Differential Modifications of Synaptic Weights During Odor Rule Learning: Dynamics of Interaction Between the Piriform Cortex with Lower and Higher Brain Areas

Abstract

Learning of a complex olfactory discrimination (OD) task results in acquisition of rule learning after prolonged training. Previously, we demonstrated enhanced synaptic connectivity between the piriform cortex (PC) and its ascending and descending inputs from the olfactory bulb (OB) and orbitofrontal cortex (OFC) following OD rule learning. Here, using recordings of evoked field postsynaptic potentials in behaving animals, we examined the dynamics by which these synaptic pathways are modified during rule acquisition. We show profound differences in synaptic connectivity modulation between the 2 input sources. During rule acquisition, the ascending synaptic connectivity from the OB to the anterior and posterior PC is simultaneously enhanced. Furthermore, post-training stimulation of the OB enhanced learning rate dramatically. In sharp contrast, the synaptic input in the descending pathway from the OFC was significantly reduced until training completion. Once rule learning was established, the strength of synaptic connectivity in the 2 pathways resumed its pretraining values. We suggest that acquisition of olfactory rule learning requires a transient enhancement of ascending inputs to the PC, synchronized with a parallel decrease in the descending inputs. This combined short-lived modulation enables the PC network to reorganize in a manner that enables it to first acquire and then maintain the rule.

Dynamic cortical lateralization during olfactory discrimination learning

“…Furthermore, olfactory rule learning also induces a transient period of heighten piriform cortical excitability (Saar & Barkai, ), as well as a transient differential modification of ascending and descending inputs to the PCX (Cohen et al . ) that recovers within days of the initial learning. By contrast, the right aPCX showed more stable beta and theta frequency changes after learning.…”

“…; Martin & Ravel, ; Cohen et al . ). Why these effects occur with different temporal dynamics in the two hemispheres during learning, resulting in aPCX asymmetry, remains unclear.…”

Cortical Odor Processing in Health and Disease

“…Thus, as odors acquire or change associative value through experience or training, the OFC may provide top-down feedback on stimulus-predicted outcomes. In fact, recent evidence has demonstrated that as animals learn difficult odor discriminations, there is a concomitant plasticity of OFC–piriform cortex top-down synaptic input, with a depression of left OFC input to left piriform cortex (Cohen et al, 2013). Once the discrimination is well learned, the strength of this connection returns to baseline levels.…”

The Olfactory Mosaic: Bringing an Olfactory Network Together for Odor Perception

“…In addition to this state dependence, the PCX-orbitofrontal cortex connection is also experience-dependent. In fact, Cohen, Wilson, and Barkai (2015) compared changes in synaptic input to the PCX from the olfactory bulb and from the orbitofrontal cortex during odor rule learning. Odor rule (or set) learning occurs when animals are trained on a difficult odor discrimination task.…”

“…Odor rule learning results in a myriad of synaptic and biophysical changes within the PCX (Barkai, 2014; Saar, Reuveni, & Barkai, 2012), but also modifies synaptic connectivity between the PCX and some of its monosynaptic partners. Specifically, during acquisition of odor rule learning the olfactory bulb synaptic input to the PCX was potentiated, and simultaneously the orbitofrontal cortex input to the PCX was depressed [(Cohen, Wilson, et al, 2015); Fig. 1].…”