Neural correlates of olfactory learning: Critical role of centrifugal neuromodulation.

The mammalian olfactory system is well established for its remarkable capability of undergoing experience-dependent plasticity. Although this process involves changes at multiple stages throughout the central olfactory pathway, even the early stages of processing, such as the olfactory bulb and piriform cortex, can display a high degree of plasticity. As in other sensory systems, this plasticity can be controlled by centrifugal inputs from brain regions known to be involved in attention and learning processes. Specifically, both the bulb and cortex receive heavy inputs from cholinergic, noradrenergic, and serotonergic modulatory systems. These neuromodulators are shown to have profound effects on both odor processing and odor memory by acting on both inhibitory local interneurons and output neurons in both regions.

[1]  Anders Hay-Schmidt,et al.  Modulation of anxiety circuits by serotonergic systems , 2005, Stress.

[2]  Donald A. Wilson,et al.  Behavioral/systems/cognitive Coordinate Synaptic Mechanisms Contributing to Olfactory Cortical Adaptation , 2022 .

[3]  M Ennis,et al.  Activation of Locus Coeruleus Enhances the Responses of Olfactory Bulb Mitral Cells to Weak Olfactory Nerve Input , 1996, The Journal of Neuroscience.

[4]  E. Keverne,et al.  Changes in the sensory processing of olfactory signals induced by birth in sheep. , 1992, Science.

[5]  A. Ghatpande,et al.  Store calcium mediates cholinergic effects on mIPSCs in the rat main olfactory bulb. , 2006, Journal of neurophysiology.

[6]  C. Harley,et al.  Beta1-adrenoceptor or alpha1-adrenoceptor activation initiates early odor preference learning in rat pups: support for the mitral cell/cAMP model of odor preference learning. , 2006, Learning & memory.

[7]  E. Barkai,et al.  Olfactory Learning-Induced Long-Lasting Enhancement of Descending and Ascending Synaptic Transmission to the Piriform Cortex , 2008, The Journal of Neuroscience.

[8]  Preserved olfactory short‐term memory after combined cholinergic and serotonergic lesions using 192 IgG‐saporin and 5,7‐ dihydroxytryptamine in rats , 2000, Neuroreport.

[9]  E. Barkai,et al.  Learning-induced enhancement of feedback inhibitory synaptic transmission. , 2009, Learning & memory.

[10]  F. Roman,et al.  Long-term potentiation in rat piriform cortex following discrimination learning , 1993, Brain Research.

[11]  A. Constanti,et al.  Muscarinic receptors mediating suppression of the M‐current in guinea‐pig olfactory cortex neurones may be of the M2‐subtype , 1987, British journal of pharmacology.

[12]  M. Leon,et al.  Enhanced neural response to familiar olfactory cues. , 1984, Science.

[13]  R. Sullivan,et al.  Norepinephrine and learning-induced plasticity in infant rat olfactory system , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  Nathalie Mandairon,et al.  Noradrenergic modulation in the olfactory bulb influences spontaneous and reward‐motivated discrimination, but not the formation of habituation memory , 2008, The European journal of neuroscience.

[15]  M. Hasselmo,et al.  Cholinergic suppression specific to intrinsic not afferent fiber synapses in rat piriform (olfactory) cortex. , 1992, Journal of neurophysiology.

[16]  Chunbo Zhang,et al.  Analysis of training-induced changes in ethyl acetate odor maps using a new computational tool to map the glomerular layer of the olfactory bulb. , 2005, Chemical senses.

[17]  F. Roman,et al.  Learning and memory of odor-reward association: selective impairment following horizontal diagonal band lesions. , 1993, Behavioral neuroscience.

[18]  C. Marsden,et al.  A role for the 5-HT(1A), 5-HT4 and 5-HT6 receptors in learning and memory. , 2008, Trends in pharmacological sciences.

[19]  P. Brennan,et al.  Changes in neurotransmitter release in the main olfactory bulb following an olfactory conditioning procedure in mice , 1998, Neuroscience.

[20]  M. Leon,et al.  Distribution and development of β‐adrenergic receptors in the rat olfactory bulb , 1995, The Journal of comparative neurology.

