Norepinephrine increases rat mitral cell excitatory responses to weak olfactory nerve input via alpha-1 receptors in vitro

Ciombor, Kelly J.; Ennis, Matthew; Shipley, Michael T.

doi:10.1016/s0306-4522(98)00437-0

Cited by 73 publications

(65 citation statements)

References 54 publications

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“…Although this result would be unexpected in the context of neonatal early learning preference, it supports studies indicating that the ␤ antagonist propanolol does not affect odor detection in adult rabbits (Gray et al 1986). Experiments in MOB slices, neuronal cultures, and anesthetized animals found ␣ adrenergic modulation of neuronal excitability and synaptic function in the MOB (Trombley 1994;Mouly et al 1995;Ciombor et al 1999;Hayar et al 2001). In our experiments, the learning curve for mice injected with the general ␣ adrenergic receptor antagonist phentolamine (28 nmol per bulb) did not differ from the saline control (NIV values did not differ significantly P = 0.999, Fig.…”

Section: Resultsmentioning

confidence: 97%

Adrenergic modulation of olfactory bulb circuitry affects odor discrimination

Doucette¹,

Milder²,

Restrepo³

2007

Learn. Mem.

132

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A rodent's survival depends upon its ability to perceive odor cues necessary to guide mate selection, sexual behavior, foraging, territorial formation, and predator avoidance. Arguably, the need to discriminate odor cues in a complex olfactory environment requires a highly adaptable olfactory system. Indeed, it has been proposed that context-dependent modulation of the initial sensory relay could alter olfactory perception. Interestingly, 40% of the adrenergic innervation from the locus coeruleus, fibers that are activated by contextual cues, innervates the first relay station in the olfactory system (the main olfactory bulb). Here we utilize restricted pharmacological inhibition of olfactory bulb noradrenergic receptors in awake-behaving animals. We show that combined blockade of ␣ and ␤ adrenergic receptors does not impair two-odor discrimination behavior per se but does impair the ability to discriminate perceptually similar odors. Thus, contextual cues conveyed by noradrenergic fibers alter processing before the second synapse in the olfactory cortex, resulting in tuning of the ability to discriminate between similar odors.Particularly intriguing, but poorly understood, is the potential role of adrenergic modulation of the main olfactory bulb (MOB) in adults. The MOB receives strong innervation from the locus coeruleus (LC)-noradrenaline (NA) system, and in rodents ∼40% of LC fibers target the MOB. The fibers are known to be densest in the internal plexiform and granule cell layers, less dense in the external plexiform layer, and sparse in the glomerular layer (McLean et al. 1989) (Fig. 1). Both ␣ and ␤ adrenergic receptors are expressed by cells in the MOB (Pieribone et al. 1994;Woo and Leon 1995;Day et al. 1997). Current evidence suggests that the LC-NA system has a behaviorally meaningful role within the MOB of adult animals engaged in olfactory learning tasks. There is a modest but reproducible release of NA in the MOB during operant conditioning in adult mice (Brennan et al. 1998). In addition, detection of the rewarded odor, presumably relayed from the prefrontal cortex to LC, triggers a brief phasic increase in firing of LC neurons (Bouret and Sara 2004). Gray and coworkers also find that the topical application of propranolol, a ␤ adrenergic antagonist, to the MOB abolished changes in ␥ frequency (40-100 Hz) oscillations in the local field potential elicited by the rewarded odor in an odor discrimination task (Gray et al. 1986). The modulation of odor-induced local field potential oscillations has been postulated to play a role in olfactory learning (Martin et al. 2006). Surprisingly, although the adrenergic effect on odor-induced changes in local field potential oscillations found by Gray and coworkers was robust, propranolol did not change the ability of rabbits to discriminate between odors. Data presented in this paper provide an explanation for the paradoxical observation of Gray and coworkers, as we show that blockade of both ␣ and ␤ adrenergic receptors in the MOB is necessary to attain a chan...

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Section: Resultsmentioning

confidence: 97%

Adrenergic modulation of olfactory bulb circuitry affects odor discrimination

Doucette¹,

Milder²,

Restrepo³

2007

Learn. Mem.

132

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“…Several studies have indicated that the overall effect of noradrenergic modulation in the MOB is excitatory (Jahr and Nicoll, 1982;Trombley and Shepherd, 1992;Mouly et al, 1995;Ciombor et al, 1999;Hayar et al, 2001) (but see McLennan, 1971;Perez et al, 1987;Mouly et al, 1995). These effects include direct depolarization of M/TCs and a decrease in the inhibitory activity at dendrodendritic synapses.…”

Section: Resultsmentioning

confidence: 99%

“…The holding potential was Ϫ60 mV. tle olfactory bulb (Jahr and Nicoll, 1982), direct excitatory action on M/TCs by activation of ␣1 adrenergic receptors in rat (Hayar et al, 2001), decreased inhibitory transmission in cultured olfactory bulb cells by ␣2 adrenergic receptors (Trombley and Shepherd, 1992), and excitation of M/TCs by stimulation in the locus ceruleus or iotophoretic application of NA in the MOB (Ciombor et al, 1999). In addition, a few studies in the AOB have suggested that NA could have a similar action as in the MOB (Brennan et al, 1995).…”

Section: Discussionmentioning

confidence: 99%

“…In the MOB, cholinergic activity produces direct depolarization of M/TCs through nicotinic receptor activation, and muscarinic receptor activity on granule cells increases GABA inhibitory transmission (Castillo et al, 1999). Similarly, noradrenergic activation produces inhibition and excitation of M/TCs in the MOB (Mouly et al, 1995;Okutani et al, 1998;Ciombor et al, 1999;Hayar et al, 2001). However, although the cholinergic effects in the AOB are similar to those observed in the MOB (R. C. Araneda, unpublished results), in the AOB the overall effect of NA was mainly inhibitory, suggesting that the mechanisms by which the noradrenergic system participates in memory formation in the AOB may be different than in the MOB.…”

