Abstract
How sensory information is processed within olfactory cortices is unclear. Here, we examined long-range circuit wiring between different olfactory cortical regions of acute mouse brain slices using a channelrhodopsin-2 (ChR2)-based neuronal targeting approach. Our results provide detailed information regarding the synaptic properties of the reciprocal long-range monosynaptic glutamatergic projections (LRMGP) between and within anterior piriform cortex (aPC), posterior piriform cortex (pPC), and lateral entorhinal cortex (LEC), thereby creating a long-range inter- and intracortical circuit diagrams at the level of synapses and single cortical neurons. Our results reveal the following information regarding hierarchical intra- and intercortical organizations: (i) there is massive bottom-up (i.e., rostral–caudal) excitation within the LRMGP accompanied with strong feedforward (FF) inhibition; (ii) there are convergent FF connections onto LEC from both aPC and pPC; (iii) feedback (FB) intercortical connections are weak with a significant fraction of presumptive silent synapses; and (iv) intra and intercortical long-range connections lack layer specificity and their innervation of interneurons are stronger than neighboring pyramidal neurons. The elucidation of the distinct hierarchical organization of long-range olfactory cortical circuits paves the way for further understanding of higher order cortical processing within the olfactory system.
Highlights
Olfactory cortex has been defined as those cortical regions receiving direct monosynaptic input from olfactory bulbs
The results from recorded PYRs showed that intracortical anterior piriform cortex (aPC) neurons received stronger intracortical long-range monosynaptic glutamatergic projections (LRMGP), while both posterior piriform cortex (pPC) and lateral entorhinal cortex (LEC) monosynaptic AMPA and NMDA synaptic strength were weaker compared to aPC ? aPC inputs (Fig. 3B–C, a)
There were no significant differences for both AMPA and NMDA currents between aPC ? pPC and aPC ? LEC synapses (Fig. 3B–C, a), indicating comparable associational monosynaptic fiber systems from aPC to both pPC and LEC
Summary
Olfactory cortex has been defined as those cortical regions receiving direct monosynaptic input from olfactory bulbs. In vivo and in vitro studies of the rodent olfactory system have begun to uncover the role of intracortical recurrent circuits within the PC (Zhan and Luo 2010; Franks et al 2011; Luo 2011; Poo and Isaacson 2011) Another subdivision of olfactory cortex – LEC, immediately caudal to pPC in rodents – is suggested to serve as a higher order olfactory center via strong reciprocal connections with memory and emotion processing structures such as amygdala and hippocampus (Haberly and Price 1978; Agster and Burwell 2009; Xu and Wilson 2012; Chapuis et al 2013). Multiple studies have defined the anatomical connections between aPC, pPC, and LEC (Luskin and Price 1983a,b; Burwell and Amaral 1998; Kerr et al 2007; Agster and Burwell 2009), quantitative information at synaptic levels remains elusive
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