[21]  J. Bockaert,et al.  Differential modulation of the 5-HT4 receptor agonists and antagonist on rat learning and memory , 2000, Neuropharmacology.

[22]  W. Freeman,et al.  Changes in spatial patterns of rabbit olfactory EEG with conditioning to odors. , 1982, Psychophysiology.

[23]  Adam C. Puche,et al.  Inhibition of Olfactory Receptor Neuron Input to Olfactory Bulb Glomeruli Mediated by Suppression of Presynaptic Calcium Influx , 2005 .

[24]  G. Aghajanian,et al.  Excitatory responses to serotonin (5‐HT) in neurons of the rat piriform cortex: Evidence for mediation by 5‐HT1C receptors in pyramidal cells and 5‐HT2 receptors in interneurons , 1991, Synapse.

[25]  G. Aghajanian,et al.  Alpha 1B-adrenoceptor-mediated excitation of piriform cortical interneurons. , 1996, European journal of pharmacology.

[26]  G. Rondouin,et al.  5-HT4 Receptors Improve Social Olfactory Memory in the Rat , 1997, Neuropharmacology.

[27]  R. Araneda,et al.  Adrenergic Enhancement of Inhibitory Transmission in the Accessory Olfactory Bulb , 2006, Journal of Neuroscience.

[28]  P. Brennan,et al.  Neurotransmitter release in the accessory olfactory bulb during and after the formation of an olfactory memory in mice , 1995, Neuroscience.

[29]  Claire Martin,et al.  Learning Modulation of Odor-Induced Oscillatory Responses in the Rat Olfactory Bulb: A Correlate of Odor Recognition? , 2004, The Journal of Neuroscience.

[30]  B. Wright,et al.  Different patterns of human discrimination learning for two interaural cues to sound-source location , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[31]  Charles A. Marsden,et al.  A role for the 5-HT1A, 5-HT4 and 5-HT6 receptors in learning and memory , 2008 .

[32]  M. Hasselmo Neuromodulation and cortical function: modeling the physiological basis of behavior , 1995, Behavioural Brain Research.

[33]  M. T. Shipley,et al.  Centre–surround inhibition among olfactory bulb glomeruli , 2003, Nature.

[34]  Y. Ishizuka,et al.  Conditioned‐fear stress increases Fos expression in monoaminergic and GABAergic neurons of the locus coeruleus and dorsal raphe nuclei , 2002, Synapse.

[35]  Gilles Laurent,et al.  Odor- and context-dependent modulation of mitral cell activity in behaving rats , 1999, Nature Neuroscience.

[36]  M. Barbado,et al.  Heterogeneous targeting of centrifugal inputs to the glomerular layer of the main olfactory bulb , 2005, Journal of Chemical Neuroanatomy.

[37]  Donald A. Wilson,et al.  Experience Modifies Olfactory Acuity: Acetylcholine-Dependent Learning Decreases Behavioral Generalization between Similar Odorants , 2002, The Journal of Neuroscience.

[38]  J. Monti,et al.  The roles of dopamine and serotonin, and of their receptors, in regulating sleep and waking. , 2008, Progress in brain research.

[39]  M. Pompeiano,et al.  Distribution and cellular localization of mRNA coding for 5-HT1A receptor in the rat brain: correlation with receptor binding , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[40]  R. Doty,et al.  Physostigmine Enhances Performance on an Odor Mixture Discrimination Test , 1998, Physiology & Behavior.

[41]  R. Broadwell Olfactory relationships of the telencephalon and diencephalon in the rabbit. II. An autoradiographic and horseradish peroxidase study of the efferent connections of the anterior olfactory nucleus , 1975, The Journal of comparative neurology.

[42]  S. Moriceau,et al.  Unique Neural Circuitry for Neonatal Olfactory Learning , 2004, The Journal of Neuroscience.

[43]  W. Nickell,et al.  Neurophysiology of magnocellular forebrain inputs to the olfactory bulb in the rat: frequency potentiation of field potentials and inhibition of output neurons , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[44]  Thomas A. Cleland,et al.  Cholinergic modulation of sensory representations in the olfactory bulb , 2002, Neural Networks.

