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Research Articles, Systems/Circuits

Synaptic Organization of Anterior Olfactory Nucleus Inputs to Piriform Cortex

Marco J. Russo, Kevin M. Franks, Roxanne Oghaz, Richard Axel and Steven A. Siegelbaum
Journal of Neuroscience 2 December 2020, 40 (49) 9414-9425; DOI: https://doi.org/10.1523/JNEUROSCI.0965-20.2020
Marco J. Russo
1Department of Neuroscience, Vagelos College of Physicians and Surgeons, Columbia University, New York, New York
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Kevin M. Franks
1Department of Neuroscience, Vagelos College of Physicians and Surgeons, Columbia University, New York, New York
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Roxanne Oghaz
1Department of Neuroscience, Vagelos College of Physicians and Surgeons, Columbia University, New York, New York
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Richard Axel
2Mortimer B. Zuckerman Mind Brain Behavior Institute, Department of Neuroscience, Department of Biochemistry and Molecular Biophysics, Howard Hughes Medical Institute, Vagelos College of Physicians & Surgeons, Columbia University, New York, New York
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Steven A. Siegelbaum
3Department of Neuroscience, Kavli Institute for Brain Science, Mortimer B. Zuckerman Mind Brain Behavior Institute, Department of Pharmacology, Vagelos College of Physicians and Surgeons, Columbia University, New York, New York
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Abstract

Odors activate distributed ensembles of neurons within the piriform cortex, forming cortical representations of odor thought to be essential to olfactory learning and behaviors. This odor response is driven by direct input from the olfactory bulb, but is also shaped by a dense network of associative or intracortical inputs to piriform, which may enhance or constrain the cortical odor representation. With optogenetic techniques, it is possible to functionally isolate defined inputs to piriform cortex and assess their potential to activate or inhibit piriform pyramidal neurons. The anterior olfactory nucleus (AON) receives direct input from the olfactory bulb and sends an associative projection to piriform cortex that has potential roles in the state-dependent processing of olfactory behaviors. Here, we provide a detailed functional assessment of the AON afferents to piriform in male and female C57Bl/6J mice. We confirm that the AON forms glutamatergic excitatory synapses onto piriform pyramidal neurons; and while these inputs are not as strong as piriform recurrent collaterals, they are less constrained by disynaptic inhibition. Moreover, AON-to-piriform synapses contain a substantial NMDAR-mediated current that prolongs the synaptic response at depolarized potentials. These properties of limited inhibition and slow NMDAR-mediated currents result in strong temporal summation of AON inputs within piriform pyramidal neurons, and suggest that the AON could powerfully enhance activation of piriform neurons in response to odor.

SIGNIFICANCE STATEMENT Odor information is transmitted from olfactory receptors to olfactory bulb, and then to piriform cortex, where ensembles of activated neurons form neural representations of the odor. While these ensembles are driven by primary bulbar afferents, and shaped by intracortical recurrent connections, the potential for another early olfactory area, the anterior olfactory nucleus (AON), to contribute to piriform activity is not known. Here, we use optogenetic circuit-mapping methods to demonstrate that AON inputs can significantly activate piriform neurons, as they are coupled to NMDAR currents and to relatively modest disynaptic inhibition. The AON may enhance the piriform odor response, encouraging further study to determine the states or behaviors through which AON potentiates the cortical response to odor.

  • anterior olfactory cortex
  • anterior olfactory nucleus
  • associational synapses
  • intracortical synapses
  • olfactory cortex
  • piriform cortex

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The Journal of Neuroscience: 40 (49)
Journal of Neuroscience
Vol. 40, Issue 49
2 Dec 2020
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Synaptic Organization of Anterior Olfactory Nucleus Inputs to Piriform Cortex
Marco J. Russo, Kevin M. Franks, Roxanne Oghaz, Richard Axel, Steven A. Siegelbaum
Journal of Neuroscience 2 December 2020, 40 (49) 9414-9425; DOI: 10.1523/JNEUROSCI.0965-20.2020

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Synaptic Organization of Anterior Olfactory Nucleus Inputs to Piriform Cortex
Marco J. Russo, Kevin M. Franks, Roxanne Oghaz, Richard Axel, Steven A. Siegelbaum
Journal of Neuroscience 2 December 2020, 40 (49) 9414-9425; DOI: 10.1523/JNEUROSCI.0965-20.2020
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Keywords

  • anterior olfactory cortex
  • anterior olfactory nucleus
  • associational synapses
  • intracortical synapses
  • olfactory cortex
  • piriform cortex

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