Organization of orosensory responses in the nucleus of the solitary tract of the rat

S. P. Travers, Ralph Norgren

Research output: Contribution to journalArticle

141 Citations (Scopus)

Abstract

1. The receptive field and topographic organization of single orosensory neurons located throughout the rostral division of the nucleus of the solitary tract (rNST) was studied by determining their responsiveness to gustatory stimulation of the entire oral cavity and to gustatory and mechanical stimulation of restricted oral regions. The rNST contained roughly equal numbers of two distinct populations of orosensory neurons, one responsive exclusively to oral mechanical stimulation (M neurons), the other to gustatory stimulation (G neurons). Some G neurons also responded to oral somatosensory stimuli, but usually less vigorously than to gustatory stimuli. The distribution of these two populations of rNST neurons was topographically organized: G neurons were centered anteriorly and medially to M neurons. 2. Eight of 44 G neurons responded only when the whole oral cavity was stimulated, but the remaining 36 cells responded to circumscribed stimulation of taste buds on the anterior tongue (AT), foliate papillae of the posterior tongue, nasoincisor ducts, retromolar mucosa (RM), or soft palate (SP). Overall, AT and SP stimulation were the most effective, and RM stimulation the least effective, for activating nucleus of the solitary tract (NST) G neurons. 3. Approximately half of the G neurons for which a receptive field could be defined (N = 36) responded to stimulation of a single taste receptor subpopulation, but the remaining neurons received convergent input from two or more taste bud groups. The receptive field configurations for convergent G neurons were orderly; convergence occurred preferentially between receptor subpopulations either within the anterior oral cavity (AO) or the posterior oral cavity (PO). An AO-PO distinction also was reflected in the topographic organization of gustatory responses. The mean location of neurons responding optimally to AO gustatory stimulation was more anterior in the NST, and also tended to be more lateral and ventral than the location of neurons that responded optimally to PO stimulation. 4. Forty-four rNST M neurons responded to innocuous mechanical stimulation of restricted areas of the tongue, palate, buccal mucosa, or periodontium. Stimulation of the hard palate and circumvallate papilla were most effective, whereas periodontal stimulation was least effective for activating these cells. 5. A majority (32 of 44) of rNST M neurons responded to stimulation of more than one of the oral sites tested. The amount of central convergence this represents cannot be quantified precisely because some (n = 7) of the oral sites tested as separate fields share a common peripheral innervation, and thus the multiple responsiveness of these central neurons either could be accounted for by peripheral branching or by central convergence. After excluding these ambiguous instances, however, it was clear that ≥56.8% of the M neurons received convergent central input. The configurations of the receptive fields for M neurons were more varied than those for G neurons. Although there was evidence that mechanical convergence occurred preferentially within the AO or PO, this tendency was weaker than for gustatory convergence. Nevertheless, an AO-PO distinction characterized the topographic organization of mechanical responses. The mean location of neurons that responded optimally to AO mechanical stimulation was more anterior and lateral, and also tended to be more ventral, than the location of neurons that responded optimally to PO stimulation. 6. The response properties of a smaller population (n = 21) of neurons just outside of the borders of the NST also were characterized. Most (n = 19) of these neurons were located on the lateral NST border, the medial spinal trigeminal nucleus, or in the intervening reticular formation. Almost all of the extra-NST neurons were M neurons. None responded to gustatory stimulation. The response properties of the M neurons outside the NST border were similar to those inside the nucleus, except that they exhibited a greater relative responsiveness to stimulation of oral sites located in the AO and a smaller relative responsiveness to sites located in the PO.