[45]  G. Aston-Jones,et al.  Discharge of noradrenergic locus coeruleus neurons in behaving rats and monkeys suggests a role in vigilance. , 1991, Progress in brain research.

[46]  N. Ravel,et al.  The effect of acetylcholine on rat olfactory bulb unit activity , 1990, Brain Research Bulletin.

[47]  A. Young,et al.  Long-term modifications in the strength of excitatory associative inputs in the piriform cortex. , 2007, Chemical senses.

[48]  M. Ennis,et al.  Direct excitation of mitral cells via activation of alpha1-noradrenergic receptors in rat olfactory bulb slices. , 2001, Journal of neurophysiology.

[49]  M. Hasselmo,et al.  Cholinergic modulation of activity-dependent synaptic plasticity in the piriform cortex and associative memory function in a network biophysical simulation , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[50]  Ben W. Strowbridge,et al.  Blanes Cells Mediate Persistent Feedforward Inhibition onto Granule Cells in the Olfactory Bulb , 2006, Neuron.

[51]  L. Heimer,et al.  The afferent connections of the main and the accessory olfactory bulb formations in the rat: An experimental HRP‐study , 1978, The Journal of comparative neurology.

[52]  Lawrence C Katz,et al.  Noradrenergic Induction of Odor-Specific Neural Habituation and Olfactory Memories , 2008, The Journal of Neuroscience.

[53]  J. Royet,et al.  5-hydroxytryptamine action in the rat olfactory bulb: In vitro electrophysiological patch-clamp recordings of juxtaglomerular and mitral cells , 2005, Neuroscience.

[54]  W. Nickell,et al.  Two anatomically specific classes of candidate cholinoceptive neurons in the rat olfactory bulb , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[55]  L. Heimer,et al.  Double and triple labeling of neurons with fluorescent substances; The study of collateral pathways in the ascending raphe system , 1980, Neuroscience Letters.

[56]  H McLennan,et al.  The pharmacology of inhibition of mitral cells in the olfactory bulb. , 1971, Brain research.

[57]  M. Pompeiano,et al.  Distribution of the serotonin 5-HT2 receptor family mRNAs: comparison between 5-HT2A and 5-HT2C receptors. , 1994, Brain research. Molecular brain research.

[58]  Michael Leon,et al.  Spontaneous versus Reinforced Olfactory Discriminations , 2002, The Journal of Neuroscience.

[59]  Thomas A Cleland,et al.  Cholinergic modulation in the olfactory bulb influences spontaneous olfactory discrimination in adult rats , 2006, The European journal of neuroscience.

[60]  R. Gervais,et al.  Cholinergic modulation of excitability in the rat olfactory bulb: Effect of local application of cholinergic agents on evoked field potentials , 1991, Neuroscience.

[61]  N. Buonviso,et al.  Olfactory experience decreases responsiveness of the olfactory bulb in the adult rat , 1999, Neuroscience.

[62]  V. Murthy,et al.  Serotonergic modulation of odor input to the mammalian olfactory bulb , 2009, Nature Neuroscience.

[63]  M. Hasselmo,et al.  Cholinergic agonist carbachol enables associative long-term potentiation in piriform cortex slices. , 1998, Journal of neurophysiology.

[64]  C. Harley,et al.  Increased beta adrenoceptor activation overcomes conditioned olfactory learning deficits induced by serotonin depletion. , 1997, Brain research. Developmental brain research.

[65]  R Gervais,et al.  Importance of beta-noradrenergic receptors in the olfactory bulb of sheep for recognition of lambs. , 1990, Behavioral neuroscience.

[66]  G. Shepherd,et al.  Analysis of Relations between NMDA Receptors and GABA Release at Olfactory Bulb Reciprocal Synapses , 2000, Neuron.

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

[68]  Brett A. Johnson,et al.  Broad activation of the glomerular layer enhances subsequent olfactory responses. , 2007, Chemical senses.

[69]  L. Hersh,et al.  An atlas of the regional and laminar distribution of choline acetyltransferase immunoreactivity in rat cerebral cortex , 1989, Neuroscience.

