Differential Muscarinic Modulation in the Olfactory Bulb

Smith, Richard; Hu, Ruilong; DeSouza, Andre; Eberly, Christian; Krahe, Krista; Chan, Wilson; Araneda, Ricardo C.

doi:10.1523/jneurosci.0099-15.2015

Cited by 50 publications

(116 citation statements)

References 81 publications

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“…GCs are a heterogeneous group of neurons, and they exhibit distinct characteristics in the AOB and MOB, including synaptic properties and regulation by neuromodulatory transmitters (Castro et al, 2007; Zimnik et al, 2013; Burton and Urban, 2015; Smith et al, 2015). Accordingly, we found that the voltage sensitivity of I h was modulated by cAMP in the MOB, but not in the AOB; nevertheless, I h activation was faster in the AOB in the presence of cAMP.…”

Section: Discussionmentioning

confidence: 99%

“…Experiments were performed in OB slices using methods previously described (Smith et al, 2015). Briefly, brain slices were prepared in an oxygenated ice-cold artificial CSF (ACSF) containing low Ca 2+ (0.5 m m ) and high Mg 2+ (6 m m ).…”

Section: Methodsmentioning

confidence: 99%

“…This internal solution, which contains Na, was used in order to compare the physiology of GCs with previous work published from our laboratory (Smith et al, 2015). In some experiments, 0.5 m m cAMP was added to the internal solution.…”

Section: Methodsmentioning

confidence: 99%

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Hyperpolarization-Activated Currents and Subthreshold Resonance in Granule Cells of the Olfactory Bulb

Ferguson

Whiteus

et al. 2016

eNeuro

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An important contribution to neural circuit oscillatory dynamics is the ongoing activation and inactivation of hyperpolarization-activated currents (Ih). Network synchrony dynamics play an important role in the initial processing of odor signals by the main olfactory bulb (MOB) and accessory olfactory bulb (AOB). In the mouse olfactory bulb, we show that Ih is present in granule cells (GCs), the most prominent inhibitory neuron in the olfactory bulb, and that Ih underlies subthreshold resonance in GCs. In accord with the properties of Ih, the currents exhibited sensitivity to changes in extracellular K+ concentration and ZD7288 (4-ethylphenylamino-1,2-dimethyl-6-methylaminopyrimidin chloride), a blocker of Ih. ZD7288 also caused GCs to hyperpolarize and increase their input resistance, suggesting that Ih is active at rest in GCs. The inclusion of cAMP in the intracellular solution shifted the activation of Ih to less negative potentials in the MOB, but not in the AOB, suggesting that channels with different subunit composition mediate Ih in these regions. Furthermore, we show that mature GCs exhibit Ih-dependent subthreshold resonance in the theta frequency range (4–12 Hz). Another inhibitory subtype in the MOB, the periglomerular cells, exhibited Ih-dependent subthreshold resonance in the delta range (1–4 Hz), while principal neurons, the mitral cells, do not exhibit Ih-dependent subthreshold resonance. Importantly, Ih size, as well as the strength and frequency of resonance in GCs, exhibited a postnatal developmental progression, suggesting that this development of Ih in GCs may differentially contribute to their integration of sensory input and contribution to oscillatory circuit dynamics.

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Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

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Hyperpolarization-Activated Currents and Subthreshold Resonance in Granule Cells of the Olfactory Bulb

Ferguson

Whiteus

et al. 2016

eNeuro

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“…the MOB and suggests that these circuits utilize different physiological solutions for processing odour information (Smith et al . ). While there is strong structural and biophysical characterization of the role of serotonergic signalling in the MOB (Hardy et al .…”

Section: Introductionmentioning

confidence: 97%

Differential serotonergic modulation across the main and accessory olfactory bulbs

