from the nucleus tractus solitarii to the rostral ventrolateral medulla. J. Comp. Neurol., 242, 511–534.[Web of Science][Medline]
Strack, A.M., Sawyer, W.B., Platt, K.B. and Loewy, A.D. (1989) CNS cell groups regulating the sympathetic outflow to adrenal gland as revealed by transneuronal cell body labeling with pseudorabies virus. Brain Res., 491, 274–296.[Web of Science][Medline]
Streefland, C., Maes, F.W. and Bohus, B. (1998) Autonomic brainstem projections to the pancreas: a retrograde transneuronal viral tracing study in the rat. J. Auton. Nerv. Syst., 74, 71–81.[Web of Science][Medline]
Strubbe, J.H. and Bouman, P.R. (1978) Plasma insulin patterns in the unanesthesized rat during intracardial infusion and spontaneous ingestion of graded loads of glucose. Metabolism, 27, 341–351.[Web of Science][Medline]
Strubbe, J.H. and Steffens, A.B. (1975) Rapid insulin release after ingestion of a meal in the unanesthesized rat. Am. J. Physiol., 229, 1019–1022.
Ter Horst, G.J. (1986) The hypothalamus, intrinsic connections and outflow pathways to the pancreas. Thesis, RU Groningen.
Ter Horst, G.J. and Streefland, C. (1993) Ascending projections of the solitary tract nucleus. In Barraco, R.A. (ed.) Nucleus of the Solitary Tract. CRC Press, Boca Raton, FL, pp. 93–103.
Ter Horst, G.J., Luiten, P.G.M. and Kuipers, F. (1984) Descending pathways from hypothalamus to dorsal motor vagus and ambiguus nuclei in the rat. J. Auton. Nerv. Syst., 11, 59–75.[Web of Science][Medline]
Ter Horst, G.J., De Boer, P., Luiten, P.G.M. and Van Willigen, J.D. (1989) Ascending projections from the solitary tract nucleus to the hypothalamus. A. Phaseolus vulgaris lectin tracing study in the rat. Neuroscience 31, 785–797.[Web of Science][Medline]
Ter Horst, G.J., Copray, J.C.V.M., Liem, R.S.B. and Van Willigen, J.D. (1991) Projections from the rostral parvocellular reticular formation to pontine and medullary nuclei in the rat: involvement in autonomic regulation and orofacial motor control. Neuroscience, 40, 735–758.[Web of Science][Medline]
Travers, J.B. (1988) Efferent projections from the anterior nucleus of the solitary tract of the hamster. Brain Res., 457, 1–11.[Web of Science][Medline]
Travers, J.B. (1995) Organization and projections of the orofacial motor nuclei. and Oromotor nuclei. In Paxinos, G. (ed.),The Rat Nervous System . Academic Press, New York, pp. 111–128 and 239–255.
Travers, J.B. and Dinardo, L.A. (1992) Distribution of lickingand swallowing-responsive cells in the medullary reticular formation in the awake freely moving rat.. Soc. Neurosci. Abstr.,18, 1069.
Travers, J.B. and Jackson, L.M. (1989) The effects of gustatory stimulation on neurons in and adjacent to the hypoglossal nucleus. Chem. Senses, 14, 756.
Travers, S.P. and Norgren, R. (1983) Afferent projections of the oral motor nuclei in the rat. J. Comp. Neurol., 220, 280–298.[Web of Science][Medline]
Travers, J.B., Grill, H.J. and Norgren, R. (1987a) The effects of glossopharyngeal and chorda tympani nerve cuts on the ingestion and rejection of sapid stimuli: an electromyographic analysis in rat. Behav. Brain Res., 25, 233–246.
Travers, J.B., Travers, S.P. and Norgren, R. (1987b) Gustatory processing in the hindbrain. Ann. Rev. Neurosci., 10, 595–632.
Whitehead, M.C. andFrank, M.E. (1983) Anatomy of the gustatory system in the hamster: central projections of the chorda tympani and the lingual nerve. J. Comp. Neurol., 220, 378–395.[Web of Science][Medline]
Accepted June 14, 1999
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  Y. K. Cho and C.-S. Li Gustatory Neural Circuitry in the Hamster Brain Stem J Neurophysiol, August 1, 2008; 100(2): 1007 - 1019. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 L. Rinaman Hindbrain contributions to anorexia Am J Physiol Regulatory Integrative Comp Physiol, November 1, 2004; 287(5): R1035 - R1036. [Full Text] [PDF]
|
|
|
|
|
|
S. P. Travers Quinine and citric acid elicit distinctive Fos-like immunoreactivity in the rat nucleus of the solitary tract Am J Physiol Regulatory Integrative Comp Physiol, June 1, 2002; 282(6): R1798 - R1810. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||