[70]  M. Hasselmo,et al.  Noradrenergic suppression of synaptic transmission may influence cortical signal-to-noise ratio. , 1997, Journal of neurophysiology.

[71]  W. T. Nickell,et al.  Chemoanatomical organization of the noradrenergic input from locus coeruleus to the olfactory bulb of the adult rat , 1989, The Journal of comparative neurology.

[72]  D. Restrepo,et al.  Profound Context-Dependent Plasticity of Mitral Cell Responses in Olfactory Bulb , 2008, PLoS biology.

[73]  James H. Fallon,et al.  Locus coeruleus projections to cortex: Topography, morphology and collateralization , 1982, Brain Research Bulletin.

[74]  A. Hunter,et al.  Cholinergic mechanisms in a simple test of olfactory learning in the rat , 2004, Psychopharmacology.

[75]  E. Barkai,et al.  Olfactory learning is associated with increased spine density along apical dendrites of pyramidal neurons in the rat piriform cortex , 2001, The European journal of neuroscience.

[76]  J. Winslow,et al.  Cholinergic modulation of a decrement in social investigation following repeated contacts between mice , 1995, Psychopharmacology.

[77]  Effect of stimulating the nucleus of the horizontal limb of the diagonal band on single unit activity in the olfactory bulb , 1991, Neuroscience.

[78]  M Ennis,et al.  Functional organization of olfactory system. , 1996, Journal of neurobiology.

[79]  C. Harley,et al.  Isoproterenol increases CREB phosphorylation and olfactory nerve-evoked potentials in normal and 5-HT-depleted olfactory bulbs in rat pups only at doses that produce odor preference learning. , 2000, Learning & memory.

[80]  S. Sara,et al.  Locus coeruleus activation modulates firing rate and temporal organization of odour‐induced single‐cell responses in rat piriform cortex , 2002, The European journal of neuroscience.

[81]  J. McKenzie,et al.  Effects of lesions in the horizontal diagonal band nucleus on olfactory habituation in the rat , 1993, Neuroscience.

[82]  G. Lynch,et al.  Evidence for synaptic potentiation in a cortical network during learning , 1987, Brain Research.

[83]  F. Jourdan,et al.  Novelty Determines the Effects of Olfactory Enrichment on Memory and Neurogenesis Through Noradrenergic Mechanisms , 2009, Neuropsychopharmacology.

[84]  A. Pignatelli,et al.  Cholinergic modulation of dopaminergic neurons in the mouse olfactory bulb. , 2008, Chemical senses.

[85]  M. Ennis,et al.  Activation of α1 and α2 noradrenergic receptors exert opposing effects on excitability of main olfactory bulb granule cells , 2010, Neuroscience.

[86]  J. McLean,et al.  5-HT2 receptor involvement in conditioned olfactory learning in the neonate rat pup. , 1996, Behavioral neuroscience.

[87]  C. Harley,et al.  Mitral cell beta1 and 5-HT2A receptor colocalization and cAMP coregulation: a new model of norepinephrine-induced learning in the olfactory bulb. , 2003, Learning & memory.

[88]  M. Luskin,et al.  The distribution of axon collaterals from the olfactory bulb and the nucleus of the horizontal limb of the diagonal band to the olfactory cortex, demonstrated by double retrograde labeling techniques , 1982, The Journal of comparative neurology.

[89]  R. Gervais,et al.  Learning‐induced Changes in Rat Piriform Cortex Activity Mapped Using Multisite Recording With Voltage Sensitive Dye , 1997, The European journal of neuroscience.

[90]  Thomas A Cleland,et al.  Noradrenergic neuromodulation in the olfactory bulb modulates odor habituation and spontaneous discrimination. , 2008, Behavioral neuroscience.

[91]  P. Brennan,et al.  NEURAL MECHANISMS OF MAMMALIAN OLFACTORY LEARNING , 1997, Progress in Neurobiology.

[92]  M. Shipley,et al.  Serotonergic afferents to the rat olfactory bulb: I. Origins and laminar specificity of serotonergic inputs in the adult rat , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[93]  Olfactory recognition memory , 1996, Journal of Physiology-Paris.

[94]  F. Jourdan,et al.  Cholinergic innervation of olfactory glomeruli in the rat: An ultrastructural immunocytochemical study , 1993, The Journal of comparative neurology.

