Effects of orochemical stimulation on postnatal development of gustatory recipient zones within the nucleus of the solitary tract

doi:10.1016/0361-9230(95)00063-K

Brain Research Bulletin

Volume 38, Issue 1, 1995, Pages 1-9

https://doi.org/10.1016/0361-9230(95)00063-K Get rights and content

Abstract

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.

References (47)

E. Antonian et al.
Fast axonally transported proteins in regenerating goldfish optic nerve: Effect of abolishing electrophysiological activity with TTX
Brain Res.
(1987)
L.I. Benowitz et al.
Activity-dependent sharpening of the regenerating retinotectal projection in goldfish: Relationship to the express of growth-associated proteins
Brain Res.
(1987)
C.E. Croul-Ottman et al.
NADPH diaphorase staining within the developing olfactory bulbs of normal and unilaterally odor-deprived rats
Brain Res.
(1988)
J. Diaz et al.
Artificial rearing of preweanling rats: The effectiveness of direct intragastric feeding
Physiol. Behav.
(1981)
J. Diaz et al.
Artificial rearing of rat pups with a protein-enriched formula
J. Nutr.
(1982)
D.L. Hill et al.
Developmental neurobiology of salt taste sensation
Trends. Neurosci.
(1990)
G. Kutty et al.
Light deprivation profoundly affects gene expression of interphotoreceptor retionoid-binding protein in the mouse eye
Exp. Eye Res.
(1994)
P.S. Lasiter
Postnatal development of gustatory recipient zones within the nucleus of the solitary tract
Brain Res. Bull.
(1992)
P.S. Lasiter et al.
Artificial rearing alters development of the nucleus of the solitary tract
Brain Res. Bull.
(1992)
P.S. Lasiter et al.
Effects of early postnatal receptor damage on development of gustatory recipient zones within the nucleus of the solitary tract
Dev. Brain. Res.
(1990)

P.S. Lasiter et al.

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

Dev. Brain. Res.

(1991)

P.S. Lasiter et al.

Postnatal development of the rostral solitary nucleus in rat: Dendritic morphology and mitochondrial enzyme activity

Brain Res. Bull.

(1989)

M. Messer et al.

Artificial feeding of infant rats by continuous gastric infusion

J. Nutr.

(1969)

M. Pierson et al.

Development of frequency-selective domains in inferior colliculus of normal and neonatally noise-exposed rats

Brain Res.

(1994)

R.T. Robertson et al.

Transient patterns of acetylcholinesterase activity in visual cortex of the rat: Normal development and the effects of neonatal monocular enucleation

Brain Res.

(1985)

D.M. Stone et al.

Decrease in tyrosine hydroxylase, but not aromatic l-amino acid decarboxylase, messenger RNA in rat olfactory bulb following neonatal, unilateral odor deprivation

Brain Res. Mol. Brain Res.

(1990)

V. Baikelandt et al.

Alterations in GAP-43 and synapsin immunoreactivity provide evidence for synaptic reorganization in adult cat dorsal lateral geniculate nucleus following retinal lesions

Eur. J. Neurosci.

(1994)

G.R. Belford et al.

The development of vibrissae representation in subcortical trigeminal centers of the neonatal rat

J. Comp. Neurol.

(1979)

G.R. Belford et al.

The sensitive period in the development of the trigeminal system of the neonatal rat

J. Comp. Neurol.

(1980)

E.M. Callaway et al.

Effects of binocular deprivation on the development of clustered horizontal connections in cat striate cortex

M.J. Cohen et al.

The response spectrum of taste fibers in the cat: A single fibre analysis

Acta Physiol. Scand.

(1955)

J. Diaz

Experimental rearing of rat pups using chronic gastric fistulas

D.O. Frost et al.

Effects of alternating monocular occlusion on the development of visual callosal connections

Exp. Brain Res.

(1990)

Cited by (15)

