Differences in chemo‐ and cytoarchitectural features within pars principalis of the rat anterior olfactory nucleus suggest functional specialization

The anterior olfactory nucleus (AON) lies between the olfactory bulb and piriform cortex and is the first bilaterally innervated structure in the olfactory system. It is typically divided into two subregions: pars externa and pars principalis. We examined the cytoarchitecture of pars principalis, the largest cellular area of the region, to determine whether it is homogeneously organized. Quantitative Nissl studies indicated that large cells (cell body area >2 standard deviations (SD) larger than the mean cell size) are densest in lateral and dorsolateral regions, while small cells (>1 SD smaller than the mean) are more numerous in medial and ventral areas. Further evidence for regional differences in the organization of the AON were obtained with immunohistochemistry for calbindin (CALB), parvalbumin (PARV), glutamic acid decarboxylase (GAD), and choline transporter (CHT). Cells immunopositive for CALB (CALB+) were denser in the deep portion of Layer II, although homogeneously dispersed throughout the circumference of the AON. PARV+ cells were located in the superficial half of Layer II and were sparse in ventral and medial regions. CHT+ and GAD+ fibers were denser in lateral versus medial regions. No regional differences were found in GAD+ somata, or in norepinephrine transporter or serotonin transporter immunoreactivity. The observed regional differences in cyto‐ and chemoarchitectural features may reflect functional heterogeneity within the AON. J. Comp. Neurol. 498:786–795, 2006. © 2006 Wiley‐Liss, Inc.

[1]  M. Molliver,et al.  Dual Serotonin (5-HT) Projections to the Nucleus Accumbens Core and Shell: Relation of the 5-HT Transporter to Amphetamine-Induced Neurotoxicity , 2000, The Journal of Neuroscience.

[2]  E. G. Jones,et al.  Two classes of cortical GABA neurons defined by differential calcium binding protein immunoreactivities , 2004, Experimental Brain Research.

[3]  M. Barbado,et al.  Changes in Immunoreactivity to Calcium-Binding Proteins in the Anterior Olfactory Nucleus of the Rat after Neonatal Olfactory Deprivation , 2002, Experimental Neurology.

[4]  L. Haberly,et al.  Parallel-distributed processing in olfactory cortex: new insights from morphological and physiological analysis of neuronal circuitry. , 2001, Chemical senses.

[5]  L. Haberly,et al.  Association and commissural fiber systems of the olfactory cortex of the rat II. Systems originating in the olfactory peduncle , 1978, The Journal of comparative neurology.

[6]  A. Lohman.  The anterior olfactory lobe of the guinea pig: a descriptive and experimental anatomical study , 1962 .

[7]  Y. Kubota,et al.  Three distinct subpopulations of GABAergic neurons in rat frontal agranular cortex , 1994, Brain Research.

[8]  S. Hendry,et al.  Co-localization of GABA and neuropeptides in neocortical neurons , 1986, Trends in Neurosciences.

[9]  S. Richardson-Burns,et al.  Protein Kinase C and Intracellular Calcium Are Required for Amphetamine-Mediated Dopamine Release via the Norepinephrine Transporter in Undifferentiated PC 12 Cells , 2001 .

[10]  S. Richardson-Burns,et al.  Protein kinase C and intracellular calcium are required for amphetamine-mediated dopamine release via the norepinephrine transporter in undifferentiated PC12 cells. , 2001, The Journal of pharmacology and experimental therapeutics.

[11]  J. DeFelipe,et al.  Neocortical neuronal diversity: chemical heterogeneity revealed by colocalization studies of classic neurotransmitters, neuropeptides, calcium-binding proteins, and cell surface molecules. , 1993, Cerebral cortex.

[12]  J. DeFelipe,et al.  Microstructure of the neocortex: Comparative aspects , 2002, Journal of neurocytology.

[13]  Fumitaka Kimura,et al.  Cholinergic modulation of cortical function: A hypothetical role in shifting the dynamics in cortical network , 2000, Neuroscience Research.

