Effects of early postnatal receptor damage on dendritic development in gustatory recipient zones of the rostral nucleus of the solitary tract

doi:10.1016/0165-3806(91)90132-3

Developmental Brain Research

Volume 61, Issue 2, 19 August 1991, Pages 197-206

https://doi.org/10.1016/0165-3806(91)90132-3 Get rights and content

Abstract

The rostral gustatory zone of the nucleus of the solitary tract (NST) exhibits extensive anatomical development during the first 3 weeks of postnatal life, and this development requires the presence of intact gustatory receptors during a critical period. We have previously shown that unilateral damage induced to fungiform papillae of the anterior tongue at postnatal day 2 (P2) alters normal migration and ramification of chorda tympani (CT) axons in the rostral NST. In addition to alterations of axonal development, P2 receptor damage decreases the intraneuronal distance between neurons that project axons to the second-order central gustatory relay, located in the caudal parabrachial nucleus (PBN). This observation suggested that P2 receptor damage may alter both axonal development and dendritic development in the rostral gustatory NST. The present study evaluated potential changes in dendritic development of PBN projection neurons following either P2 or P10 receptor damage. Morphological studies were first conducted to quantitatively define somatic characteristics of neurons that project axons to the PBN. Independent experiments used fluorescent labeling combined with subsequent Golgi-impregnation to study dendritic architecture of identified PBN projection neurons. Results confirmed that P2 receptor damage alters dendritic development of PBN projection neurons located in CT terminal fields. Anterior tongue receptor damage at P2 (1) reduces planar length of first- and second-order dendritic branches, (2) reduces the mean number of second-order branches per neuron, and (3) reduces the density of spine processes on second-order dendritic branches. A critical period exists for these effects, similar to that reported for axonal development, insofar as P2 receptor damage alters dendritic development of PBN projection neurons, whereas P10 receptor damage does not. Dendrites of identified PBN projection neurons located in regions of the NST that receive primary afferent axons from the glossopharyngeal nerve are not affected by anterior tongue damage at P2. These results show that early postnatal receptor damage influences both pre- and postsynaptic development in the rostral gustatory NST. These anatomical changes are undoubtedly related to alterations in taste-guided behaviors that are observed following P2 receptor damage.