[95]  M. T. Shipley,et al.  Tonic and synaptically evoked presynaptic inhibition of sensory input to the rat olfactory bulb via GABA(B) heteroreceptors. , 2000, Journal of neurophysiology.

[96]  Donald A Wilson,et al.  Olfactory Bulb Mitral-Tufted Cell Plasticity: Odorant-Specific Tuning Reflects Previous Odorant Exposure , 2003, The Journal of Neuroscience.

[97]  R. Nicoll,et al.  An intracellular analysis of dendrodendritic inhibition in the turtle in vitro olfactory bulb , 1982, The Journal of physiology.

[98]  David H Gire,et al.  Long-term enhancement of synchronized oscillations by adrenergic receptor activation in the olfactory bulb. , 2008, Journal of neurophysiology.

[99]  Norman M. Weinberger,et al.  Learning-Induced Physiological Memory in Adult Primary Auditory Cortex: Receptive Field Plasticity, Model, and Mechanisms , 1998, Audiology and Neurotology.

[100]  J. Fallon,et al.  Catecholamine innervation of the basal forebrain III. Olfactory bulb, anterior olfactory nuclei, olfactory tubercle and piriform cortex , 1978, The Journal of comparative neurology.

[101]  M. Hasselmo,et al.  Electrical stimulation of the horizontal limb of the diagonal band of broca modulates population EPSPs in piriform cortex. , 1999, Journal of neurophysiology.

[102]  D. Restrepo,et al.  Adrenergic modulation of olfactory bulb circuitry affects odor discrimination. , 2007, Learning & memory.

[103]  M. T. Shipley,et al.  the connections of the mouse olfactory bulb: A study using orthograde and retrograde transport of wheat germ agglutinin conjugated to horseradish peroxidase , 1984, Brain Research Bulletin.

[104]  F. Bloom,et al.  ANALYSIS OF INDIVIDUAL RABBIT OLFACTORY BULB NEURON RESPONSES TO THE MICROELECTROPHORESIS OF ACETYLCHOLINE, NOREPINEPHRINE AND SEROTONIN SYNERGISTS AND ANTAGONISTS. , 1964, The Journal of pharmacology and experimental therapeutics.

[105]  F. Bloom,et al.  ADRENERGIC MECHANISMS IN RABBIT OLFACTORY BULB. , 1964, The American journal of physiology.

[106]  J. Isaacson,et al.  Intraglomerular inhibition: signaling mechanisms of an olfactory microcircuit , 2005, Nature Neuroscience.

[107]  Christiane Linster,et al.  Noradrenergic modulation of behavioral odor detection and discrimination thresholds in the olfactory bulb , 2010, The European journal of neuroscience.

[108]  Diagonal band stimulation increases piriform cortex neuronal excitability in vivo. , 1999, Neuroreport.

[109]  D. Wilson,et al.  Neurobiology of associative learning in the neonate: early olfactory learning. , 1994, Behavioral and neural biology.

[110]  S. Sara The locus coeruleus and noradrenergic modulation of cognition , 2009, Nature Reviews Neuroscience.

[111]  Michael Leon,et al.  A learned odor evokes an enhanced Fos-like glomerular response in the olfactory bulb of young rats , 1995, Brain Research.

[112]  C. Harley,et al.  Optical imaging of odor preference memory in the rat olfactory bulb. , 2002, Journal of neurophysiology.

[113]  M. Hasselmo,et al.  Neuromodulation and the functional dynamics of piriform cortex. , 2001, Chemical senses.

[114]  R. Sullivan,et al.  Serotonergic influence on olfactory learning in the neonate rat. , 1993, Behavioral and neural biology.

[115]  N. Schoppa,et al.  Adrenergic receptor-mediated disinhibition of mitral cells triggers long-term enhancement of synchronized oscillations in the olfactory bulb. , 2010, Journal of neurophysiology.

[116]  R. Dantzer,et al.  Specific modulation of social memory in rats by cholinomimetic and nootropic drugs, by benzodiazepine inverse agonists, but not by psychostimulants , 1989, Psychopharmacology.

