Cholinergic modulation in the olfactory bulb influences spontaneous olfactory discrimination in adult rats

Mandairon, Nathalie; Ferretti, Casara Jean; Stack, Conor; Rubin, Daniel B.; Cleland, Thomas A.; Linster, Christiane

doi:10.1111/j.1460-9568.2006.05212.x

Cited by 149 publications

(218 citation statements)

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“…The major centrifugal inputs to OB glomeruli are cholinergic and serotonergic fibers from the basal forebrain and the raphe (McLean and Shipley, 1987;Gomez et al, 2005). Cholinergic agents applied to the OB alter odor detection thresholds (Mandairon et al, 2006), and serotonin excites juxtaglomerular interneurons, including ET cells, in OB slices (Aungst and Shipley, 2005;Hardy et al, 2005). Such modulation may occur slowly, e.g., during the sleep/wake cycle, or rapidly, e.g., during exploratory behavior.…”

Section: Tonic Presynaptic Inhibition At the Receptor Neuron Terminalmentioning

confidence: 99%

In Vivo Modulation of Sensory Input to the Olfactory Bulb by Tonic and Activity-Dependent Presynaptic Inhibition of Receptor Neurons

Pírez¹,

Wachowiak²

2008

Journal of Neuroscience

115

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The first reorganization of odor representations in the nervous system occurs at the synapse between olfactory receptor neurons and second-order neurons in olfactory bulb glomeruli. Signal transmission at this synapse is modulated presynaptically by several mechanisms, a major one being mediated by GABA B receptors, which suppress presynaptic calcium influx and subsequent transmitter release from the receptor neuron terminal. Here, we imaged stimulus-evoked calcium influx into the receptor neuron terminal in anesthetized mice and used odorant and electrical stimulation combined with in vivo pharmacology to characterize the functional determinants of GABA B -mediated presynaptic inhibition and to test hypotheses on the role of this inhibition in olfactory processing. As expected from previous studies, blocking presynaptic GABA B receptors in vivo increased odorant-evoked presynaptic calcium signals, confirming that GABA B -mediated inhibition modulates the strength of receptor inputs. Surprisingly, we found that the strength of this inhibition was affected little by the nature of the input, being independent of the spatial distribution of activated glomeruli, independent of the sniff frequency used to sample the odorant, and similar for weak and strong odorant-evoked inputs. Instead, we found that tonic inhibition was a major determinant of receptor input strength; this tonic inhibition in turn was dependent on glutamatergic transmission from second-order neurons in the glomerular layer. Thus, rather than adaptively shaping odor representations in an activity-dependent manner, a primary role of presynaptic inhibition in vivo may be to modulate the magnitude of sensory input to the brain as a function of behavioral state.

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Section: Tonic Presynaptic Inhibition At the Receptor Neuron Terminalmentioning

confidence: 99%

In Vivo Modulation of Sensory Input to the Olfactory Bulb by Tonic and Activity-Dependent Presynaptic Inhibition of Receptor Neurons

Pírez¹,

Wachowiak²

2008

Journal of Neuroscience

115

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“…Current experiments show that sensory deprivation decreases the survival of newborn cells in the OB (Mandairon et al 2003(Mandairon et al , 2006c, whereas odor enrichment enhances the survival of newborn cells (Rochefort et al 2002) and modifies the responses of adult-born neurons to odorants (Magavi et al 2005). Similarly, the acquisition of an olfactory-discrimination task also modulates the survival of newborn granule cells in an odor-and task-specific manner (Alonso et al 2006;Mandairon et al 2006b) (Fig. 2B).…”

Section: Introductionmentioning

confidence: 96%

“…The granule cell layer was divided into 36 sectors of 10°with the reference axis drawn on the ventral aspect of the subependymal layer of the OB. The volume of the granule cell layer was represented by an array in which each bin has the value of BrdU-positive cells density in one 10°sector and each column corresponds to one section (for details, see Mandairon et al 2006b). C: manipulation of the bulbar network via daily injections of N-methyl-D-aspartate (NMDA) modulates behavioral perception.…”

Section: Introductionmentioning

confidence: 99%

“…This modulation of inhibition is evidenced by changes in mitral cell responses to odorants (Buonviso and Chaput 2000), activation patterns of inhibitory interneurons in response to odor stimulation (Mandairon et al 2008a), changes in inhibitory neuron survival in the glomerular and granule cell layers (Alonso et al 2006;Mandairon et al 2006b;Mouret et al 2008), and changes in oscillatory dynamics (Beshel et al 2007;Martin et al 2004).…”

Section: Introductionmentioning

confidence: 99%

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Odor Perception and Olfactory Bulb Plasticity in Adult Mammals