Original languageEnglish (US)
Pages (from-to)2144-2162
Number of pages19
JournalJournal of Neurophysiology
Volume73
Issue number6
DOIs
StatePublished - Jan 1 1995

Fingerprint

Solitary Nucleus
Organizations
Neurons
Mouth
Tongue
Taste Buds
Soft Palate

All Science Journal Classification (ASJC) codes

  • Neuroscience(all)
  • Physiology

Cite this

@article{7d5ac116f6024f3f91bc8fecd7242e5d,
title = "Organization of orosensory responses in the nucleus of the solitary tract of the rat",
abstract = "1. The receptive field and topographic organization of single orosensory neurons located throughout the rostral division of the nucleus of the solitary tract (rNST) was studied by determining their responsiveness to gustatory stimulation of the entire oral cavity and to gustatory and mechanical stimulation of restricted oral regions. The rNST contained roughly equal numbers of two distinct populations of orosensory neurons, one responsive exclusively to oral mechanical stimulation (M neurons), the other to gustatory stimulation (G neurons). Some G neurons also responded to oral somatosensory stimuli, but usually less vigorously than to gustatory stimuli. The distribution of these two populations of rNST neurons was topographically organized: G neurons were centered anteriorly and medially to M neurons. 2. Eight of 44 G neurons responded only when the whole oral cavity was stimulated, but the remaining 36 cells responded to circumscribed stimulation of taste buds on the anterior tongue (AT), foliate papillae of the posterior tongue, nasoincisor ducts, retromolar mucosa (RM), or soft palate (SP). Overall, AT and SP stimulation were the most effective, and RM stimulation the least effective, for activating nucleus of the solitary tract (NST) G neurons. 3. Approximately half of the G neurons for which a receptive field could be defined (N = 36) responded to stimulation of a single taste receptor subpopulation, but the remaining neurons received convergent input from two or more taste bud groups. The receptive field configurations for convergent G neurons were orderly; convergence occurred preferentially between receptor subpopulations either within the anterior oral cavity (AO) or the posterior oral cavity (PO). An AO-PO distinction also was reflected in the topographic organization of gustatory responses. The mean location of neurons responding optimally to AO gustatory stimulation was more anterior in the NST, and also tended to be more lateral and ventral than the location of neurons that responded optimally to PO stimulation. 4. Forty-four rNST M neurons responded to innocuous mechanical stimulation of restricted areas of the tongue, palate, buccal mucosa, or periodontium. Stimulation of the hard palate and circumvallate papilla were most effective, whereas periodontal stimulation was least effective for activating these cells. 5. A majority (32 of 44) of rNST M neurons responded to stimulation of more than one of the oral sites tested. The amount of central convergence this represents cannot be quantified precisely because some (n = 7) of the oral sites tested as separate fields share a common peripheral innervation, and thus the multiple responsiveness of these central neurons either could be accounted for by peripheral branching or by central convergence. After excluding these ambiguous instances, however, it was clear that ≥56.8{\%} of the M neurons received convergent central input. The configurations of the receptive fields for M neurons were more varied than those for G neurons. Although there was evidence that mechanical convergence occurred preferentially within the AO or PO, this tendency was weaker than for gustatory convergence. Nevertheless, an AO-PO distinction characterized the topographic organization of mechanical responses. The mean location of neurons that responded optimally to AO mechanical stimulation was more anterior and lateral, and also tended to be more ventral, than the location of neurons that responded optimally to PO stimulation. 6. The response properties of a smaller population (n = 21) of neurons just outside of the borders of the NST also were characterized. Most (n = 19) of these neurons were located on the lateral NST border, the medial spinal trigeminal nucleus, or in the intervening reticular formation. Almost all of the extra-NST neurons were M neurons. None responded to gustatory stimulation. The response properties of the M neurons outside the NST border were similar to those inside the nucleus, except that they exhibited a greater relative responsiveness to stimulation of oral sites located in the AO and a smaller relative responsiveness to sites located in the PO.",
author = "Travers, {S. P.} and Ralph Norgren",
year = "1995",
month = "1",
day = "1",
doi = "10.1152/jn.1995.73.6.2144",
language = "English (US)",
volume = "73",
pages = "2144--2162",
journal = "Journal of Neurophysiology",
issn = "0022-3077",
publisher = "American Physiological Society",
number = "6",

}

Organization of orosensory responses in the nucleus of the solitary tract of the rat. / Travers, S. P.; Norgren, Ralph.