[117]  L. Haberly,et al.  NMDA-dependent induction of long-term potentiation in afferent and association fiber systems of piriform cortex in vitro , 1990, Brain Research.

[118]  M Ennis,et al.  Glutamate and Synaptic Plasticity at Mammalian Primary Olfactory Synapses a , 1998, Annals of the New York Academy of Sciences.

[119]  M. Hasselmo,et al.  Muscarinic cholinergic neuromodulation reduces proactive interference between stored odor memories during associative learning in rats. , 2000, Behavioral neuroscience.

[120]  Vikrant Kapoor,et al.  Activity-dependent gating of lateral inhibition in the mouse olfactory bulb , 2008, Nature Neuroscience.

[121]  L. Butcher,et al.  Cholinergic systems in the rat brain: I. Projections to the limbic telencephalon , 1984, Brain Research Bulletin.

[122]  S. Nakanishi,et al.  Refinement of odor molecule tuning by dendrodendritic synaptic inhibition in the olfactory bulb. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[123]  Yoram Grossman,et al.  Learning-induced enhancement of postsynaptic potentials in pyramidal neurons. , 2002, Journal of neurophysiology.

[124]  N. Ravel,et al.  A study of the effects of noradrenaline in the rat olfactory bulb using evoked field potential response , 1995, Brain Research.

[125]  Christiane Linster,et al.  Bulbar Acetylcholine Enhances Neural and Perceptual Odor Discrimination , 2009, The Journal of Neuroscience.

[126]  N. Ravel,et al.  Scopolamine impairs the ability of parturient ewes to learn to recognise their lambs , 1997, Psychopharmacology.

[127]  T. Ho¨kfelt,et al.  Transmitter histochemistry of the rat olfactory bulb. II. fluorescence histochemical, autoradiographic and electron microscopic localization of monoamines , 1978, Brain Research.

[128]  L. Cohen,et al.  Interglomerular center-surround inhibition shapes odorant-evoked input to the mouse olfactory bulb in vivo. , 2006, Journal of neurophysiology.

[129]  Michael Leon,et al.  Exposure to a broad range of odorants decreases cell mortality in the olfactory bulb , 2006, Neuroreport.

[130]  H. Mutoh,et al.  Long-Term Depression at Olfactory Nerve Synapses , 2005, The Journal of Neuroscience.

[131]  Hong-Wei Dong,et al.  Noradrenergic regulation of GABAergic inhibition of main olfactory bulb mitral cells varies as a function of concentration and receptor subtype. , 2009, Journal of neurophysiology.

[132]  D A Wilson,et al.  Spatial patterns of olfactory bulb single-unit responses to learned olfactory cues in young rats. , 1988, Journal of neurophysiology.

[133]  M. Cattarelli,et al.  Catecholamine innervation of the piriform cortex: a tracing and immunohistochemical study in the rat , 1996, Brain Research.

[134]  M. T. Shipley,et al.  Surprisingly rich projection from locus coeruleus to the olfactory bulb in the rat , 1985, Brain Research.

[135]  M. Hasselmo,et al.  Selective loss of cholinergic neurons projecting to the olfactory system increases perceptual generalization between similar, but not dissimilar, odorants. , 2001, Behavioral neuroscience.

[136]  S. Amir,et al.  Enhanced Fos expression within the primary olfactory and limbic pathways induced by an aversive conditioned odor stimulus , 2000, Neuroscience.

[137]  O. Bertrand,et al.  Olfactory learning modifies the expression of odour‐induced oscillatory responses in the gamma (60–90 Hz) and beta (15–40 Hz) bands in the rat olfactory bulb , 2003, The European journal of neuroscience.

[138]  M. Hasselmo Neuromodulation: acetylcholine and memory consolidation , 1999, Trends in Cognitive Sciences.

[139]  T. Ichikawa,et al.  Organization of choline acetyltransferase-containing structures in the forebrain of the rat , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[140]  L. Haberly,et al.  Deep neurons in piriform cortex. II. Membrane properties that underlie unusual synaptic responses. , 1989, Journal of neurophysiology.

[141]  M. Hasselmo,et al.  Modulation of the input/output function of rat piriform cortex pyramidal cells. , 1994, Journal of neurophysiology.

