Learning-Induced Enhancement of Postsynaptic Potentials in Pyramidal Neurons

Abstract

We studied the effect of olfactory learning-induced modifications in piriform (olfactory) cortex pyramidal neurons on the propagation of postsynaptic potentials (PSPs). Rats were trained to distinguish between odors in pairs, in an olfactory discrimination task. Three days after training completion, PSPs were evoked in layer II pyramidal cells in piriform cortex brain slices by electrical stimulation of two pathways. Stimulation of layer Ib activated the intra-cortical fibers that terminate on the proximal region of the apical and basal dendrites. Stimulation of layer Ia activated the afferent axons that originate from the olfactory bulb and terminate on the distal apical dendrites. We have previously shown that olfactory training is accompanied by enhanced synaptic transmission in the intrinsic pathway, but not in the afferent pathway at 3 days after training. Here we show that at this stage, in both pathways PSPs evoked in neurons from trained rats had significantly faster rise time measured at the soma compared with PSPs in neurons from pseudo-trained and naive rats. Activation of the slow afterhyperpolarization (AHP), which is generated by potassium channels probably located at the proximal region of both apical and basal dendrites, reduced the amplitude measured at the soma of the proximal intrinsic pathway PSPs more effectively than PSPs that were generated distally by the afferent fibers. Thus the amount of reduction by AHP was used as a measure for the relative distance of PSP-generating sites from the soma. In neurons from trained rats, despite the previously reported reduction in AHP amplitude, AHP conductance shunted the PSPs from both synaptic pathways more efficiently compared with neurons from the control rats. We suggest that in neurons from trained rats PSPs are electrotonicly closer to the soma.

Olfactory Learning-Induced Long-Lasting Enhancement of Descending and Ascending Synaptic Transmission to the Piriform Cortex

“…Therefore, the ascending synaptic connections are enhanced by exposure to the odors or the training apparatus and not only by learning (although learning still accounts for most of the enhancement observed in trained rats). The second synaptic response, reflecting activity of the association fibers interconnecting the pyramidal neurons, is enhanced only after learning, as shown previously in brain slices (Saar et al, 1999(Saar et al, , 2002Brosh et al, 2007). Only moderate LTP was observed after stimulating this pathway.…”

“…In vivo recordings were performed 3 d after training completion, when most cellular modifications are present (Saar et al, 1999(Saar et al, , 2002Knafo et al, 2001). …”

“…Previous work has shown that OD learning is accompanied by long-lasting postsynaptic modifications in these neurons: the intrinsic excitability of the neurons is enhanced (Saar and Barkai, 2003), the rise time of PSPs evoked by activating the associative fibers interconnecting the pyramidal neurons is reduced (Saar et al, 2002), and the number of synaptic spines is increased (Knafo et al, 2001). These modifications are all present 3 d after learning and could potentially account for strengthening the synaptic connectivity between the orbitofrontal and the piriform cortices.…”

“…OD rule learning is accompanied by a series of profound physiological and morphological modifications in piriform cortex (PC) pyramidal neurons. In particular, intrinsic neuronal excitability is increased (for review, see Saar and Barkai, 2003), synaptic transmission is enhanced (Saar et al, 1999(Saar et al, , 2002, and the number of dendritic spines is increased (Knafo et al, 2001). Such OD learning-related modifications are not confined to a subpopulation of cells but are spread throughout the neuronal ensemble (Saar et al, 1999;Knafo et al, 2001).…”

Molecular Biology Of Early Olfactory Memory: Figure 1.

“…While olfactory memory in adults is associated with changes in the hippocampus (Staubli et al 1986;Alvarez et al 2002), amygdala (Rosenkranz and Grace 2002;Tronel and Sara, 2002), piriform cortex (Roman et al 1987;Litaudon et al 1997;Zinyuk et al 2001;Saar et al 2002), perirhinal cortex (Herzog and Otto 1998), and orbitofrontal cortex (Ramus and Eichenbaum, 2000;Rolls 2001) among elsewhere, many of these structures are not anatomically mature or effectively activated by odors during the first postnatal week in the rat. Early olfactory learning (during the first postnatal week) is dependent on changes that occur within the olfactory bulb itself, and those changes in turn require noradrenergic (NE) input from the locus coeruleus for their acquisition (Sullivan et al 1989;2000), but not expression (Sullivan and Wilson 1991b).…”