Section: Discussionmentioning

confidence: 99%

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Adrenergic Enhancement of Inhibitory Transmission in the Accessory Olfactory Bulb

Araneda¹,

Firestein²

2006

J. Neurosci.

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Noradrenergic modulation of dendrodendritic synapses between the mitral and granule cells in the accessory olfactory bulb (AOB) is postulated to play a key role in the formation of memory in olfactory-mediated behaviors. Current models propose that noradrenaline (NA) increases excitation of mitral/tufted cells (M/TCs) by decreasing the release of GABA from granule cells. However, surprisingly little is known about the actions of NA at the cellular level in the AOB. Here, in recordings from AOB slices, we show that NA decreases the firing frequency of M/TCs in response to stimulation. This effect is attributable to an increase in the GABA inhibitory input to M/TCs. Application of NA (10 M) produced an ϳ20-fold increase in the frequency of GABA-induced miniature IPSCs (mIPSCs) without changing their amplitude. A pharmacological analysis indicated that the increase in mIPSCs frequency results from activation of ␣1 adrenergic receptors. In addition to increasing the mIPSC frequency, NA also potentiated GABA inhibitory currents induced by direct stimulation of granule cells. Together, our results suggest that NA increases the release of GABA from granule cells by acting on presynaptic receptors. Thus, the role of the noradrenergic activity in the AOB may be opposite than suggested previously: we find that the overall effect of NA in the AOB is inhibition of M/TCs.

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“…Therefore, the increased lateral SAPs could be caused by the accumulation of these products over time. Alternatively, the increased lateral and͞or decreased dorsal activations may be attributed to varied accessibility of odor molecules to receptor neurons in different locations within the nasal cavity (23), inhibition of the activated glomerulus to its surrounding glomeruli (24), and͞or central feedback into the OB from higher brain regions (25).…”

Section: Modification Of Saps With Prolonged Exposurementioning

confidence: 99%

Assessment and discrimination of odor stimuli in rat olfactory bulb by dynamic functional MRI

Kida²,

Hyder³

et al. 2000

Proc. Natl. Acad. Sci. U.S.A.

114

118

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Dynamic blood oxygenation level-dependent functional MRI was applied at 7 T in the rat olfactory bulb (OB) with pulsed delivery of iso-amyl acetate (IAA) and limonene. Acquisition times for singleslice and whole OB data were 8 and 32 s, respectively, with spatial resolution of 220 ؋ 220 ؋ 250 m. On an intrasubject basis, short IAA exposures of 0.6 min separated by 3.5-min intervals induced reproducible spatial activity patterns (SAPs) in the olfactory nerve layer, glomerular layer, and external plexiform layer. During long exposures (Ϸ10 min), the initially dominant dorsal SAPs declined in intensity and area, whereas in some OB regions, the initially weak ventral͞lateral SAPs increased first and then decreased. The SAPs of different concentrations were topologically similar, which implies that whereas an odor at various concentrations activates the same subsets of receptor cells, different concentrations are assessed and discriminated by variable magnitudes of laminarspecific activations. IAA and limonene reproducibly activated different subsets of receptor cells with some overlaps. Whereas qualitative topographical agreement was observed with results from other methods, the current dynamic blood oxygenation level-dependent functional MRI results can provide quantitative SAPs of the entire OB.blood oxygenation level-dependent ͉ functional mapping ͉ olfactory bulb I n mammals, olfactory behaviors such as determination of food palatability and searching require accurate assessment and discrimination of different odor types, concentrations, and exposure duration (1). Distinctions between these behavioral tasks are believed to rely on a spatial-encoding mechanism in which different odor and concentrations evoke spatial activity patterns (SAPs) in the olfactory bulb (OB). The SAPs are derived from functionally induced activity in olfactory receptor neurons that synapse at specific glomeruli (2).Insights into the coding of olfactory information have been partially inferred from SAPs in the OB, where the data can be obtained by various methods: 2-deoxyglucose autoradiography (3), electrophysiology (4), c-fos expression (5), functional MRI (fMRI) (6), and optical imaging of voltage-sensitive dyes (7) or intrinsic signals (8). Experimental limitations of each method affect data interpretations because each method maps a specific signal. Certain experimental criteria have to be met for olfactory perception to be systematically and ideally derived from the functional architecture revealed by the SAPs: (i) the neuroanatomy of the whole OB has to be mapped; (ii) the dynamic nature of SAPs in the whole OB has to be mapped with both high spatial and temporal resolutions; (iii) laminar-specific activations in the different layers have to be quantitated; and (iv) reproducibility of SAPs has to be established in a quantitative manner such that the effects of stimulus parameters (e.g., odor type, concentration, and exposure duration) can be easily identified and separated. If each criterion is met on an intrasubject basis by a par...

show abstract

Norepinephrine increases rat mitral cell excitatory responses to weak olfactory nerve input via alpha-1 receptors in vitro

Cited by 73 publications

References 54 publications

Adrenergic modulation of olfactory bulb circuitry affects odor discrimination

Adrenergic modulation of olfactory bulb circuitry affects odor discrimination

Adrenergic Enhancement of Inhibitory Transmission in the Accessory Olfactory Bulb

Assessment and discrimination of odor stimuli in rat olfactory bulb by dynamic functional MRI

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