Intracortical Excitation Rules in Piriform Cortex

The cerebral cortex continuously encodes new sensory information and organizes it within an experiential intracortical framework. The cortical integration of internal and external information forms the associations that are the basis for higher order sensory representation, and ultimately, perception. Deciphering the cellular and synaptic principles of sensory-cortical integration requires a system with a simplified interface between the internal and external worlds. The piriform cortex provides a relatively simple substrate for the study of intracortical modulation of sensory coding. Within piriform, primary sensory information from the olfactory bulb converges onto neurons in a single cortical layer, where it directly integrates with intracortical input. The major barrier to studying intracortical influences on sensory representation in piriform has been the inability to isolate single types of intracortical input. Here, we use optogenetic techniques to functionally isolate two important classes of intracortical input to piriform pyramidal neurons, and slice electrophysiology to assess their synaptic properties. We first expressed channelrhodopsin in a small subset of piriform neurons, effectively isolating the recurrent synapses formed onto piriform pyramidal neurons by their peers. Recurrent collaterals form strong excitatory connections that extend throughout piriform without spatial attenuation in strength, linking distant piriform neurons. This extensive recurrent network is constrained by powerful disynaptic inhibition, which can also reduce activation by primary sensory inputs in a timing-dependent manner. Next, we functionally isolated inputs to the piriform from the anterior olfactory nucleus (AON), an early target of olfactory bulb output whose role in olfaction is largely unknown. The AON makes weaker excitatory connections with piriform, but unlike recurrent connections, these inputs do not drive strong disynaptic inhibition. Sequential activation of AON inputs leads to pronounced summation that boosts piriform activation in an NMDA-receptor-dependent manner, and may enhance plasticity of AON-to-piriform synapses. The AON is a potentially powerful modulator of piriform cortex, whose role in odor information processing merits further study. Our results collectively illustrate critical features of intracortical input classes to piriform cortex, and how these inputs may have distinct roles in shaping odor representations and olfactory learning.