1. The effects of three metabotropic glutamate receptor (mGluR) agonists were tested in two pathways of rat piriform cortex. The group I, II and III mGluR agonists used were RS-3,5-dihydroxyphenenylglycine (DHPG) (10–100 μM), (2S,1′S,2′S)-2-Carboxycyclopropyl (L-CCG) (20–100 μM) and L(+)-2-amino-4-phosphonobutyric acid (L-AP4) (5–500 μM), respectively.
2. The effects of the three groups of agonists on synaptic transmission in the two piriform cortex pathways also were examined. All three agonists reduced the amplitude of the monosynaptic EPSPs generated by stimulation of the lateral olfactory tract (LOT) or of the association fiber pathway (ASSN). This was always accompanied by an increase in paired pulse facilitation.
3. Group I and II mGluR agonists had similar synaptic effects on the two pathways, while the group III mGluR agonist suppressed the LOT pathway more than the association pathway.
4. The group II and III mGluR agonists had no effect on passive membrane properties of pyramidal neurons. Group I agonists depolarized the pyramidal neuron membrane potential, and enhanced both membrane resistance and noise.
5. Our data suggest that all three types of mGluRs modulate synaptic transmission in both of these pathways in piriform cortex. Only group I agonists alter post-synaptic membrane properties, while all three types of receptor regulate synaptic transmission. Groups I and II are equally potent in the LOT and association fiber pathways, while group III receptors are more potent in the LOT than the association fiber pathways.
Similar content being viewed by others
REFERENCES
Anwyl, R. (1999). Metabotropic glutamate receptors: Electrophysiological properties and role in plasticity. Brain Res. Rev. 29:83–120.
Benitez, R., Fernadnez-Capetillo, O., Lazaro, E., Mateos, J. M., Osorio, A., Elezgarai, I., Bilbao, A., Kingenhoehl, K., Van Der Putten, H., Hampson, D. R., Kuhn, R., Knopfel, T., and Grandes, P. (2000). Immunocytochemical localization of the metabotropic glutamate receptor mGluR4a in the piriform cortex of the rat. J. Comp. Neurol. 417:263–274.
Best, A. R., Thompson, J. V., Fletcher, M. L., and Wilson, D. A. (2005). Cortical metabotropic glutamate receptors contribute to habituation of a simple odor-evoked behavior. J. Neurosci. 25:2513–2517.
Bortolotto, Z. A., Fitzjohn, S. M., and Collingridge, G. L. (1999). Roles of metabotropic glutamate receptors in LTP and LTD in the hippocampus. Cur. Opinion Neurobiol. 9:299–304.
Conn, P. J., and Pin, J. P. (1997). Pharmacology and functions of metabotropic glutamate receptors. Ann. Rev. Pharmacol. 37:205–237.
Davis, S., and Laroache, S. (1996). Activation of metabotropic glutamate receptors induce differential effects on synaptic transmission in the dentate gyrus and CA1 of the hippocampus in the anaesthetized rat. Neuropharmacology 35:337–346.
Debanne, D., Guerineau, N. C., Gahwiler, B. H., and Thompson, S. M. (1996). Paired-pulse facilitation and depression at unitary synapses in rat hippocampus: quantal fluctuation affects subsequent release. J. Physiol. (Lond.) 491(1):163–176.
ffrench-Mullen, J. M. H., Hori, N., and Carpenter, D. O. (1986). Receptors for the excitatory amino acids on neurons in rat pyriform cortex. J. Neurophysiol. 55:1283–1294.
Gereau, R. W., and Conn, P. J. (1995). Multiple presynaptic metabotropic glutamate receptors modulate excitatory and inhibitory synaptic transmission in hippocampal area CA1. J. Neurosci. 15:6879–6889.
Haberly, L. B. (1990) Olfactory cortex. In Shepherd, G. M. (ed.), The Synaptic Organization of the Brain, chapter 10, Oxford University Press, New York, New Tork, pp. 317–345.
Hess, G., Kuhnt, U., and Voronin, L. L. (1987). Quantal analysis of paired-pulse facilitation in guinea pig hippocampal slices. Neurosci. Letts. 77:187–192.
Hori, N., Akaike, N., and Carpenter, D. O. (1988). Piriform cortex brain slices: Techniques for isolation of synaptic inputs. J. Neurosci. Meth 25:197–208.
Kinoshita, A., Ohishi, H., Neki, A., Nomura, S., Shigemoto, R., Takada, M., Nakanishi, S., and Mizuno, N. (1996). Presynaptic localization of a metabotropic glutamate receptor, mGluR8, in the rhinencephalic areas: a light an electron microscope study in the rat. Neurosci. Lett. 207:61–64.
Kinzie, J. M., Shinohara, M. M., Van Den Pol, A. N., Westbrook, G. L., and Segerson, T. P. (1997). Immunolocalization of metabotropic glutamate receptor 7 in the rat olfactory bulb. J. Comp. Neurol 385:372–384.
Mannaioni, G., Marino, M. J., Valenti, O., Traynelis, S. F., and Conn, P. J. (2001). Metabotropic glutamate receptors 1 and 5 differentially regulate CA1 pyramidal cell function. J. Neurosci. 21:5925–5934.
Ong, W. Y., He, Y., Tan, K. K., and Garey, L. J. (1998). Differential localization of the metabotropic glutamate receptor mGluR1a and the ionotropic glutamate receptor GluR2/3 in neurons of the human cerebral cortex. Exp. Brain Res. 119:367–374.
Riedel, G., and Reymann, K. G. (1996). Metabotropic glutamate receptors in hippocampal long-term potentiation and learning and memory. Act. Physiol. Scand 157:1–19.
Shigemoto, R., Kinoshita, A., Wada, E., Nomura, S., Ohishi, H., Takada, M., Flor, P. J., Neki, A., Abe, T., Nakanishi, S., and Mizuno, N. (1997). Differential presynaptic localization of metabotropic glutamate receptor subtypes in the rat hippocampus. J. Neurosci. 17:7503–7522.
Sugitani, M., Sugai, T., and Onoda, N. (2004). Postsynaptic metabotropic glutamate receptors mGluR1 mediates the alter component of signal propagation in the guinea pig piriform cortex: optical imaging study. Neurosci. Letts. 356:29–32.
Tan, Y., Hori, N., and Carpenter, D. O. (2003). The mechanism of presynaptic long-term depression mediated by group I metabotropic glutamate receptors. Cell. Molec. Neurobiol. 23:187–203.
Wada, E., Shigemoto, R., Kinoshita, A., Ohishi, H., and Mizuno, N. (1998). Metabotropic glutamate receptor subtypes in axon terminals of projection fibers from the main and accessory olfactory bulbs: A light and electron microscopic immunohistochemical study in the rat. J. Comp. Neurol. 393:493–504.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Tan, Y., Hori, N. & Carpenter, D. Electrophysiological Effects of Three Groups of Glutamate Metabotropic Receptors in Rat Piriform Cortex. Cell Mol Neurobiol 26, 913–922 (2006). https://doi.org/10.1007/s10571-006-9102-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10571-006-9102-4