Learning‐induced Changes in Rat Piriform Cortex Activity Mapped Using Multisite Recording With Voltage Sensitive Dye

Abstract

The piriform cortex (PCx) has a potential role in storage and recall of olfactory information. This study is a first extensive investigation of the spatiotemporal distribution of activity in the PCx induced by learned sensory inputs following conditioning. In a conditioned group, rats chronically implanted with four electrodes in the olfactory bulb were trained to associate the electrical stimulation of a given bulbar electrode with a positive reinforcement, while stimulation of a different electrode predicted a negative reinforcement. In a familiarized group, rats received the same protocol of daily electrical stimulation with no associated reinforcement. At the end of the conditioning or familiarization episode, activity evoked in the PCx was optically mapped using a 144 photodiode array. In the anaesthetized rats, PCx maps were recorded in response to stimulation of each of the four bulbar electrodes using either high (0.5-1 mA) or low (0.1 mA) test current intensities. Low intensity stimulation revealed that conditioning selectively enhanced the probability of occurrence of a signal composed of a single late (56-73 ms) component which occurred almost simultaneously on a large PCx area. In the conditioned group, high intensity stimulation through either of the four electrodes revealed a potentiation of the early (17-30 ms) disynaptic component of the PCx response in the most posterior part of the PCx as well as a homogeneous increase of the late (39-52 ms) component spread over the PCx areas. These data suggest that learning induces synaptic changes at different nodes of the PCx circuitry.

Ontogeny of odor-LiCl vs. odor-shock learning: Similar behaviors but divergent ages of functional amygdala emergence

“…These data are consistent with the important role of the adult piriform cortex in olfactory conditioning (Litaudon et al 1997;Barkai and Saar 2001;Mouly et al 2001;Mouly and Gervais 2002;Tronel and Sara 2002;Sevelinges et al 2004Sevelinges et al , 2007Wilson et al 2004). However, the specific roles of the anterior and posterior piriform in preference and aversion learning are not consistent with the adult literature, where both have been found important for learning (Hasselmo and Barkai 1995;Litaudon et al 1997;Barkai and Saar 2001;Haberly 2001;Mouly et al 2001;Tronel and Sara 2002;Sevelinges et al 2004;Wilson et al 2004).…”

“…These data are consistent with the important role of the adult piriform cortex in olfactory conditioning (Litaudon et al 1997;Barkai and Saar 2001;Mouly et al 2001;Mouly and Gervais 2002;Tronel and Sara 2002;Sevelinges et al 2004Sevelinges et al , 2007Wilson et al 2004). However, the specific roles of the anterior and posterior piriform in preference and aversion learning are not consistent with the adult literature, where both have been found important for learning (Hasselmo and Barkai 1995;Litaudon et al 1997;Barkai and Saar 2001;Haberly 2001;Mouly et al 2001;Tronel and Sara 2002;Sevelinges et al 2004;Wilson et al 2004). It appears as though the anterior piriform cortex is involved in sensory processes and simple forms of memory like habituation or perceptual learning (Wilson 1997(Wilson , 2000Kadohisa and Wilson 2006), while the posterior piriform cortex expands on this processing and is involved in more complex learning processes and integration of information from other sensory modalities and previous experience (Litaudon et al 1997(Litaudon et al , 2003Chabaud et al 1999Chabaud et al , 2000Haberly 2001;Mouly et al 2001;Sevelinges et al 2004;Gottfried et al 2006;Kadohisa and Wilson 2006;Calu et al 2007).…”

“…In contrast to adult odor-LiCl learning, which relies on the amygdala (Touzani and Sclafani 2005), this early-life, odoraversion learning relies on the olfactory bulb until the pup approaches weaning age, when the amygdala is incorporated into the learning circuitry (Shionoya et al 2006). In contrast, if infant rats receive an odor paired with a moderately painful stimulus (0.5-mA foot or tail shock, or tail pinch) the amygdala appears to be incorporated into this learning circuitry around postnatal day Here we expand assessment of the developing pups' odoraversion learning circuit by including the anterior and posterior piriform cortex, which have previously been demonstrated to be important for both pup and adult odor learning (Litaudon et al 1997;Barkai and Saar 2001;Mouly et al 2001;Mouly and Gervais 2002;Tronel and Sara 2002;Moriceau and Sullivan 2004;Sevelinges et al 2004;Wilson et al 2004;Roth et al 2006). We also extend the assessment of the development of odor-aversion learning by directly comparing a range of odor-aversion learning paradigms and including different intensities of shock.…”

“…Here we expand assessment of the developing pups' odoraversion learning circuit by including the anterior and posterior piriform cortex, which have previously been demonstrated to be important for both pup and adult odor learning (Litaudon et al 1997;Barkai and Saar 2001;Mouly et al 2001;Mouly and Gervais 2002;Tronel and Sara 2002;Moriceau and Sullivan 2004;Sevelinges et al 2004;Wilson et al 2004;Roth et al 2006). We also extend the assessment of the development of odor-aversion learning by directly comparing a range of odor-aversion learning paradigms and including different intensities of shock.…”

“…We used rats ranging from an age of complete dependence on the mother through an age of independence at weaning. We focused on the amygdala basolateral complex, which is implicated in adult fear conditioning and odor-malaise learning (Bermudez-Rattoni et al 1986;LeDoux 2000;Batsell and Blankenship 2002;Gale et al 2004;Holland and Gallagher 2004), and the anterior and posterior piriform cortex, olfactory pathway areas that have previously been implicated in infant odor-aversion and odor-preference learning Roth and Sullivan 2005;Roth et al 2006) as well as adult odor learning (Ferry and Di Scala 1997;Litaudon et al 1997;Barkai and Saar 2001;Mouly et al 2001;Mouly and Gervais 2002;Tronel and Sara 2002;Sevelinges et al 2004;Wilson et al 2004;Touzani and Sclafani 2005).…”