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The Journal of Neuroscience, October 8, 2008, 28(41):10311-10322; doi:10.1523/JNEUROSCI.2608-08.2008

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Cellular/Molecular
Intrinsic Conductances Actively Shape Excitatory and Inhibitory Postsynaptic Responses in Olfactory Bulb External Tufted Cells

Shaolin Liu and Michael T. Shipley

Department of Anatomy and Neurobiology, Program in Neuroscience, University of Maryland School of Medicine, Baltimore, Maryland 21201

Correspondence should be addressed to Michael T. Shipley, Department of Anatomy and Neurobiology, Program in Neuroscience, University of Maryland School of Medicine, 20 Penn Street, Baltimore, MD 21201. Email: mshipley{at}umaryland.edu

The initial synapse in the olfactory system is from olfactory nerve (ON) terminals to postsynaptic targets in olfactory bulb glomeruli. Recent studies have disclosed multiple presynaptic factors that regulate this important linkage, but less is known about the contribution of postsynaptic intrinsic conductances to integration at these synapses. The present study demonstrates voltage-dependent amplification of EPSPs in external tufted (ET) cells in response to monosynaptic (ON) inputs. This amplification is mainly exerted by persistent Na⁺ conductance. Larger EPSPs, which bring the membrane potential to a relatively depolarized level, are further boosted by the low-voltage-activated Ca²⁺ conductance. In contrast, the hyperpolarization-activated nonselective cation conductance (I_h) attenuates EPSPs mainly by reducing EPSP duration; this also reduces temporal summation of multiple EPSPs. Regulation of EPSPs by these subthreshold, voltage-dependent conductances can enhance both the signal-to-noise ratio and the temporal summation of multiple synaptic inputs and thus help ET cells differentiate high- and low-frequency synaptic inputs. I_h can also transform inhibitory inputs to postsynaptic excitation. When the ET cell membrane potential is relatively depolarized, as during a burst of action potentials, IPSPs produce classic inhibition. However, near resting membrane potentials where I_h is engaged, IPSPs produce rebound bursts of action potentials. ET cells excite GABAergic PG cells. Thus, the transformation of inhibitory inputs to postsynaptic excitation in ET cells may enhance intraglomerular inhibition of mitral/tufted cells, the main output neurons in the olfactory bulb, and hence shape signaling to olfactory cortex.

Key words: synaptic integration; persistent Na⁺ current; hyperpolarization-activated nonselective cation current; EPSP; IPSP; rebound depolarization

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Received June 6, 2008; revised Aug. 12, 2008; accepted Sept. 1, 2008.

Correspondence should be addressed to Michael T. Shipley, Department of Anatomy and Neurobiology, Program in Neuroscience, University of Maryland School of Medicine, 20 Penn Street, Baltimore, MD 21201. Email: mshipley{at}umaryland.edu

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