[14]  Y. Kubota,et al.  Co-localization of two calcium binding proteins in GABA cells of rat piriform cortex , 1993, Brain Research.

[15]  R. Wightman,et al.  Catecholamine release and uptake in the mouse prefrontal cortex , 2001, Journal of neurochemistry.

[16]  T. Kosaka,et al.  An aspect of the organization of the GABAergic system in the rat main olfactory bulb: laminar distribution of immunohistochemically defined subpopulations of GABAergic neurons , 1987, Brain Research.

[17]  Y. Kawaguchi,et al.  Parvalbumin, somatostatin and cholecystokinin as chemical markers for specific GABAergic interneuron types in the rat frontal cortex , 2002, Journal of neurocytology.

[18]  L. Haberly,et al.  A new subdivision of anterior piriform cortex and associated deep nucleus with novel features of interest for olfaction and epilepsy , 2001, The Journal of comparative neurology.

[19]  Seong-Seng Tan,et al.  Constructing the mammalian neocortex: the role of intrinsic factors. , 2003, Developmental biology.

[20]  D. G. Blackburn,et al.  Expression of calbindin-D28K by yolk sac and chorioallantoic membranes of the corn snake, Elaphe guttata. , 2004, Journal of experimental zoology. Part B, Molecular and developmental evolution.

[21]  F. Gage,et al.  Choline Transporter 1 Maintains Cholinergic Function in Choline Acetyltransferase Haploinsufficiency , 2004, The Journal of Neuroscience.

[22]  J. Sandkühler,et al.  Physiological, neurochemical and morphological properties of a subgroup of GABAergic spinal lamina II neurones identified by expression of green fluorescent protein in mice , 2004, The Journal of physiology.

[23]  D. Jacobowitz,et al.  Chemically defined neuron groups and their subpopulations in the glomerular layer of the rat main olfactory bulb , 1995, Neuroscience Research.

[24]  J. DeFelipe,et al.  Catecholaminergic innervation of pyramidal neurons in the human temporal cortex. , 2005, Cerebral cortex.

[25]  A. Levey,et al.  Polarized Expression of the Antidepressant-Sensitive Serotonin Transporter in Epinephrine-Synthesizing Chromaffin Cells of the Rat Adrenal Gland , 1997, Molecular and Cellular Neuroscience.

[26]  E. Braak,et al.  Calbindin-D-28k-like immunoreactive structures in the olfactory bulb and anterior olfactory nucleus of the human adult: Distribution and cell typology—partial complementarity with parvalbumin , 1991, Neuroscience.

[27]  M. Luskin,et al.  The topographic organization of associational fibers of the olfactory system in the rat, including centrifugal fibers to the olfactory bulb , 1983, The Journal of comparative neurology.

[28]  Peter C. Brunjes,et al.  A field guide to the anterior olfactory nucleus (cortex) , 2005, Brain Research Reviews.

[29]  M. Celio,et al.  Parvalbumin in most gamma-aminobutyric acid-containing neurons of the rat cerebral cortex. , 1986, Science.

[30]  D. Simmons,et al.  The Final Stage of Cholinergic Differentiation Occurs Below Inner Hair Cells During Development of the Rodent Cochlea , 2006, Journal of the Association for Research in Otolaryngology.

[31]  E. G. Jones,et al.  Synapses of double bouquet cells in monkey cerebral cortex visualized by calbindin immunoreactivity , 1989, Brain Research.

[32]  E G Jones,et al.  Visualization of chandelier cell axons by parvalbumin immunoreactivity in monkey cerebral cortex. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[33]  T. Waldrop,et al.  Decrease in glutamic acid decarboxylase level in the hypothalamus of spontaneously hypertensive rats , 1998, Journal of hypertension.

[34]  F. Mascagni,et al.  Colocalization of calcium-binding proteins and GABA in neurons of the rat basolateral amygdala , 2001, Neuroscience.

[35]  J. G. Briñón,et al.  Distribution of calbindin D-28K and parvalbumin immunoreactivities in the nucleus olfactorius anterior of the rat , 1992, Brain Research Bulletin.