Mandairon¹,

Linster²

2009

Journal of Neurophysiology

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110

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Mandairon N, Linster C. Odor perception and olfactory bulb plasticity in adult mammals. J Neurophysiol 101: 2204 -2209, 2009. First published March 4, 2009 doi:10.1152/jn.00076.2009. The adult mammalian olfactory bulb (OB) is unique in that olfactory sensory neurons project directly, without prior thalamic relay, to the OB. This review discusses evidence for the direct involvement of the OB in odor perception and its modulation by olfactory experience. We first discuss recent data showing that the OB exhibits a high level of plasticity in response to olfactory experience including exposure, enrichment, and learning. We next review evidence showing that, in return, experimental manipulation of the OB neural network changes how odorants are processed and perceived. We finally review in more detail a few experiments showing a tight correlation between the modulation of OB neural processing and odor perception. We argue that the OB has evolved to be an adapting network, allowing animals to adjust olfactory computations to changing environments. I N T R O D U C T I O NSensory processing involves a hierarchy of interconnected sensory, cortical, and subcortical areas. When discussing these hierarchies and interactions, olfactory processing is often set apart due to the lack of direct thalamic pathways between sensory and cortical processing areas. Indeed, olfactory signals, after being received and transformed by sensory neurons, are projected directly to an anatomically well studied cortical structure-the olfactory bulb (OB)-with projections to the thalamus established further downstream of the pathway. A recent review has compared the OB to the thalamus in its functional signal processing properties (Kay and Sherman 2007) and discussed how both structures act as early processing stages in which cortical and modulatory feedback can substantially shape sensory representations. Here, we review recent evidence showing that, indeed, the OB is more than a relay station or a feedforward filter but rather actively shapes, and is actively shaped by, olfactory perception-a notion introduced Ͼ20 yr ago by Freeman and Schneider (1982). A crucial component of this function constitutes the central projections to the OB, including cortical, subcortical, and modulatory projections (reviewed in Shipley and Ennis 1996) (Fig. 1). We discuss data showing how olfactory experience changes the OB network and how manipulations of the OB network change odor perception on several timescales. We finally review in more detail a few experiments showing a tight correlation between the modulation of OB neural activity and odor perception. Literature pertaining to neonatal olfactory learning has been intensely and clearly reviewed elsewhere

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“…Blocking olfactory system cholinergic receptors disrupts several aspects of olfactory processing including olfactory shortterm memory (Hunter and Murray 1989;Paolini and McKenzie 1993;Miranda et al 2009), perceptual learning, and discrimination (Ravel et al 1992;Fletcher and Wilson 2002;Linster and Cleland 2002;Mandairon et al 2006). Despite this, relatively little is known about the role of cholinergic activation during acquisition of olfactory aversive learning.…”

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confidence: 99%

Cholinergic modulation during acquisition of olfactory fear conditioning alters learning and stimulus generalization in mice

et al. 2012

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We investigated the role of cholinergic neurotransmission in olfactory fear learning. Mice receiving pairings of odor and foot shock displayed fear to the trained odor the following day. Pretraining injections of the nicotinic antagonist mecamylamine had no effect on subsequent freezing, while the muscarinic antagonist scopolamine significantly reduced freezing. To test whether cholinergic manipulation affected fear generalization, mice were presented with odors similar to the trained odor. Generalization was increased following pretraining scopolamine, while the muscarinic agonist oxotremorine decreased generalization. These results suggest that muscarinic neurotransmission during the acquisition of olfactory association modulates both the strength and specificity of learning.The olfactory system receives cholinergic input from the horizontal limb of the diagonal band of Broca (HDB) (Zaborszky et al. 1986). Blocking olfactory system cholinergic receptors disrupts several aspects of olfactory processing including olfactory shortterm memory (Hunter and Murray 1989;Paolini and McKenzie 1993;Miranda et al. 2009), perceptual learning, and discrimination (Ravel et al. 1992;Fletcher and Wilson 2002;Linster and Cleland 2002;Mandairon et al. 2006). Despite this, relatively little is known about the role of cholinergic activation during acquisition of olfactory aversive learning. While a recent study has demonstrated that cholinergic blockade during acquisition reduces odor-evoked displays of defensive responses to the learned odor (Kroon and Carobrez 2009), the cholinergic contribution to the magnitude and specificity of olfactory fear learning is currently unknown.Sensory cue-evoked fear conditioning has long been used in the study of the neural mechanisms underlying associative memory. In the standard fear-conditioning paradigm, a neutral stimulus is associated with an aversive foot shock, allowing the conditioned stimulus to acquire an aversive valence and induce fear responses, such as freezing (LeDoux 2003). Olfactory cues have been used as an effective conditioned stimulus in promoting fear-conditioned responses (Otto et al. 2000;Jones et al. 2005;Kroon and Carobrez 2009) and studies in other sensory systems have shown that cholinergic neurotransmission is involved in fear learning (Tinsley et al. 2004). For example, in auditory-cued fear conditioning, blockade of muscarinic receptors disrupts the acquisition of the tone-fear conditioning (Young et al. 1995;Anagnostaras et al. 1999;Feiro and Gould 2005), while blocking nicotinic activation does not affect this learning (Feiro and Gould 2005). Despite this, it remains to be seen whether nicotinic and muscarinic receptors can also mediate conditioned freezing responses to olfactory stimuli.In this study, we found that pretraining injections of the nicotinic receptor antagonist (nAChR) mecamylamine had no effect on olfactory fear learning. However, pretraining injections of the muscarinic antagonist scopolamine (mAChR) significantly reduced freezing to the trained od...

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Cholinergic modulation in the olfactory bulb influences spontaneous olfactory discrimination in adult rats

Cited by 149 publications

References 58 publications

In Vivo Modulation of Sensory Input to the Olfactory Bulb by Tonic and Activity-Dependent Presynaptic Inhibition of Receptor Neurons

In Vivo Modulation of Sensory Input to the Olfactory Bulb by Tonic and Activity-Dependent Presynaptic Inhibition of Receptor Neurons

Odor Perception and Olfactory Bulb Plasticity in Adult Mammals

Cholinergic modulation during acquisition of olfactory fear conditioning alters learning and stimulus generalization in mice

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