QUICK SEARCH:   [advanced] Author: Keyword(s): Year:  Vol:  Page:

HOME  |   SEARCH  |   ARCHIVE  |   SUBSCRIBE  |   CONTACT  |   HELP

The Journal of Neuroscience, October 20, 2004, 24(42):9332-9340; doi:10.1523/JNEUROSCI.1991-04.2004

This Article Full Text Full Text (PDF) Submit an eLetter Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in ISI Web of Science Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via ISI Web of Science (15) Citing Articles via Google Scholar Google Scholar Articles by Jin, Y.-H. Articles by Andresen, M. C. Search for Related Content PubMed PubMed Citation Articles by Jin, Y.-H. Articles by Andresen, M. C.

 Previous Article  |  Next Article 

Behavioral/Systems/Cognitive
Cranial Afferent Glutamate Heterosynaptically Modulates GABA Release onto Second-Order Neurons via Distinctly Segregated Metabotropic Glutamate Receptors

Young-Ho Jin, Timothy W. Bailey, and Michael C. Andresen

Department of Physiology and Pharmacology, Oregon Health and Science University, Portland, Oregon 97239-3098

The balance between excitation and inhibition dictates central integration. Glutamatergic and GABAergic neurotransmission dominate this process. Cranial primary afferents enter the brainstem to release glutamate (Glu) onto second-order neurons within the caudal nucleus tractus solitarius (NTS) to initiate autonomic reflexes. The simplest pathways for these reflexes contain as few as two central neurons, but display robust frequency-dependent behavior. Within NTS, multiple metabotropic Glu receptors (mGluRs) are present, but their roles are poorly understood. Using synaptically discriminated second-order NTS neurons in brainstem slices and mechanically dissociated NTS neurons with intact boutons, we show that Glu differentially controls GABA release via distinct presynaptic mGluRs. In second-order NTS neurons recorded in slices, activation of primary afferents at frequencies as low as 10 shocks per second released sufficient Glu to alter rates of spontaneous IPSCs (sIPSCs). In both approaches, group I mGluRs increased GABA release in some neurons, but, on different neurons, group II and group III mGluRs decreased the sIPSC rate. mGluR actions were remarkably rapid, with onset and reversal beginning within 100 msec. In all cases, mGluR actions were exclusively presynaptic, and mGluRs did not alter postsynaptic properties in second-order neurons in either slices or isolated neurons. Tests with capsaicin and -methylene ATP suggest that myelinated and unmyelinated afferent pathways engage both mGluR-GABA mechanisms. Afferent Glu spillover provides heterosynaptic cross talk with GABAergic inhibition in NTS. This process may critically shape the dynamic character and use dependence for cranial afferent transmission at the first stage of autonomic reflexes.

Key words: presynaptic modulation; autonomic; brainstem; nucleus tractus solitarius; GABA; afferent; baroreceptor; sensory neurons; slice; glutamate; metabotropic; heterosynaptic

---

Received May 21, 2004; revised August 17, 2004; accepted August 31, 2004.

This article has been cited by other articles:

				Y.-H. Hsieh, T. E. Dick, and R. E. Siegel Adaptation to hypobaric hypoxia involves GABAA receptors in the pons Am J Physiol Regulatory Integrative Comp Physiol, February 1, 2008; 294(2): R549 - R557. [Abstract] [Full Text] [PDF]

				K. N. Browning and R. A. Travagli Functional Organization of Presynaptic Metabotropic Glutamate Receptors in Vagal Brainstem Circuits J. Neurosci., August 22, 2007; 27(34): 8979 - 8988. [Abstract] [Full Text] [PDF]

				T. W. Bailey, S. M. Hermes, M. C. Andresen, and S. A. Aicher 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., November 15, 2006; 26(46): 11893 - 11902. [Abstract] [Full Text] [PDF]

				A. V. Derbenev, M. J. Monroe, N. R. Glatzer, and B. N. Smith Vanilloid-mediated heterosynaptic facilitation of inhibitory synaptic input to neurons of the rat dorsal motor nucleus of the vagus. J. Neurosci., September 20, 2006; 26(38): 9666 - 9672. [Abstract] [Full Text] [PDF]

				A. E. Simms, J. F. R. Paton, and A. E. Pickering Disinhibition of the cardiac limb of the arterial baroreflex in rat: a role for metabotropic glutamate receptors in the nucleus tractus solitarii J. Physiol., September 15, 2006; 575(3): 727 - 738. [Abstract] [Full Text] [PDF]

				K. N. Browning, Z. Zheng, T. W. Gettys, and R. A. Travagli Vagal afferent control of opioidergic effects in rat brainstem circuits J. Physiol., September 15, 2006; 575(3): 761 - 776. [Abstract] [Full Text] [PDF]

				S.-i. Sekizawa and A. C. Bonham Group I Metabotropic Glutamate Receptors on Second-Order Baroreceptor Neurons Are Tonically Activated and Induce a Na+-Ca2+ Exchange Current J Neurophysiol, February 1, 2006; 95(2): 882 - 892. [Abstract] [Full Text] [PDF]

Home  |   Search  |   Archive  |   Subscribe  |   Contact  |   Help