A Major Role for Intracortical Circuits in the Strength and Tuning of Odor-Evoked Excitation in Olfactory Cortex

In primary sensory cortices, there are two main sources of excitation: afferent sensory input relayed from the periphery and recurrent intracortical input. Untangling the functional roles of these two excitatory pathways is fundamental for understanding how cortical neurons process sensory stimuli. Odor representations in the primary olfactory (piriform) cortex depend on excitatory sensory afferents from the olfactory bulb. However, piriform cortex pyramidal cells also receive dense intracortical excitatory connections, and the relative contribution of these two pathways to odor responses is unclear. Using a combination of in vivo whole-cell voltage-clamp recording and selective synaptic silencing, we show that the recruitment of intracortical input, rather than olfactory bulb input, largely determines the strength of odor-evoked excitatory synaptic transmission in rat piriform cortical neurons. Furthermore, we find that intracortical synapses dominate odor-evoked excitatory transmission in broadly tuned neurons, whereas bulbar synapses dominate excitatory synaptic responses in more narrowly tuned neurons.

[1]  Geoffrey Schoenbaum,et al.  Associative encoding in anterior piriform cortex versus orbitofrontal cortex during odor discrimination and reversal learning. , 2006, Cerebral cortex.

[2]  Michael D. Ehlers,et al.  Neural Circuit Mechanisms for Pattern Detection and Feature Combination in Olfactory Cortex , 2011, Neuron.

[3]  Donald A Wilson,et al.  Olfactory perceptual stability and discrimination , 2008, Nature Neuroscience.

[4]  Norimitsu Suzuki,et al.  Two Layers of Synaptic Processing by Principal Neurons in Piriform Cortex , 2011, The Journal of Neuroscience.

[5]  L. C. Katz,et al.  Optical Imaging of Odorant Representations in the Mammalian Olfactory Bulb , 1999, Neuron.

[6]  Dan D. Stettler,et al.  Representations of Odor in the Piriform Cortex , 2009, Neuron.

[7]  J. Isaacson,et al.  Odor Representations in Olfactory Cortex: “Sparse” Coding, Global Inhibition, and Oscillations , 2009, Neuron.

[8]  Guangying K. Wu,et al.  Defining cortical frequency tuning with recurrent excitatory circuitry , 2007, Nature Neuroscience.

[9]  M. Hasselmo,et al.  Selective suppression of intrinsic but not afferent fiber synaptic transmission by baclofen in the piriform (olfactory) cortex , 1994, Brain Research.

[10]  D. Wilson,et al.  Receptive fields in the rat piriform cortex. , 2001, Chemical senses.

[11]  L. Cohen,et al.  Representation of Odorants by Receptor Neuron Input to the Mouse Olfactory Bulb , 2001, Neuron.

[12]  Donald A Wilson,et al.  Spatial and Temporal Distribution of Odorant-Evoked Activity in the Piriform Cortex , 2007, The Journal of Neuroscience.

[13]  Jeffry S. Isaacson,et al.  From Dendrite to Soma: Dynamic Routing of Inhibition by Complementary Interneuron Microcircuits in Olfactory Cortex , 2010, Neuron.

[14]  Brice Bathellier,et al.  Properties of Piriform Cortex Pyramidal Cell Dendrites: Implications for Olfactory Circuit Design , 2009, The Journal of Neuroscience.

[15]  L. Haberly,et al.  New Features of Connectivity in Piriform Cortex Visualized by Intracellular Injection of Pyramidal Cells Suggest that “Primary” Olfactory Cortex Functions Like “Association” Cortex in Other Sensory Systems , 2000, The Journal of Neuroscience.

[16]  T. Cutforth,et al.  Sensory maps in the olfactory cortex defined by long-range viral tracing of single neurons , 2011, Nature.

[17]  N. Bowery.  GABAB receptor pharmacology. , 1993, Annual review of pharmacology and toxicology.

[18]  Markus Meister,et al.  Precision and diversity in an odor map on the olfactory bulb , 2009, Nature Neuroscience.

[19]  Naoshige Uchida,et al.  Odor maps in the mammalian olfactory bulb: domain organization and odorant structural features , 2000, Nature Neuroscience.

[20]  J. Isaacson,et al.  Synapse-Specific Downregulation of NMDA Receptors by Early Experience: A Critical Period for Plasticity of Sensory Input to Olfactory Cortex , 2005, Neuron.

[21]  N. Bowery.  GABAbeta Receptor Pharmacology , 1993 .

[22]  Minmin Luo,et al.  Diverse Patterns of Odor Representation by Neurons in the Anterior Piriform Cortex of Awake Mice , 2010, The Journal of Neuroscience.

[23]  S. R. Datta,et al.  Distinct representations of olfactory information in different cortical centres , 2011, Nature.

[24]  S. Siegelbaum,et al.  Recurrent Circuitry Dynamically Shapes the Activation of Piriform Cortex , 2011, Neuron.

[25]  Massimo Scanziani,et al.  Pyramidal Cells in Piriform Cortex Receive Convergent Input from Distinct Olfactory Bulb Glomeruli , 2010, The Journal of Neuroscience.

[26]  D. Ferster,et al.  Strength and Orientation Tuning of the Thalamic Input to Simple Cells Revealed by Electrically Evoked Cortical Suppression , 1998, Neuron.

[27]  J. Bower,et al.  Facilitating and nonfacilitating synapses on pyramidal cells: a correlation between physiology and morphology. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[28]  L. Haberly,et al.  Odor‐evoked activity is spatially distributed in piriform cortex , 2003, The Journal of comparative neurology.

[29]  L. Haberly,et al.  Association and commissural fiber systems of the olfactory cortex of the rat. I. Systems originating in the piriform cortex and adjacent areas , 1978, The Journal of comparative neurology.

[30]  Ian R. Wickersham,et al.  Cortical representations of olfactory input by trans-synaptic tracing , 2011, Nature.

[31]  J. Isaacson,et al.  An Early Critical Period for Long-Term Plasticity and Structural Modification of Sensory Synapses in Olfactory Cortex , 2007, The Journal of Neuroscience.

[32]  D. Tolhurst,et al.  Characterizing the sparseness of neural codes , 2001, Network.

[33]  D. Tolhurst,et al.  Characterizing the sparseness of neural codes , 2001 .

[34]  Norimitsu Suzuki,et al.  Neural Coding by Two Classes of Principal Cells in the Mouse Piriform Cortex , 2006, The Journal of Neuroscience.

[35]  L. Haberly,et al.  Parallel-distributed processing in olfactory cortex: new insights from morphological and physiological analysis of neuronal circuitry. , 2001, Chemical senses.