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

Abstract

Arc ensembles in adult rat olfactory bulb (OB) and anterior piriform cortex (PC) were assessed after discrimination training on highly similar odor pairs. Nonselective ␣-and ␤-adrenergic antagonists or saline were infused in the OB or anterior PC during training. OB adrenergic blockade slowed, but did not prevent, odor discrimination learning. After criterion performance, Arc ensembles in anterior piriform showed enhanced stability for the rewarded odor and pattern separation for the discriminated odors as described previously. Anterior piriform adrenergic blockade prevented acquisition of similar odor discrimination and of OB ensemble changes, even with extended overtraining. Mitral and granule cell Arc ensembles in OB showed enhanced stability for rewarded odor only in the saline group. Pattern separation was not seen in the OB. Similar odor discrimination co-occurs with increased stability in rewarded odor representations and pattern separation to reduce encoding overlap. The difficulty of similar discriminations may relate to the necessity to both strengthen rewarded representations and weaken overlap across similar representations.

Aversive learning-induced plasticity throughout the adult mammalian olfactory system: insights across development

“…The effect of PCx 5-HT during associative learning is completely unexplored; however, optogenetic stimulation of 5-HT inputs decreases spontaneous PCx firing without affecting odor-evoked PCx activity (Lottem et al 2016), which could facilitate cortical olfactory learning and plasticity. Blockade of NE receptors in PCx prevents acquisition of olfactory associative appetitive learning in both pups (Ghosh et al 2015;Morrison et al 2013) and adults (Shakhawat et al 2015) and NE stimulation reverses learning-induced hyperexcitability of PCx pyramidal cells (Brosh et al 2006), indicating a function for NE in olfactory learninginduced PCx plasticity. Data from electrophysiological and computational studies indicate ACh places PCx in a permissive state for both learning and recall in adult associative learning (Barkai et al 1994; Barkai and Hasselmo 1997;Hasselmo et al 1992) by simultaneously suppressing synaptic transmission and enhancing synaptic modification (Linster and Hasselmo 2001) and enhancing long-term potentiation in PCx pyramidal cells (Hasselmo and Barkai 1995;Patil et al 1998).…”

Encoding of Odor Fear Memories in the Mouse Olfactory Cortex

“…Storage of information is made possible by NMDA-dependent, associative plasticity of connections [13][14][15]. Furthermore, changes in piriform network activity [16][17][18] and stabilization of odor representations [19] have been observed after associative olfactory learning. Finally, excitotoxic lesions of the posterior PCx in rats perturb odor fear memories [20], and optogenetic stimulation of artificial piriform ensembles is sufficient to drive learned behaviors [21].…”

Precision of Classification of Odorant Value by the Power of Olfactory Bulb Oscillations Is Altered by Optogenetic Silencing of Local Adrenergic Innervation

“…Local field potential (LFP) oscillations in the olfactory bulb (OB) reflect circuit processing for stimulus detection and sensory decision making for animals learning to differentiate between odorants (Kay, 2014 ; Frederick et al, 2016 ). Local infusion of noradrenergic drugs has shown that noradrenergic modulation plays a role in olfactory bulb/piriform cortex circuit processing for successful odorant discrimination by altering mitral/tufted cell synchronized firing, signal to noise ratio in the output to piriform cortex and pattern separation in piriform cortex (Doucette et al, 2007 , 2011 ; Escanilla et al, 2012 ; de Almeida et al, 2015 ; Shakhawat et al, 2015 ). In addition, studies of circuit dynamics in olfactory bulb slices indicate that adrenergic receptor activation leads to long term enhancement of synchronized oscillations in the olfactory bulb (Pandipati et al, 2010 ), and infusion of the beta noradrenergic blocker propranolol alters the odorant-elicited oscillatory response in the olfactory bulb for the rewarded odorant (Gray et al, 1986 ).…”