[142]  C. Shute,et al.  The ascending cholinergic reticular system: neocortical, olfactory and subcortical projections. , 1967, Brain : a journal of neurology.

[143]  T. Hökfelt,et al.  Distribution of alpha 1 adrenoceptors in rat brain revealed by in situ hybridization experiments utilizing subtype-specific probes , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[144]  G. Lynch,et al.  Long-term potentiation of monosynaptic EPSPs in rat piriform cortex in vitro. , 1990, Synapse.

[145]  E. Barkai,et al.  Long-Lasting Cholinergic Modulation Underlies Rule Learning in Rats , 2001, The Journal of Neuroscience.

[146]  G. Aghajanian,et al.  Serotonin (5-HT) induces IPSPs in pyramidal layer cells of rat piriform cortex: evidence for the involvement of a 5-HT2 -activated interneuron , 1990, Brain Research.

[147]  Anne Didier,et al.  Odor enrichment increases interneurons responsiveness in spatially defined regions of the olfactory bulb correlated with perception , 2008, Neurobiology of Learning and Memory.

[148]  Association of an odor with activation of olfactory bulb noradrenergic beta-receptors or locus coeruleus stimulation is sufficient to produce learned approach responses to that odor in neonatal rats. , 2000, Behavioral neuroscience.

[149]  C. Berridge,et al.  The locus coeruleus–noradrenergic system: modulation of behavioral state and state-dependent cognitive processes , 2003, Brain Research Reviews.

[150]  D. K. Patneau,et al.  Selective long-term potentiation in the pyriform cortex , 1988, Brain Research.

[151]  Christelle Rochefort,et al.  Enriched Odor Exposure Increases the Number of Newborn Neurons in the Adult Olfactory Bulb and Improves Odor Memory , 2002, The Journal of Neuroscience.

[152]  M. T. Shipley,et al.  Dopamine D2 receptor-mediated presynaptic inhibition of olfactory nerve terminals. , 2001, Journal of neurophysiology.

[153]  A. Carobrez,et al.  Olfactory fear conditioning paradigm in rats: Effects of midazolam, propranolol or scopolamine , 2009, Neurobiology of Learning and Memory.

[154]  Tsuyoshi Inoue,et al.  Muscarinic Receptor Activation Modulates Granule Cell Excitability and Potentiates Inhibition onto Mitral Cells in the Rat Olfactory Bulb , 2007, The Journal of Neuroscience.

[155]  G. Aghajanian,et al.  Pyramidal cells in piriform cortex receive a convergence of inputs from monoamine activated GABAergic interneurons , 1993, Brain Research.

[156]  M. Hasselmo,et al.  Neural activity in the horizontal limb of the diagonal band of Broca can be modulated by electrical stimulation of the olfactory bulb and cortex in rats , 2000, Neuroscience Letters.

[157]  K. Carson Localization of acetylcholinesterase-positive neurons projecting to the mouse main olfactory bulb , 1984, Brain Research Bulletin.

[158]  J. Isaacson,et al.  Olfactory Reciprocal Synapses: Dendritic Signaling in the CNS , 1998, Neuron.

[159]  G M Shepherd,et al.  Noradrenergic inhibition of synaptic transmission between mitral and granule cells in mammalian olfactory bulb cultures , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[160]  A. Blokland Acetylcholine: a neurotransmitter for learning and memory? , 1995, Brain Research Reviews.

[161]  Short‐lasting exposure to one odour decreases general reactivity in the olfactory bulb of adult rats , 1998, The European journal of neuroscience.

[162]  M. Leon,et al.  Early odor preference training increases olfactory bulb norepinephrine. , 1995, Brain research. Developmental brain research.

[163]  R Gervais,et al.  Scopolamine injection into the olfactory bulb impairs short-term olfactory memory in rats. , 1994, Behavioral neuroscience.

[164]  J. R. Wolff,et al.  Synaptic and non-synaptic cholinergic innervation of the various types of neurons in the main olfactory bulb of adult rat: Immunocytochemistry of choline acetyltransferase , 1995, Neuroscience.

