The effects of dietary protein restriction on chorda tympani nerve taste responses and terminal field organization

Abstract

Prenatal dietary sodium restriction produces profound developmental effects on rat functional taste responses and formation of neural circuits in the brainstem. Converging evidence indicates that the underlying mechanisms for these effects are related to a compromised nutritional state and not to direct stimulus-receptor interactions. We explored whether early malnourishment produces similar functional and structural effects to those seen following dietary sodium restriction by using a protein deficient, sodium replete diet. To determine if early dietary protein-restriction affects the development of the peripheral gustatory system, multi-fiber neurophysiological recordings were made from the chorda tympani nerve and anterograde track tracing of the chorda tympani nerve into the nucleus of the solitary tract (NTS) was accomplished in rats fed a protein-restricted or a control diet (6% and 20%, respectively). The dietary regimens began on embryonic day 7 and continued until rats were used for neurophysiological recordings (postnatal days (P) 35-50) or for chorda tympani terminal field labeling (P40-50). Responses to a concentration series of NaCl, sodium acetate, KCl, and to 0.50 M sucrose, 0.03 M quinine-HCl, and 0.01 N HCl revealed attenuated responses (30-60%) to sodium-specific stimuli in rats fed the 6% protein diet compared with those fed the 20% protein diet. Responses to all other stimuli were similar between groups. Terminal field volumes were nearly twofold larger in protein-restricted rats compared with controls, with the differences located primarily in the dorsal-caudal zone of the terminal field. These results are similar to the results seen previously in rats fed a sodium-restricted diet throughout pre-and postnatal development, suggesting that dietary sodium-and protein-restriction share similar mechanisms in altering gustatory development. Keywordsnucleus of the solitary tract; gustation; development; prenatal diet; plasticity . E-mail address: dh2t@virginia.edu (D. L. Hill). Publisher's Disclaimer: This article appeared in a journal published by Elsevier. The attached copy is furnished to the author for internal non-commercial research and education use, including for instruction at the authors institution and sharing with colleagues. Other uses, including reproduction and distribution, or selling or licensing copies, or posting to personal, institutional or third party websites are prohibited. In most cases authors are permitted to post their version of the article (e.g. in Word or Tex form) to their personal website or institutional repository. Authors requiring further information regarding Elsevier's archiving and manuscript policies are encouraged to visit: http://www.elsevier.com/copyright NIH Public Access Sensory systems adapt to environmental influences by coordinated alterations in structure and function, often referred to as "plastic" changes. Unlike other sensory systems, there is a remarkable amount of environmentally induced plasticity resident in peripheral and brainstem g...

Chorda Tympani Nerve Terminal Field Maturation and Maintenance Is Severely Altered Following Changes to Gustatory Nerve Input to the Nucleus of the Solitary Tract

“…When the afferent gustatory system is perturbed, the chorda tympani nerve terminal field reverts to or exceeds an immature size by adulthood, primarily through the expansion of terminal fields in the dorsal zones of the NTS (King and Hill, 1991; Krimm and Hill, 1997; May and Hill, 2006; Mangold and Hill, 2007, 2008; May et al, 2008). For these studies, early developmental dietary manipulations produced attenuated neural responses and/or changes in the early environment of the peripheral and central nervous system that resulted in expanded terminal fields at adulthood (Sollars et al, 2006; Thomas and Hill, 2008). In some cases, the expanded terminal fields only occurred at adulthood (Mangold and Hill, 2008).…”

“…Moreover, the developing gustatory system exhibits significant anatomical and functional plasticity (Lasiter and Kachele, 1990; King and Hill, 1991; Mangold and Hill, 2007, 2008; Thomas and Hill, 2008). The mechanisms that drive these changes have not been identified.…”

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

“…No attempt was made to deliver the same amount of BDA among rats; rather, the tracer was generously applied to obtain a gelatinous consistency over the entire cut end of the nerve for all animals. This procedure was used in previous studies that yielded terminal field labels in rats of different ages and experimental conditions (Corson and Hill, 2011; Mangold and Hill, 2007; 2008; May and Hill, 2006; Sollars and Hill, 2000; Sollars et al, 2006; Thomas and Hill, 2008). There were no noticeable differences between groups in accessing the chorda tympani nerve or in labeling it with BDA.…”

“…Brainstems were then blocked and sectioned with a vibratome in the horizontal plane at 50 μm. As in our previous studies of afferent nerve terminal field organization in the NTS, we chose to focus our analyses on horizontal sections of the NTS, because the largest extent of the terminal fields can be visualized in the fewest horizontal planes, in large part because the axons project rostral to caudal and send off terminals medially in approximately the same plane (Corson and Hill, 2011; Lasiter, 1992, 1995; Lasiter and Diaz, 1992; Lasiter and Kachele, 1990; Lasiter et al, 1989; Mangold and Hill, 2007; 2008; May and Hill, 2006; Pittman and Contreras, 2002; Sollars and Hill, 2000; Sollars et al, 2006; Thomas and Hill, 2008). However, analyses of afferent and efferent projections within NTS subdivisions have been made in coronally sectioned tissue (Corson et al, 2011; Whitehead, 1988, 1990, 1993; Whitehead et al, 1993).…”

Gustatory solitary tract development: A role for neuropilins

“…As the projecting nerves enter this complex tract, which extends through a large portion of the brainstem, they are spatially organized. Much of the work related to the development of the ST has focused on postnatal development of the terminal fields of the gustatory nerves (Mangold and Hill, 2007, 2008; Thomas and Hill, 2008). No study has attempted to examine the components involved in the guidance and projection of ST fibers in early development.…”