Developmental changes in odor-evoked activity in rat piriform cortex

Abstract

In adult rats, odor-evoked Fos protein expression is found in rostrocaudally-oriented bands of cells in anterior piriform cortex (APC), likely indicating functionally distinct subregions, while activated cells in posterior piriform cortex (PPC) lack apparent spatial organization. To determine whether these patterns are present during early postnatal life, and whether they change during development, Fos expression was assessed following acute exposure to single aliphatic acid odors in developing rats beginning at postnatal day 3 (P3). In the olfactory bulb, Fos-immunoreactive cells were present in the granule cell, mitral cell and glomerular layers at the earliest ages examined. Cells immunopositive for Fos were clustered in areas previously reported as active in response to these odors. In piriform cortex, activation in layers II/III shared some features with that seen in the adult; in APC, rostro-caudally oriented bands of Fos-positive cells alternated with bands relatively free of label, while labeled cells were found dispersed throughout PPC. However, in P3-P7 animals, Fospositive cells in APC were found in a central rostrocaudally oriented band that was flanked by two bands relatively free of Fos-positive cells. This contrasted with the adult pattern, a central cell-poor band flanked by cell-rich bands, which was observed beginning at P10. These results suggest that subregions of APC visualized by odor-evoked Fos expression are active and functionally distinct shortly after birth. Changes in activity within these subregions during early postnatal development coincide with a shift toward adult-like olfactory learning behavior in the second postnatal week, and may play a role in this behavioral shift.Olfactory information is processed by several higher-order brain areas, including the anterior (APC) and posterior piriform cortex (PPC). In adult animals, acute presentation of odorants evokes activity in cells that are spatially distributed throughout piriform cortex, as revealed by in situ hybridization and immunolabeling for immediate early genes (Illig and Haberly, 2003;Zou et al., 2005). One feature of odor-evoked activity is that the distribution of activated cells appears to have some order in the APC, where activity is concentrated in prominent rostrocaudally-oriented bands. This banding pattern is mirrored by regional differences in cytoarchitectural features and by connectivity patterns, suggesting the presence of subregions within APC (Luskin and Price, 1983;Haberly, 2001;Ekstrand et al., 2001a;Ekstrand et al., 2001b;Illig and Haberly, 2003;Illig, 2005). In PPC, however, activity appears more broadly distributed, without obvious odor-associated patterns, suggesting differences in the organization and function of APC and PPC.The physiological responses of cells in piriform cortex and the maturation of mitral and tufted cell afferent fibers is incomplete until the second week of life or later (Schwob et al., 1984;

Spatial distribution of neural activity in the anterior olfactory nucleus evoked by odor and electrical stimulation

“…Relatively few studies have examined whether the receptor-based organization seen in the OB is conserved in these regions. Examinations of IEG expression in the rodent piriform cortex indicate that odor exposure leads to widespread rather than patchy postsynaptic cellular activation (Illig and Haberly, 2003; Zou and Buck, 2006; Illig, 2007), and single-unit and whole-cell voltage clamp recordings suggest that cells with similar odor response profiles do not cluster together (Rennaker et al, 2007; Poo and Isaacson, 2009). Live calcium imaging of piriform cortex also indicates that odors activate unique but dispersed ensembles of neurons (Stettler and Axel, 2009).…”

Differential regional expression of brain-derived neurotrophic factor following olfactory fear learning

“…Locally blocking the action of BDNF prevents learning in hippocampal-dependent tasks as shown by infusion of antisense BDNF oligonucleotides (Mizuno et al 2000) and by regional knock-out of BDNF (Heldt et al 2007). In the amygdala, expression of a truncated form of the TrkB receptor, which blocks the activity of the full-length receptor, blocks both the acquisition of a cued fear (Rattiner et al 2004b) and extinction of fear (Chhatwal et al 2006).Although many studies of BDNF in sensory systems have focused on its developmental role, few studies have linked BDNF to learning in the olfactory system, even though the olfactory system at multiple levels shows signs of learning-induced change, including LTP (Ennis et al 1998;Lebel et al 2001), dendritic spine plasticity (Knafo et al 2001), and c-fos activation (Funk and Amir 2000;Schettino and Otto 2001;Illig 2007). In the olfactory system, BDNF is expressed in the olfactory bulb and piriform cortex, and is upregulated in these areas following kainic acid-induced seizures (Katoh-Semba et al 1999).…”

“…Although many studies of BDNF in sensory systems have focused on its developmental role, few studies have linked BDNF to learning in the olfactory system, even though the olfactory system at multiple levels shows signs of learning-induced change, including LTP (Ennis et al 1998;Lebel et al 2001), dendritic spine plasticity (Knafo et al 2001), and c-fos activation (Funk and Amir 2000;Schettino and Otto 2001;Illig 2007). In the olfactory system, BDNF is expressed in the olfactory bulb and piriform cortex, and is upregulated in these areas following kainic acid-induced seizures (Katoh-Semba et al 1999).…”

Novel, continuous visual motion induces c-fos expression in the avian optokinetic nuclei and optic tectum

“…© 2009 IBRO. Published by Elsevier Ltd. All rights reserved.Key words: accessory optic system, metabolic mapping, neural plasticity, immediate-early genes, chicken.The immediate-early gene c-fos is transiently expressed in neurons immediately after a variety of physiological and pharmacological stimuli (Cole et al, 1989;Morgan and Curran, 1991), and its protein product, like that of other well known immediate-early genes such as jun and zif268, functions as a transcription factor, presumably coupling extracellular signals to changes in neuronal function (Morgan and Curran, 1991;Curran and Franza, 1988;Herdegen and Leah, 1998).Immunocytochemical staining with c-fos has been extensively used in mapping functional activity with cellular resolution in a variety of systems (Sagar et al, 1988;Dragunow and Faull, 1989;Montero, 1995;Melzer and Steiner, 1997;Bisler et al, 2002;Illig and Haberly, 2003;Zou et al, 2005;Illig, 2007). Yet, as c-fos expression is linked to neuronal depolarization by a complex signaling cascade (Morgan and Curran, 1986;Sheng et al, 1990;Zhao et al, 2007, see also Gilman et al, 1988 andThompson et al, 1995), the specific circumstances leading to c-fos expression and the consequences of this expression in the normal functioning of neurons remain largely unknown.…”

“…Immunocytochemical staining with c-fos has been extensively used in mapping functional activity with cellular resolution in a variety of systems (Sagar et al, 1988;Dragunow and Faull, 1989;Montero, 1995;Melzer and Steiner, 1997;Bisler et al, 2002;Illig and Haberly, 2003;Zou et al, 2005;Illig, 2007). Yet, as c-fos expression is linked to neuronal depolarization by a complex signaling cascade (Morgan and Curran, 1986;Sheng et al, 1990;Zhao et al, 2007, see also Gilman et al, 1988 andThompson et al, 1995), the specific circumstances leading to c-fos expression and the consequences of this expression in the normal functioning of neurons remain largely unknown.…”