In: Journal of Neurophysiology, Vol. 73, No. 6, 01.01.1995, p. 2144-2162.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Organization of orosensory responses in the nucleus of the solitary tract of the rat

AU - Travers, S. P.

AU - Norgren, Ralph

PY - 1995/1/1

Y1 - 1995/1/1

N2 - 1. The receptive field and topographic organization of single orosensory neurons located throughout the rostral division of the nucleus of the solitary tract (rNST) was studied by determining their responsiveness to gustatory stimulation of the entire oral cavity and to gustatory and mechanical stimulation of restricted oral regions. The rNST contained roughly equal numbers of two distinct populations of orosensory neurons, one responsive exclusively to oral mechanical stimulation (M neurons), the other to gustatory stimulation (G neurons). Some G neurons also responded to oral somatosensory stimuli, but usually less vigorously than to gustatory stimuli. The distribution of these two populations of rNST neurons was topographically organized: G neurons were centered anteriorly and medially to M neurons. 2. Eight of 44 G neurons responded only when the whole oral cavity was stimulated, but the remaining 36 cells responded to circumscribed stimulation of taste buds on the anterior tongue (AT), foliate papillae of the posterior tongue, nasoincisor ducts, retromolar mucosa (RM), or soft palate (SP). Overall, AT and SP stimulation were the most effective, and RM stimulation the least effective, for activating nucleus of the solitary tract (NST) G neurons. 3. Approximately half of the G neurons for which a receptive field could be defined (N = 36) responded to stimulation of a single taste receptor subpopulation, but the remaining neurons received convergent input from two or more taste bud groups. The receptive field configurations for convergent G neurons were orderly; convergence occurred preferentially between receptor subpopulations either within the anterior oral cavity (AO) or the posterior oral cavity (PO). An AO-PO distinction also was reflected in the topographic organization of gustatory responses. The mean location of neurons responding optimally to AO gustatory stimulation was more anterior in the NST, and also tended to be more lateral and ventral than the location of neurons that responded optimally to PO stimulation. 4. Forty-four rNST M neurons responded to innocuous mechanical stimulation of restricted areas of the tongue, palate, buccal mucosa, or periodontium. Stimulation of the hard palate and circumvallate papilla were most effective, whereas periodontal stimulation was least effective for activating these cells. 5. A majority (32 of 44) of rNST M neurons responded to stimulation of more than one of the oral sites tested. The amount of central convergence this represents cannot be quantified precisely because some (n = 7) of the oral sites tested as separate fields share a common peripheral innervation, and thus the multiple responsiveness of these central neurons either could be accounted for by peripheral branching or by central convergence. After excluding these ambiguous instances, however, it was clear that ≥56.8% of the M neurons received convergent central input. The configurations of the receptive fields for M neurons were more varied than those for G neurons. Although there was evidence that mechanical convergence occurred preferentially within the AO or PO, this tendency was weaker than for gustatory convergence. Nevertheless, an AO-PO distinction characterized the topographic organization of mechanical responses. The mean location of neurons that responded optimally to AO mechanical stimulation was more anterior and lateral, and also tended to be more ventral, than the location of neurons that responded optimally to PO stimulation. 6. The response properties of a smaller population (n = 21) of neurons just outside of the borders of the NST also were characterized. Most (n = 19) of these neurons were located on the lateral NST border, the medial spinal trigeminal nucleus, or in the intervening reticular formation. Almost all of the extra-NST neurons were M neurons. None responded to gustatory stimulation. The response properties of the M neurons outside the NST border were similar to those inside the nucleus, except that they exhibited a greater relative responsiveness to stimulation of oral sites located in the AO and a smaller relative responsiveness to sites located in the PO.

