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The Journal of Neuroscience, September 7, 2005, 25(36):8197-8208; doi:10.1523/JNEUROSCI.2374-05.2005

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Cellular/Molecular
Olfactory Bulb External Tufted Cells Are Synchronized by Multiple Intraglomerular Mechanisms

Abdallah Hayar,¹ Michael T. Shipley,² and Matthew Ennis¹

¹Department of Anatomy and Neurobiology, University of Tennessee Health Science Center, Memphis, Tennessee 38163, and ²Department of Anatomy and Neurobiology, Program in Neuroscience, University of Maryland, Baltimore, Maryland 21201

In rat olfactory bulb slices, external tufted (ET) cells spontaneously generate spike bursts. Only ET cells affiliated with the same glomerulus exhibit significant synchronous activity, suggesting that synchrony results mainly from intraglomerular interactions. The intraglomerular mechanisms underlying their synchrony are unknown. Using dual extracellular and patch-clamp recordings from ET cell pairs of the same glomerulus, we found that the bursting of ET cells is synchronized by several mechanisms. First, ET cell pairs of the same glomerulus receive spontaneous synchronous fast excitatory synaptic input that can also be evoked by olfactory nerve stimulation. Second, they exhibit correlated spontaneous slow excitatory synaptic currents that can also be evoked by stimulation of the external plexiform layer. These slow currents may reflect the repetitive release of glutamate via spillover from the dendritic tufts of other ET or mitral/tufted cells affiliated with the same glomerulus. Third, ET cells exhibit correlated bursts of inhibitory synaptic activity immediately after the synchronous fast excitatory input. These bursts of IPSCs were eliminated by CNQX and may therefore reflect correlated feedback inhibition from periglomerular cells that are driven by ET cell spike bursts. Fourth, in the presence of fast synaptic blockers, ET cell pairs exhibit synchronous slow membrane current oscillations associated with rhythmic spikelets, which were sensitive to the gap junction blocker carbenoxolone. These findings suggest that coordinated synaptic transmission and gap junction coupling synchronize the spontaneous bursting of ET cells of the same glomerulus.

Key words: external tufted; bursting; dual recordings; coefficient of correlation; IPSCs; synchrony

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Received March 1, 2005; revised July 27, 2005; accepted July 27, 2005.

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