Huang

Thiebaud

Fadool

2017

The Journal of Physiology

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Mitral cells (MCs) contained in the main (MOB) and accessory (AOB) olfactory bulb have distinct intrinsic membrane properties but the extent of neuromodulation across the two systems has not been widely explored. Herein, we investigated a widely distributed CNS modulator, serotonin (5-HT), for its ability to modulate the biophysical properties of MCs across the MOB and AOB, using an in vitro, brain slice approach in postnatal 15-30 day mice. In the MOB, 5-HT elicited three types of responses in 93% of 180 cells tested. Cells were either directly excited (70%), inhibited (10%) or showed a mixed response (13%)- first inhibition followed by excitation. In the AOB, 82% of 148 cells were inhibited with 18% of cells showing no response. Albeit located in parallel partitions of the olfactory system, 5-HT largely elicited MC excitation in the MOB while it evoked two different kinetic rates of MC inhibition in the AOB. Using a combination of pharmacological agents, we found that the MC excitatory responses in the MOB were mediated by 5-HT receptors through a direct activation. In comparison, 5-HT-evoked inhibitory responses in the AOB arose due to a polysynaptic, slow-onset inhibition attributed to 5-HT receptor activation exciting GABAergic interneurons. The second type of inhibition had a rapid onset as a result of direct inhibition mediated by the 5-HT class of receptors. The distinct serotonergic modulation of MCs between the MOB and AOB could provide a molecular basis for differential chemosensory behaviours driven by the brainstem raphe nuclei into these parallel systems.

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“…In the OB, Ach has been shown to modulate principal cells and different classes of interneurons via both nicotinic and muscarinic receptors (Ravel et al, 1990; Castillo et al, 1999; Crespo et al, 2000; Pressler et al, 2007; D'souza and Vijayaraghavan, 2012; Ma and Luo, 2012; D'souza et al, 2013; Rothermel et al, 2014; Liu et al, 2015; Smith et al, 2015; Bendahmane et al, 2016). From these data, the net functional effect of ACh inputs to the OB can be constructed as enhancing mitral cell selectivity to odorants through increased inhibition and filtering of low amplitude inputs in concert with increased excitability in response to selective odorants; this idea is supported by behavioral and electrophysiological data (Elaagouby et al, 1991; Linster et al, 2001; Wilson et al, 2004; Mandairon et al, 2006; Devore et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

Internal Cholinergic Regulation of Learning and Recall in a Model of Olfactory Processing

Almeida

Idiart

Dean

et al. 2016

Front. Cell. Neurosci.

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In the olfactory system, cholinergic modulation has been associated with contrast modulation and changes in receptive fields in the olfactory bulb, as well the learning of odor associations in olfactory cortex. Computational modeling and behavioral studies suggest that cholinergic modulation could improve sensory processing and learning while preventing pro-active interference when task demands are high. However, how sensory inputs and/or learning regulate incoming modulation has not yet been elucidated. We here use a computational model of the olfactory bulb, piriform cortex (PC) and horizontal limb of the diagonal band of Broca (HDB) to explore how olfactory learning could regulate cholinergic inputs to the system in a closed feedback loop. In our model, the novelty of an odor is reflected in firing rates and sparseness of cortical neurons in response to that odor and these firing rates can directly regulate learning in the system by modifying cholinergic inputs to the system. In the model, cholinergic neurons reduce their firing in response to familiar odors—reducing plasticity in the PC, but increase their firing in response to novel odor—increasing PC plasticity. Recordings from HDB neurons in awake behaving rats reflect predictions from the model by showing that a subset of neurons decrease their firing as an odor becomes familiar.

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Differential Muscarinic Modulation in the Olfactory Bulb

Cited by 50 publications

References 81 publications

Hyperpolarization-Activated Currents and Subthreshold Resonance in Granule Cells of the Olfactory Bulb

Hyperpolarization-Activated Currents and Subthreshold Resonance in Granule Cells of the Olfactory Bulb

Differential serotonergic modulation across the main and accessory olfactory bulbs

Internal Cholinergic Regulation of Learning and Recall in a Model of Olfactory Processing

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