Tzu Chi Medical Journal
Volume 19, Issue 4 , Pages 181-185, December 2007

Cellular Heterogeneity Within the Solitary Tract Nucleus and Visceral Afferent Processing—Electrophysiological Approaches to Discerning Pathway Performance

  • Michael C. Andresen

      Affiliations

    • Department of Physiology and Pharmacology, Oregon Health and Science University, Portland, Oregon, USA
    • Corresponding Author InformationCorresponding author. Department of Physiology and Pharmacology, Oregon Health and Science University, 3181 SW Sam Jackson Park Road, Portland, Oregon 97239-3098, USA
  • ,
  • Timothy W. Bailey

      Affiliations

    • Department of Physiology and Pharmacology, Oregon Health and Science University, Portland, Oregon, USA
  • ,
  • Young-Ho Jin

      Affiliations

    • Department of Physiology and Pharmacology, Oregon Health and Science University, Portland, Oregon, USA
  • ,
  • Stuart J. McDougall

      Affiliations

    • Department of Physiology and Pharmacology, Oregon Health and Science University, Portland, Oregon, USA
  • ,
  • James H. Peters

      Affiliations

    • Department of Physiology and Pharmacology, Oregon Health and Science University, Portland, Oregon, USA
  • ,
  • Sue A. Aicher

      Affiliations

    • Institute of Neurological Sciences, Oregon Health and Science University, Portland, Oregon, USA

Received 12 June 2007; received in revised form 17 September 2007; accepted 20 September 2007.

Article Outline

Abstract 

Many homeostatic reflexes depend on autonomic central nervous system mechanisms to systemically coordinate visceral organ function. The nucleus of the solitary tract (NTS) is the common entry of cranial visceral afferents into these regulatory pathways. Such NTS neurons initiate adjustments in cardiovascular, respiratory, gastrointestinal and other visceral systems. Diversity of neurons within the NTS appears integral to such pro cessing but is daunting to approach experimentally. This review outlines three experimental approaches to understanding cellular heterogeneity within NTS and its relation to function. Brainstem slice preparations coupled with patch recordings afford cellular–molecular resolution with substantial links to the more intact system. Pharmacological approaches based on visceral afferent phenotype have helped identify myelinated and unmyelinated solitary tract inputs to NTS neurons. An interesting outcome has been the robust association of A-type potassium currents with NTS neurons receiving unmyelinated afferents. Neuroanatomical tracers offer a second, complementary approach. Anterograde transport of fluorescent dye identifies cranial visceral afferent terminals on second order neurons that cluster on or proximal to the soma—a highly unusual distribution in the central nervous system. Thus, second order baroreceptive neurons can be identified neuroanatomically in vitro. Equally helpful has been identification of NTS projection neurons by retrograde tracers injected into target regions of the hypothalamus or brainstem and this approach indicates substantial specialization—relative homogeneous neurons within the overall heterogeneity of NTS. Lastly, transgenic mouse strains, particularly those expressing marker chromophores, have identified phenotypic subtypes such as GABAergic inhibitory neurons within NTS. Combined methodologies are forging new understanding of NTS and autonomic regulation.

