Direct excitation of mitral cells via activation of alpha1-noradrenergic receptors in rat olfactory bulb slices

J Neurophysiol. 2001 Nov;86(5):2173-82. doi: 10.1152/jn.2001.86.5.2173.

Abstract

The main olfactory bulb receives a significant modulatory noradrenergic input from the locus coeruleus. Previous in vivo and in vitro studies showed that norepinephrine (NE) inputs increase the sensitivity of mitral cells to weak olfactory inputs. The cellular basis for this action of NE is not understood. The goal of this study was to investigate the effect of NE and noradrenergic agonists on the excitability of mitral cells, the main output cells of the olfactory bulb, using whole cell patch-clamp recording in vitro. The noradrenergic agonists, phenylephrine (PE, 10 microM), isoproterenol (Isop, 10 microM), and clonidine (3 microM), were used to test for the functional presence of alpha1-, beta-, and alpha2-receptors, respectively, on mitral cells. None of these agonists affected olfactory nerve (ON)-evoked field potentials recorded in the glomerular layer, or ON-evoked postsynaptic currents recorded in mitral cells. In whole cell voltage-clamp recordings, NE (30 microM) induced an inward current (54 +/- 7 pA, n = 16) with an EC(50) of 4.7 microM. Both PE and Isop also produced inward currents (22 +/- 4 pA, n = 19, and 29 +/- 9 pA, n = 8, respectively), while clonidine produced no effect (n = 6). In the presence of TTX (1 microM), and blockers of excitatory and inhibitory fast synaptic transmission [gabazine 5 microM, 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX) 10 microM, and (+/-)-2-amino-5-phosphonopentanoic acid (APV) 50 microM], the inward current induced by PE persisted (EC(50) = 9 microM), whereas that of Isop was absent. The effect of PE was also observed in the presence of the Ca(2+) channel blockers, cadmium (100 microM) and nickel (100 microM). The inward current caused by PE was blocked when the interior of the cell was perfused with the nonhydrolyzable GDP analogue, GDPbetaS, indicating that the alpha1 effect is mediated by G-protein coupling. The current-voltage relationship in the absence and presence of PE indicated that the current induced by PE decreased near the equilibrium potential for potassium ions. In current-clamp recordings from bistable mitral cells, PE shifted the membrane potential from the downstate (-52 mV) toward the upstate (-40 mV), and significantly increased spike generation in response to perithreshold ON input. These findings indicate that NE excites mitral cells directly via alpha1 receptors, an effect that may underlie, at least in part, increased mitral cell responses to weak ON input during locus coeruleus activation in vivo.

Publication types

  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Adrenergic alpha-Agonists / pharmacology
  • Animals
  • Evoked Potentials / physiology
  • Excitatory Postsynaptic Potentials / physiology
  • In Vitro Techniques
  • Membrane Potentials / drug effects
  • Membrane Potentials / physiology
  • Neurons / drug effects
  • Neurons / physiology
  • Norepinephrine / metabolism*
  • Olfactory Bulb / cytology
  • Olfactory Bulb / drug effects
  • Olfactory Bulb / physiology*
  • Olfactory Nerve / physiology
  • Rats
  • Rats, Sprague-Dawley
  • Receptors, Adrenergic, alpha-1 / physiology*

Substances

  • Adrenergic alpha-Agonists
  • Receptors, Adrenergic, alpha-1
  • Norepinephrine