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In the present study we examined the effects of neonatal orosensory deprivation on taste-elicited gustatory activity in the rat parabrachial nucleus (PBN) using the functional anatomical marker c-Fos. Animals in three groups (GG, GO and GM) received gastric cannula implantation surgery on postnatal day 9 (P9). Animals in the fourth group (MR) did not receive any surgery. GG rats were fed by infusion of artificial milk directly into the stomach. GO rats were fed by intraoral infusion of artificial milk. GM and MR rats were reared by their mother with free access to mother's milk, water and rat chow. Rats from all groups were similar in body weight and length by P21. On P21 rats in all groups were intraorally presented with 0.5 M sucrose solution and the brains were extracted and processed for c-Fos immunohistochemistry. Taste-elicited c-Fos expression in both the gustatory waist area, and the external lateral subnucleus of the PBN in rats in the GG group was significantly more robust than in the other three groups. These findings suggest a substantial alteration in orosensory-evoked neuronal response in this nucleus, due to sensory or motor deprivation during a critical developmental stage.
Developmental sodium restriction and gustatory afferent terminal field organization in the parabrachial nucleus
1998, Physiology and Behavior
WALKER, B. R. AND D. L. HILL. Developmental sodium restriction and gustatory afferent terminal field organization in the parabrachial nucleus. Physiol Behav 64(2) 173–178, 1998. Dietary sodium restriction instituted early in prenatal development produces physiological, anatomical, and functional changes in the gustatory system. For example, a rearrangement of the chorda tympani nerve terminal field within the nucleus of the solitary tract (NST) is observed in rats sodium restricted during development. The altered pattern of the chorda tympani nerve innervation within the nucleus of the solitary tract remains even after dietary sodium is restored in the diet at adulthood. In light of these observations, the terminal fields of second-order projections from the nucleus of the solitary tract to the parabrachial nucleus (PBn) were examined. To determine the possible rearrangements of the second-order projections, the rostral pole of the NST in control, restricted, and repleted rats was injected with the fluorescent tracer Fluoro-Ruby and the terminal fields in the parabrachial nucleus were analyzed. Results show no differences in the size or topography of the parabrachial nucleus terminal field among control, restricted, and repleted rats. These results suggest that the terminal field of second-order gustatory neurons is resistant to dietary sodium restriction during development. The apparent target-dependent effects may relate to differences in the developmental processes along the gustatory pathway.
Effects of orochemical stimulation on postnatal development of gustatory recipient zones within the nucleus of the solitary tract
1995, Brain Research Bulletin
Previous receptor damage studies and artificial rearing (AR) studies in rat have demonstrated that orochemical stimulation between the postnatal ages of P2 and P14 is necessary for development of primary gustatory axons and terminal endings in the rostral nucleus of the solitary tract (NST). Objectives of the present experiment were to evaluate the qualitative nature of orochemical stimulation and amount of orochemical stimulation that is necessary to produce normal axonal and terminal development in gustatory recipient zones of the rostral and intermediate NST. To this end, ultra-pure water, 30,150, and 500 mM NaCl, 80 and 340 mM lactose, whole rat milk, and rat milk that had been subject to extensive dialysis (12–14 kD MWCO) was delivered to independent groups of rat pups during AR procedures. Unstimulated AR animals and matched mother-reared (MR) animals were used as controls. AR animals received experimental orochemical stimulation between the ages of P4 and P10, and were there-after returned to lactating dams until the time of weaning; MR animals received experimental orochemical stimulation during the course of normal nursing. Following maturation, anterograde fluorescent dual-labeling experiments were conducted to map the course and distribution of primary gustatory axons within the NST. Results show that experimental stimulation with water during AR procedures is not sufficient to produce normal development of primary gustatory axons and terminal endings in the gustatory NST. Stimulation with 30,150, and 500 mM NaCl produced normal axonal development in the NST, as did 80 and 340 mM lactose, whole rat milk, and hdialyzed rat milk. These results indicate that orochemical stimulation with qualitatively different tastants during critical periods of postnatal development is sufficient to produce normal development of primary gustatory axons within the rostral NST. In a second experiment, rat pups received either 1 day or 3 days of stimulation with 150 mM NaCl to determine the time-course of stimulation necessary to produce normal development of terminal fields in the rostral NST. Results indicated that 1 day of stimulation with NaCl was not sufficient to produce normal development of rostral NST axons, whereas 3 days stimulation with NaCl was effective in producing normal axonal development. Therefore, like other sensory systems, the gustatory system is susceptible to anatomical modification by taste stimulation during critical or sensitive periods of postnatal development.
Substance P excites neurons in the gustatory zone of the rat nucleus tractus solitarius
1993, Brain Research
