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The Journal of Neuroscience, January 21, 2004, 24(3):652-660; doi:10.1523/JNEUROSCI.4220-03.2004

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Behavioral/Systems/Cognitive
Coordinate Synaptic Mechanisms Contributing to Olfactory Cortical Adaptation

Aaron R. Best and Donald A. Wilson

Department of Zoology, University of Oklahoma, Norman, Oklahoma 73019

Anterior piriform cortex (aPCX) neurons rapidly filter repetitive odor stimuli despite relatively maintained input from mitral cells. This cortical adaptation is correlated with short-term depression of afferent synapses, in vivo. The purpose of this study was to elucidate mechanisms underlying this nonassociative neural plasticity using in vivo and in vitro preparations and to determine its role in cortical odor adaptation. Lateral olfactory tract (LOT)-evoked responses were recorded in rat aPCX coronal slices. Extracellular and intracellular potentials were recorded before and after simulated odor stimulation of the LOT. Results were compared with in vivo intracellular recordings from aPCX layer II/III neurons and field recordings in urethane-anesthetized rats stimulated with odorants. The onset, time course, and extent of LOT synaptic depression during both in vitro electrical and in vivo odorant stimulation methods were similar. Similar to the odor specificity of cortical odor adaptation in vivo, there was no evidence of heterosynaptic depression between independent inputs in vitro. In vitro evidence suggests at least two mechanisms contribute to this activity-dependent synaptic depression: a rapidly recovering presynaptic depression during the initial 10-20 sec of the post-train recovery period and a longer lasting (~120 sec) depression that can be blocked by the metabotropic glutamate receptor (mGluR) II/III antagonist (RS)-{alpha}-cyclopropyl-4-phosphonophenylglycine (CPPG) and by the {beta}-adrenergic receptor agonist isoproterenol. Importantly, in line with the in vitro findings, both adaptation of odor responses in the {beta} (15-35 Hz) spectral range and the associated synaptic depression can also be blocked by intracortical infusion of CPPG in vivo.

Key words: habituation; olfaction; neuronal adaptation; synaptic depression; piriform cortex; vesicle depletion; metabotropic glutamate receptor; isoproterenol


Received Sep 15, 2003; revised October 28, 2003; accepted November 13, 2003.




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