Activity-Dependent Changes in Cholinergic Innervation of the Mouse Olfactory Bulb

Salcedo, Ernesto E.; Tran, Tuan Q.; Ly, Xuan; Lopez, Robert; Barbica, Cortney; Restrepo, Diego; Vijayaraghavan, Sukumar

doi:10.1371/journal.pone.0025441

Cited by 29 publications

(41 citation statements)

References 37 publications

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“…This is consistent with the patterning of cholinergic innervation in the glomerular layer (Salcedo et al, 2011). The postnatal development of cholinergic innervation also extends to the EPL where GC dendrites make GABAergic contacts with the MCs.…”

Section: Cholinergic Receptor Distribution In the Obsupporting

confidence: 88%

“…This innervation is complete by postnatal day 12 (Salcedo et al, 2011). However, during further maturation, there is a distinct patterning of the innervation, with the predominant projections being directed to the glomerular layer ( Figures 2 and 3 ) and sparser projections to other OB layers (Macrides et al, 1981; Salcedo et al, 2011).…”

Section: The Olfactory Bulb and Its Cholinergic Inputmentioning

confidence: 99%

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Paying attention to smell: cholinergic signaling in the olfactory bulb

D’Souza

Vijayaraghavan

2014

Front. Synaptic Neurosci.

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The tractable, layered architecture of the olfactory bulb (OB), and its function as a relay between odor input and higher cortical processing, makes it an attractive model to study how sensory information is processed at a synaptic and circuit level. The OB is also the recipient of strong neuromodulatory inputs, chief among them being the central cholinergic system. Cholinergic axons from the basal forebrain modulate the activity of various cells and synapses within the OB, particularly the numerous dendrodendritic synapses, resulting in highly variable responses of OB neurons to odor input that is dependent upon the behavioral state of the animal. Behavioral, electrophysiological, anatomical, and computational studies examining the function of muscarinic and nicotinic cholinergic receptors expressed in the OB have provided valuable insights into the role of acetylcholine (ACh) in regulating its function. We here review various studies examining the modulation of OB function by cholinergic fibers and their target receptors, and provide putative models describing the role that cholinergic receptor activation might play in the encoding of odor information.

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Section: Cholinergic Receptor Distribution In the Obsupporting

confidence: 88%

Section: The Olfactory Bulb and Its Cholinergic Inputmentioning

confidence: 99%

Paying attention to smell: cholinergic signaling in the olfactory bulb

D’Souza

Vijayaraghavan

2014

Front. Synaptic Neurosci.

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“…In the rodent MOB, massive fibers originated from HDB neurons primarily terminate in the glomerular layer and internal plexiform layer to form synapses with M/T cells and interneurons, mainly PG cells and granule cells (Nickell and Shipley, 1988a;Le Jeune and Jourdan, 1993;Salcedo et al, 2011). Consistently, bulbar neurons express nicotinic-type and muscarinic-type cholinergic receptors (Castillo et al, 1999;Crespo et al, 2000).…”

Section: Discussionmentioning

confidence: 98%

“…The MOB receives strong centrifugal inputs from the horizontal limb of the diagonal band of Broca (HDB), in which many cholinergic neurons are located (Macrides et al, 1981;Brashear et al, 1986;Salcedo et al, 2011). Although it is commonly believed that acetylcholine modulates signal processing in the MOB (Fletcher and Chen, 2010), its exact effects appear to be complex and different studies report seemingly opposite findings.…”

Section: Introductionmentioning

confidence: 99%

Optogenetic Activation of Basal Forebrain Cholinergic Neurons Modulates Neuronal Excitability and Sensory Responses in the Main Olfactory Bulb

Ma¹,

Luo²

2012

Journal of Neuroscience

115

138

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The main olfactory bulb (MOB) in mammals receives massive centrifugal input from cholinergic neurons in the horizontal limb of the diagonal band of Broca (HDB) in the basal forebrain, the activity of which is thought to be correlated with animal behaving states, such as attention. Cholinergic signals in the bulb facilitate olfactory discrimination and learning, but it has remained controversial how the activity of HDB cholinergic neurons modulates neuronal excitability and olfactory responses in the MOB. In this study, we used an optogenetic approach to selectively activate HDB cholinergic neurons and recorded the effect of this activation on the spontaneous firing activity and odor-evoked responses of mouse MOB neurons. Cells were juxtacellularly labeled and their specific types were morphologically determined. We find that light stimulation of HDB cholinergic neurons inhibits the spontaneous firing activity of all major cell types, including mitral/tufted (M/T) cells, periglomerular (PG) cells, and GABAergic granule cells. Inhibitions are significantly produced by stimulation at 10 Hz and further enhanced at higher frequencies. In addition, cholinergic activation sharpens the olfactory tuning curves of a majority of M/T cells but broadly potentiates odor-evoked responses of PG cells and granule cells. These results demonstrate strong effects of the basal forebrain cholinergic system on modulating neuronal excitability in the MOB and support the hypothesis that cholinergic activity increases olfactory discrimination capability.

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“…The variable and diffuse cholinergic projections from the basal forebrain (24,25) and the lack of specific topography within the horizontal limb of the diagonal band of Broca suggest that cholinergic modulation occurs across the bulb, rather than in a glomerular-or odor-specific manner. Such an arrangement points to control of more global arousal/attentional processes (26,27) than specific odor-driven modulation.…”

Section: Discussionmentioning

confidence: 99%

Signaling between periglomerular cells reveals a bimodal role for GABA in modulating glomerular microcircuitry in the olfactory bulb

Parsa

D’Souza

Vijayaraghavan

2015

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

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In the mouse olfactory bulb glomerulus, the GABAergic periglomerular (PG) cells provide a major inhibitory drive within the microcircuit. Here we examine GABAergic synapses between these interneurons. At these synapses, GABA is depolarizing and exerts a bimodal control on excitability. In quiescent cells, activation of GABA A receptors can induce the cells to fire, thereby providing a means for amplification of GABA release in the glomerular microcircuit via GABA-induced GABA release. In contrast, GABA is inhibitory in neurons that are induced to fire tonically. PG-PG interactions are modulated by nicotinic acetylcholine receptors (nAChRs), and our data suggest that changes in intracellular calcium concentrations triggered by nAChR activation can be amplified by GABA release. Our results suggest that bidirectional control of inhibition in PG neurons can allow for modulatory inputs, like the cholinergic inputs from the basal forebrain, to determine threshold set points for filtering out weak olfactory inputs in the glomerular layer of the olfactory bulb via the activation of nAChRs.

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Activity-Dependent Changes in Cholinergic Innervation of the Mouse Olfactory Bulb

Cited by 29 publications

References 37 publications

Paying attention to smell: cholinergic signaling in the olfactory bulb

Paying attention to smell: cholinergic signaling in the olfactory bulb

Optogenetic Activation of Basal Forebrain Cholinergic Neurons Modulates Neuronal Excitability and Sensory Responses in the Main Olfactory Bulb

Signaling between periglomerular cells reveals a bimodal role for GABA in modulating glomerular microcircuitry in the olfactory bulb

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