A role for the anterior piriform cortex in early odor preference learning: evidence for multiple olfactory learning structures in the rat pup

Abstract

cFos activation in the anterior piriform cortex (aPC) occurs in early odor preference learning in rat pups (Roth and Sullivan 2005). Here we provide evidence that the pairing of odor as a conditioned stimulus and β-adrenergic activation in the aPC as an unconditioned stimulus generates early odor preference learning. β-Adrenergic blockade in the aPC prevents normal preference learning. Enhancement of aPC cAMP response element-binding protein (CREB) phosphorylation in trained hemispheres is consistent with a role for this cascade in early odor preference learning in the aPC. In vitro experiments suggested theta-burst-mediated long-term potentiation (LTP) at the lateral olfactory tract (LOT) to aPC synapse depends on N-methyl-D-aspartate (NMDA) receptors and can be significantly enhanced by β-adrenoceptor activation, which causes increased glutamate release from LOT synapses during LTP induction. NMDA receptors in aPC are also shown to be critical for the acquisition, but not expression, of odor preference learning, as would be predicted if they mediate initial β-adrenoceptor-promoted aPC plasticity. Ex vivo experiments 3 and 24 h after odor preference training reveal an enhanced LOT-aPC field excitatory postsynaptic potential (EPSP). At 3 h both presynaptic and postsynaptic potentiations support EPSP enhancement while at 24 h only postsynaptic potentiation is seen. LOT-LTP in aPC is excluded by odor preference training. Taken together with earlier work on the role of the olfactory bulb in early odor preference learning, these outcomes suggest early odor preference learning is normally supported by and requires multiple plastic changes at least at two levels of olfactory circuitry.

Epac activation initiates associative odor preference memories in the rat pup

“…Epac also enhances intracellular calcium levels and has been shown to recruit calcium calmodulin kinase II (CAMKII), both of which promote neurotransmitter secretion in other systems (Mani et al 2014). In early odor learning an initial, but transient, increase in transmitter release is associated with isoproterenol facilitation of u burst stimulation in piriform cortex (Morrison et al 2013), consistent with possible presynaptic support of STM. Other investigators have speculated that CaMKII has a particular role in STM through autophosphorylation and effects on post-synaptic proteins (Miller and Kennedy 1986;Rich and Schulman 1998;Yang and Schulman 1999;Lisman et al 2002).…”

Arc-Expressing Neuronal Ensembles Supporting Pattern Separation Require Adrenergic Activity in Anterior Piriform Cortex: An Exploration of Neural Constraints on Learning

“…PC itself receives extensive NE input from the LC (Shipley and Ennis, 1996). In rat pups, anterior PC (aPC) odor-NE pairings are sufficient to induce odor preference learning (Morrison et al, 2013). In adult rats, PC LC-NE appears to sharpen odor representations (Bouret and Sara, 2002).…”

A Lateralized Odor Learning Model in Neonatal Rats for Dissecting Neural Circuitry Underpinning Memory Formation

“…The present study employs a well-established early odor preference paradigm wherein an odor, in this case peppermint, is combined with tactile stimulation in order to produce a preference for peppermint 24 hr later 10,11,20 . These odors memories are dependent on intact olfactory circuitry, primarily including the olfactory bulbs (OB) [21][22][23] and the anterior piriform cortex (aPC) 24,25 .…”

“…Olfactory sensory neurons (OSN) in the olfactory epithelium project onto mitral/tufted cells in the OB and these mitral/tufted cells in turn project ipsilaterally to piriform cortex (PC) via the lateral olfactory tract (LOT), among other structures 29 . Both the OSN synapses in the OB 30,31 and the LOT synapses 24,25 in aPC have been identified as critical loci for synaptic changes that support learning and memory. Third, in an early age in rats, olfactory inputs can readily be lateralized.…”