[165]  S. Sara,et al.  Locus coeruleus-evoked responses in behaving rats: A clue to the role of noradrenaline in memory , 1994, Brain Research Bulletin.

[166]  F. Macrides,et al.  Cholinergic and catecholaminergic afferents to the olfactory bulb in the Hamster: A neuroanatomical, biochemical, and histochemical investigation , 1981, The Journal of comparative neurology.

[167]  C. Harley,et al.  Early Odor Preference Learning in the Rat: Bidirectional Effects of cAMP Response Element-Binding Protein (CREB) and Mutant CREB Support a Causal Role for Phosphorylated CREB , 2003, The Journal of Neuroscience.

[168]  P. Luppi,et al.  Serotonergic and non-serotonergic projections from the raphe nuclei to the piriform cortex in the rat: a cholera toxin B subunit (CTb) and 5-HT immunohistochemical study , 1995, Brain Research.

[169]  L. Heimer,et al.  Cholinergic and GABAergic afferents to the olfactory bulb in the rat with special emphasis on the projection neurons in the nucleus of the horizontal limb of the diagonal band , 1986, The Journal of comparative neurology.

[170]  N. Buonviso,et al.  Altered odor-induced expression of c-fos and arg 3.1 immediate early genes in the olfactory system after familiarization with an odor. , 2002, Journal of neurobiology.

[171]  M. T. Shipley,et al.  Norepinephrine increases rat mitral cell excitatory responses to weak olfactory nerve input via alpha-1 receptors in vitro , 1999, Neuroscience.

[172]  T. Moriizumi,et al.  Olfactory disturbance induced by deafferentation of serotonergic fibers in the olfactory bulb , 1994, Neuroscience.

[173]  M. Hasselmo,et al.  Contribution of the cholinergic basal forebrain to proactive interference from stored odor memories during associative learning in rats. , 2001, Behavioral neuroscience.

[174]  Gordon M. Shepherd,et al.  The Olfactory Bulb , 1988 .

[175]  M. Leon,et al.  A learned odor decreases the number of Fos-immunopositive granule cells in the olfactory bulb of young rats , 1996, Brain Research.

[176]  G. Lynch,et al.  Long‐term potentiation of monosynaptic EPSPS in rat piroform cortex in vitro , 1990, Synapse.

[177]  M. Miranda,et al.  Differential involvement of cholinergic and beta-adrenergic systems during acquisition, consolidation, and retrieval of long-term memory of social and neutral odors , 2009, Behavioural Brain Research.

[178]  G. Collins,et al.  Excitatory and inhibitory effects of dopamine on synaptic transmission in the rat olfactory cortex slice , 1985, Brain Research.

[179]  R. Sullivan,et al.  Blockade of mitral/tufted cell habituation to odors by association with reward: a preliminary note , 1992, Brain Research.

[180]  D. Wilson,et al.  Noradrenergic modulation of olfactory bulb excitability in the postnatal rat. , 1988, Brain research.

[181]  D. Wilson,et al.  The role of olfactory bulb norepinephrine in early olfactory learning. , 1992, Brain research. Developmental brain research.

[182]  N. Kopell,et al.  Olfactory Bulb Gamma Oscillations Are Enhanced with Task Demands , 2007, The Journal of Neuroscience.

[183]  W. Singer,et al.  Modulation of visual cortical plasticity by acetylcholine and noradrenaline , 1986, Nature.

[184]  W. Precht The synaptic organization of the brain G.M. Shepherd, Oxford University Press (1975). 364 pp., £3.80 (paperback) , 1976, Neuroscience.

[185]  D. Wilson,et al.  Scopolamine enhances generalization between odor representations in rat olfactory cortex. , 2001, Learning & memory.

[186]  A. Carleton,et al.  Multiple and Opposing Roles of Cholinergic Transmission in the Main Olfactory Bulb , 1999, The Journal of Neuroscience.

[187]  K. Shionoya,et al.  Auditory Stimulation Dishabituates Olfactory Responses via Noradrenergic Cortical Modulation , 2009, Neural plasticity.

[188]  N. Ravel,et al.  Scopolamine impairs delayed matching in an olfactory task in rats , 2005, Psychopharmacology.