AB - 1. The receptive field and topographic organization of single orosensory neurons located throughout the rostral division of the nucleus of the solitary tract (rNST) was studied by determining their responsiveness to gustatory stimulation of the entire oral cavity and to gustatory and mechanical stimulation of restricted oral regions. The rNST contained roughly equal numbers of two distinct populations of orosensory neurons, one responsive exclusively to oral mechanical stimulation (M neurons), the other to gustatory stimulation (G neurons). Some G neurons also responded to oral somatosensory stimuli, but usually less vigorously than to gustatory stimuli. The distribution of these two populations of rNST neurons was topographically organized: G neurons were centered anteriorly and medially to M neurons. 2. Eight of 44 G neurons responded only when the whole oral cavity was stimulated, but the remaining 36 cells responded to circumscribed stimulation of taste buds on the anterior tongue (AT), foliate papillae of the posterior tongue, nasoincisor ducts, retromolar mucosa (RM), or soft palate (SP). Overall, AT and SP stimulation were the most effective, and RM stimulation the least effective, for activating nucleus of the solitary tract (NST) G neurons. 3. Approximately half of the G neurons for which a receptive field could be defined (N = 36) responded to stimulation of a single taste receptor subpopulation, but the remaining neurons received convergent input from two or more taste bud groups. The receptive field configurations for convergent G neurons were orderly; convergence occurred preferentially between receptor subpopulations either within the anterior oral cavity (AO) or the posterior oral cavity (PO). An AO-PO distinction also was reflected in the topographic organization of gustatory responses. The mean location of neurons responding optimally to AO gustatory stimulation was more anterior in the NST, and also tended to be more lateral and ventral than the location of neurons that responded optimally to PO stimulation. 4. Forty-four rNST M neurons responded to innocuous mechanical stimulation of restricted areas of the tongue, palate, buccal mucosa, or periodontium. Stimulation of the hard palate and circumvallate papilla were most effective, whereas periodontal stimulation was least effective for activating these cells. 5. A majority (32 of 44) of rNST M neurons responded to stimulation of more than one of the oral sites tested. The amount of central convergence this represents cannot be quantified precisely because some (n = 7) of the oral sites tested as separate fields share a common peripheral innervation, and thus the multiple responsiveness of these central neurons either could be accounted for by peripheral branching or by central convergence. After excluding these ambiguous instances, however, it was clear that ≥56.8% of the M neurons received convergent central input. The configurations of the receptive fields for M neurons were more varied than those for G neurons. Although there was evidence that mechanical convergence occurred preferentially within the AO or PO, this tendency was weaker than for gustatory convergence. Nevertheless, an AO-PO distinction characterized the topographic organization of mechanical responses. The mean location of neurons that responded optimally to AO mechanical stimulation was more anterior and lateral, and also tended to be more ventral, than the location of neurons that responded optimally to PO stimulation. 6. The response properties of a smaller population (n = 21) of neurons just outside of the borders of the NST also were characterized. Most (n = 19) of these neurons were located on the lateral NST border, the medial spinal trigeminal nucleus, or in the intervening reticular formation. Almost all of the extra-NST neurons were M neurons. None responded to gustatory stimulation. The response properties of the M neurons outside the NST border were similar to those inside the nucleus, except that they exhibited a greater relative responsiveness to stimulation of oral sites located in the AO and a smaller relative responsiveness to sites located in the PO.

UR - http://www.scopus.com/inward/record.url?scp=0029013295&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0029013295&partnerID=8YFLogxK

U2 - 10.1152/jn.1995.73.6.2144

DO - 10.1152/jn.1995.73.6.2144

M3 - Article

C2 - 7666129

AN - SCOPUS:0029013295

VL - 73

SP - 2144

EP - 2162

JO - Journal of Neurophysiology

JF - Journal of Neurophysiology

SN - 0022-3077

IS - 6

ER -