Whole-cell patch recordings of neurons in the rostal (gustatory) nucleus tractus solitarius (rNTS) were performed in a brain slice preparation from rat medulla. Neural responses to brief applications (10–45 s) of substance P (SP), via a constant superfusion apparatus, were recorded. SP transiently depolarized 80 of 117 (68%) rNTS neurons in a dose-dependent manner. Sub-micromolar concentrations of SP had potent excitatory effects, and the half maximal response occurred at 0.6 μM. The depolarizing effect of SP was accompanied by an increase in input resistance in 81% of the responsive neurons. The excitatory effects of SP persisted in low Ca²⁺ (0.2 mM) and high Mg²⁺ (12 mM) saline as well as in the presence of 2 μM TTX (n = 5 for each), suggesting direct postsynaptic action on the recorded neurons. SP also hyperpolarized 4 neurons (4%) and had no effect on 33 neurons (28%). Each of the 4 neurons which were hyperpolarized by SP showed a decrease in input resistance. A more detailed assessment of the types of neurons in the rNTS which respond to SP was also conducted. Neurons were separated into 4 electrophysiological groups on the basis of their repetitive firing pattern induced by a hyperpolarizing and depolarizing current injection paradigm. Neurons belonging to each of the 4 electrophysiological groups responded to SP. Eighteen neurons, which were filled with 1% biocytin during recording, were categorized as ovoid, multipolar or fusiform based on their morphological characteristics. SP excited all 3 morphological types of neurons in similar proportion. These results suggest that SP is an excitatory neurotransmitter in the rNTS. The effects of SP are not restricted to a particular neuron type defined either biophysically or morphologically. The implications of these results on the possible role of SP in processing gustatory and somatosensory information within the rNTS are discussed.
Influence of GABA on neurons of the gustatory zone of the rat nucleus of the solitary tract
1993, Brain Research
The role of γ-aminobutyric acid (GABA) as an inhibitory neurotransmitter in the rostral, gustatory zone of the nucleus of the solitary tract (rNST) was examined using whole cell recordings in brain slices of the adult rat medulla. Superfusion of GABA resulted in a concentration-dependent reduction in input resistance in 68% of the neurons in rNST. The change in input resistance was often accompanied by membrane hyperpolarization. The effect of GABA was a direct action on the postsynaptic membrane since it could be elicited when synaptic transmission was blocked by tetrodotoxin or in a low Ca²⁺ and high Mg²⁺ perfusing solution. The mean reversal potential of the GABA effect was about −60 mV, determined by applying GABA at different holding potentials, or from the intersection of current-voltage curves measured in control saline and saline containing GABA. When neurons were separated into groups based on intrinsic membrane properties, some neurons in each group responded to GABA. Superfusion of the slices with either the GABA_A agonist, muscimol, or the GABA_B agonist, baclofen, caused a decrease in input resistance accompanied by membrane hyperpolarization. The GABA_A antagonist bicuculline either totally or partially blocked the neuronal response to GABA and blocked the response to muscimol but did not antagonize responses to baclofen. Superfision of the GABA_B antagonist phaclofen depressed the membrane responses to GABA. The use of the GABA_A and GABA_B agonists and antagonists demonstrates that some neurons in rNSt have both GABA_A and GABA_B receptors. Since most rNST neurons studied respond to GABA, inhibition probably plays a major role in sensory processing by the rNST.
Artificial rearing alters development of the nucleus of the solitary tract
1992, Brain Research Bulletin
Previous studies have shown that damage induced to fungiform papillae of the anterior tongue at postnatal day 2 (P2) alters both pre- and postsynaptic development of gustatory recipient zones within the rostral nucleus of the solitary tract (NST). The present study was conducted to determine whether or not artificial rearing (AR) manipulations, which reduce normal orochemical stimulation during early postnatal development, would be sufficient to produce alterations in anatomical development of the rostral gustatory NST. Two groups of Long-Evans hooded rats were examined. One group received normal rearing with a lactating dam from birth to weaning (mother reared; MR). A second group of animals received artificial rearing via intragastric cannulae between the ages of P4 and P14, and were thereafter returned to lactating dams until the age of weaning (P21). Following weaning and maturation to adulthood (P49), the organization of gustatory afferent terminal fields in the NST was examined using fluorescent tracing procedures which permit the simultaneous visualization of gustatory afferent terminal fields arising from the seventh and ninth cranial nerves. Results show that AR manipulations between the ages of P4 and P14 produce alterations in development of gustatory afferent terminal fields in the NST that are essentially similar to those observed following early postnatal receptor damage. These results confirm previous suggestions that orochemical stimulation during a limited portion of rats' postnatal life is essential in inducing normal presynaptic development in the gustatory NST.

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Research reportEffects of early postnatal receptor damage on dendritic development in gustatory recipient zones of the rostral nucleus of the solitary tract

Abstract

J. Nutr.

Brain Res.

Brain Res.

Brain Res. Rev.

Brain Res.

Brain Res. Bull.

Brain Res. Bull.

Dev. Brain Res.

Dev. Brain. Res.

Brain Res. Bull.

Physiol. Behav.

Brain Res.

Brain Res.

Salt preference in the preweanling rat

Dev. Psychobiol.

Effects of neonatal whisker lesions on mouse central trigeminal pathways

J. Comp. Neurol.

Early postnatal differentiation of granule cell dendrites in the olfactory bulbs of normal and unilaterally odor-deprived rats

Dev. Brain Res.

Axon arbors of X and Y retinal ganglion cells are differentially affected by prenatal disruption of binocular inputs

Central projections of gustatory nerves in the rat

J. Comp. Neurol.

Connections of the parabrachial nucleus with the nucleus of the solitary tract and the medullary reticular formation in the rat

J. Comp. Neurol.

Research report
Effects of early postnatal receptor damage on dendritic development in gustatory recipient zones of the rostral nucleus of the solitary tract