keywords:  C-fiber , Parasympathetic , Paraventricular nucleus , Sensory , Vagus

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References 

  1. Andresen MC , Kunze DL . Nucleus tractus solitarius: gateway to neural circulatory control . Ann Rev Physiol . 1994;56:93–116
  2. Pilowsky PM , Goodchild AK . Baroreceptor reflex pathways and neurotransmitters: 10 years on . J Hypertens . 2002;20:1675–1688
  3. Travagli RA , Hermann GE , Browning KN , Rogers RC . Brainstem circuits regulating gastric function . Ann Rev Physiol . 2006;68:279–305
  4. Jordan D . Central nervous pathways and control of the airways . Respir Physiol . 2001;125:67–81
  5. Loewy AD . Central autonomic pathways . In:  Loewy AD ,  Spyer KM editor. Central Regulation of Autonomic Functions . New York: Oxford University Press; 1990;p. 88–103
  6. Chan RK , Sawchenko PE . Organization and transmitter specificity of medullary neurons activated by sustained hypertension: implications for understanding baroreceptor reflex circuitry . J Neurosci . 1998;18:371–387
  7. Monnikes H , Lauer G , Arnold R . Peripheral administration of cholecystokinin activates c-fos expression in the locus coeruleus/subcoeruleus nucleus, dorsal vagal complex and paraventricular nucleus via capsaicin-sensitive vagal afferents and CCK-A receptors in the rat . Brain Res . 1997;770:277–288
  8. Dahlstrom A , Fuxe K . Evidence for the existence of monoamine-containing neurons in the central nervous system I. Demonstration of monoamines in the cell bodies of brain stem neurons . Acta Physiol Scand . 1964;62:1–79
  9. Lawson SN . Phenotype and function of somatic primary afferent nociceptive neurones with C-, Adelta-or Aalpha/beta-fibres . Exp Physiol . 2002;87:239–244
  10. Andresen MC , Doyle MW , Bailey TW , Jin YH . Differentiation of autonomic reflex control begins with cellular mechanisms at the first synapse within the nucleus tractus solitarius . Braz J Med Biol Res . 2004;37:549–558
  11. Tominaga M , Caterina MJ , Malmberg AB , et al.   The cloned capsaicin receptor integrates multiple pain-producing stimuli . Neuron . 1998;21:531–543
  12. Reynolds PJ , Fan W , Andresen MC . Capsaicin-resistant arterial baroreceptors . J Negat Results Biomed . 2006;5:6
  13. Fan W , Andresen MC . Differential frequency-dependent reflex integration of myelinated and nonmyelinated rat aortic baroreceptors . Am J Physiol . 1998;275:H632–H640
  14. Bailey TW , Jin YH , Doyle MW , Smith SM , Andresen MC . Vasopressin inhibits glutamate release via two distinct modes in the brainstem . J Neurosci . 2006;26:6131–6142
  15. Bailey TW , Jin YH , Doyle MW , Andresen MC . Vanilloid sensitive afferents activate neurons with prominent A-type potassium currents in nucleus tractus solitarius . J Neurosci . 2002;22:8230–8237
  16. Bailey TW , Hermes SM , Andresen MC , Aicher SA . Cranial visceral afferent pathways through the nucleus of the solitary tract to caudal ventrolateral medulla or paraventricular hypothalamus: target-specific synaptic reliability and convergence patterns . J Neurosci . 2006;26:11893–11902
  17. Doyle MW , Bailey TW , Jin YH , Andresen MC . Vanilloid receptors presynaptically modulate visceral afferent synaptic transmission in nucleus tractus solitarius . J Neurosci . 2002;22:8222–8229
  18. Jin YH , Bailey TW , Doyle MW , et al.   Ketamine differentially blocks sensory afferent synaptic transmission in medial nucleus tractus solitarius (mNTS) . Anesthesiology . 2003;98:121–132
  19. Jin YH , Bailey TW , Andresen MC . Cranial afferent glutamate heterosynaptically modulates GABA release onto second-order neurons via distinctly segregated metabotropic gluta-mate receptors . J Neurosci . 2004;24:9332–9340
  20. Jin YH , Bailey TW , Li BY , Schild JH , Andresen MC . Purinergic and vanilloid receptor activation releases glutamate from separate cranial afferent terminals in nucleus tractus solitarius . J Neurosci . 2004;24:4709–4717
  21. Bailey TW , Hermes SM , Aicher SA , Andresen MC . Target-specific, dynamic pathway tuning by A-type potassium channels in solitary tract nucleus: cranial visceral afferent pathways to caudal ventrolateral medulla or paraventricular hypothalamus . J Physiol . 2007;582:613–628
  22. Barnes KL , DeWeese DM , Andresen MC . Angiotensin potentiates excitatory synaptic transmission to medial solitary tract nucleus neurons . Am J Physiol Regul Integr Comp Physiol . 2003;284:R1340–R1353
  23. Appleyard SM , Bailey TW , Doyle MW , et al.   Proopiomelanocortin neurons in nucleus tractus solitarius are activated by visceral afferents: regulation by cholecystokinin and opioids . J Neurosci . 2005;25:3578–3585
  24. Devor M , Wall PD . Effect of peripheral nerve injury on receptive fields of cells in the cat spinal cord . J Comp Neurol . 1981;199:277–291
  25. Mannion RJ , Doubell TP , Coggeshall RE , Woolf CJ . Collateral sprouting of uninjured primary afferent A-fibers into the superficial dorsal horn of the adult rat spinal cord after topical capsaicin treatment to the sciatic nerve . J Neurosci . 1996;16:5189–5195
  26. Mukherjee S , Soe TT , Maxfield FR . Endocytic sorting of lipid analogues differing solely in the chemistry of their hydrophobic tails . J Cell Biol . 1999;144:1271–1284
  27. Doyle MW , Bailey TW , Jin YH , Appleyard SM , Low MJ , Andresen MC . Strategies for cellular identification in nucleus tractus solitarius slices . J Neurosci Methods . 2004;37:37–48
  28. Oliva AA , Jiang M , Lam T , Smith KL , Swann JW . Novel hippocampal interneuronal subtypes identified using transgenic mice that express green fluorescent protein in GABAergic interneurons . J Neurosci . 2000;20:3354–3368
  29. Bailey TW , Appleyard SM , Andresen MC . Cranial visceral afferent transmission to GABAergic neurons in nucleus tractus solitarius (NTS) from GAD-EGFP mice . Soc Neurosci Abstr . 2005;

PII: S1016-3190(10)60014-6

doi:10.1016/S1016-3190(10)60014-6

Tzu Chi Medical Journal
Volume 19, Issue 4 , Pages 181-185, December 2007