Early-life influences of low-calorie sweetener consumption on sugar taste
2023, Physiology and Behavior
Children and adolescents are the highest consumers of added sugars, particularly from sugar-sweetened beverages (SSB). Regular consumption of SSB early in life induces a variety of negative consequences on health that can last into adulthood. Low-calorie sweeteners (LCS) are increasingly used as an alternative to added sugars because they provide a sweet sensation without adding calories to the diet. However, the long-term effects of early-life consumption of LCS are not well understood. Considering LCS engage at least one of the same taste receptors as sugars and potentially modulate cellular mechanisms of glucose transport and metabolism, it is especially important to understand how early-life LCS consumption impacts intake of and regulatory responses to caloric sugars. In our recent study, we found that habitual intake of LCS during the juvenile-adolescence period significantly changed how rats responded to sugar later in life. Here, we review evidence that LCS and sugars are sensed via common and distinct gustatory pathways, and then discuss the implications this has for shaping sugar-associated appetitive, consummatory, and physiological responses. Ultimately, the review highlights the diverse gaps in knowledge that will be necessary to fill to understand the consequences of regular LCS consumption during important phases of development.
Deconstructing the function of maternal stimulation in offspring development: Insights from the artificial rearing model in rats
2016, Hormones and Behavior
Citation Excerpt :
Artificial rearing using the gastrostomy approach has also been shown to affect the morphology of the primary gustatory afferent terminal fields arising from the seventh cranial nerve (N. VII) and ending in the rostral nucleus of the solitary tract (NST, Lasiter and Diaz, 1992). In a follow-up study, it was found that stimulation of the anterior tongue of pups (5 times daily, from PND 4 to 10) with solutions of NaCl, lactose, dialyzed rat milk or whole rat milk, but not water, was effective in producing normal development of the N.VII axons and the terminals of the NST in adult AR rats (Lasiter, 1995). These results demonstrate the importance of suckling and exposure to the chemical stimuli from milk in the development of oro-motor function and the gustatory system, respectively.
This article is part of a Special Issue on “Parental Care”.
Maternal behavior has an important function in stimulating adequate growth and development of the young. Several approaches have been used in primates and rodents to deconstruct and examine the influence of specific components of maternal stimulation on offspring development. These approaches include observational studies of typical mother–infant interactions and studies of the effects of intermittent or complete deprivation of maternal contact. In this review, we focus on one unique approach using rats that enables the complete control of maternal variables by means of rearing rat pups artificially without contact with the mother or litter, while maintaining stable nutrition, temperature and exposure to stressful stimuli. This artificial rearing model permits the removal and controlled replacement of relevant maternal and litter stimuli and has contributed valuable insights regarding the influence of these stimuli on various developmental outcomes. It also enables the analysis of factors implicated in social isolation itself and their long-term influence. We provide an overview of the effects of artificial rearing on behavior, physiology, and neurobiology, including the influence of replacing maternal tactile stimulation and littermate contact on these outcomes. We then discuss the relevance of these effects in terms of the maternal role in regulating different aspects of offspring development and implications for human research. We emphasize that artificial rearing of rats does not lead to a global insult of nervous system development, making this paradigm useful in investigating specific developmental effects associated with maternal stimulation.
Orosensory deprivation alters taste-elicited c-Fos expression in the parabrachial nucleus of neonatal rats
2010, Neuroscience Research
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.
Age-related decrease of the chorda tympani nerve terminal field in the nucleus of the solitary tract is prevented by dietary sodium restriction during development
2006, Neuroscience
Institution of a low-NaCl diet beginning at embryonic day 3 and continued throughout pre- and postnatal development has widespread effects on the neuroanatomical organization of the first gustatory relay in the nucleus of the solitary tract. To determine when these effects are expressed postnatally, the terminal field of the chorda tympani nerve was compared between sodium-restricted and sodium-replete rats at postnatal days 15–17, postnatal days 25–27, postnatal days 35–37, and adults. Total terminal fields were significantly larger in postnatal days 35–37 and adult sodium-restricted rats compared with aged-matched controls. The group-related differences appear related more to a remodeling of the terminal field in the dorsal zone of the terminal field in controls. Specifically, the terminal field volume in the dorsal zone in controls decreased dramatically from postnatal days 25–27 to postnatal days 35–37 and then again from postnatal days 35–37 to adulthood. In contrast, the fields did not change during development in sodium-restricted rats. These findings suggest that remodeling of the chorda tympani field occurs in controls at about the developmental period of taste response maturation. The lack of remodeling in sodium-restricted rats may be explained by a corresponding lack of functional response development to sodium salts. These results also illustrate the specificity and extent of how early dietary manipulations shape the developing brainstem.
Abnormal physiological responses to touch among children with persistent feeding difficulties
2006, Developmental Medicine and Child Neurology
Impact of chorda tympani nerve injury on cell survival, axon maintenance, and morphology of the chorda tympani nerve terminal field in the nucleus of the solitary tract
2012, Journal of Comparative Neurology

View all citing articles on Scopus

View full text

ArticleEffects of orochemical stimulation on postnatal development of gustatory recipient zones within the nucleus of the solitary tract

Abstract

Brain Res.

Brain Res.

Brain Res.

Physiol. Behav.

J. Nutr.

Trends. Neurosci.

Exp. Eye Res.

Brain Res. Bull.

Brain Res. Bull.

Dev. Brain. Res.

Dev. Brain. Res.

Brain Res. Bull.

J. Nutr.

Brain Res.

Brain Res.

Brain Res. Mol. Brain Res.

Alterations in GAP-43 and synapsin immunoreactivity provide evidence for synaptic reorganization in adult cat dorsal lateral geniculate nucleus following retinal lesions

Eur. J. Neurosci.

The development of vibrissae representation in subcortical trigeminal centers of the neonatal rat

J. Comp. Neurol.

The sensitive period in the development of the trigeminal system of the neonatal rat

J. Comp. Neurol.

Effects of binocular deprivation on the development of clustered horizontal connections in cat striate cortex

The response spectrum of taste fibers in the cat: A single fibre analysis

Acta Physiol. Scand.

Experimental rearing of rat pups using chronic gastric fistulas

Effects of alternating monocular occlusion on the development of visual callosal connections

Exp. Brain Res.

Article
Effects of orochemical stimulation on postnatal development of gustatory recipient zones within the nucleus of the solitary tract