Input dependent modulation of olfactory bulb activity by HDB GABAergic projections

Böhm, Erik; Brunert, Daniela; Rothermel, Markus

doi:10.1038/s41598-020-67276-z

Cited by 38 publications

(69 citation statements)

References 122 publications

(170 reference statements)

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“…On the other hand, other experiments have revealed that basal forebrain cholinergic projections to the olfactory bulb increase excitability, modulate signal to noise ratios in mitral cell firing, and can rapidly dishabituate olfactory bulb odor responses (Ma and Luo, 2012;Rothermel et al, 2014;Ogg et al, 2018). Finally, more recent studies have directly compared optogenetic stimulation of basal forebrain cholinergic and GABAergic terminals within the olfactory bulb (Böhm et al, 2020), describing that local stimulation of cholinergic terminals increased mitral cell firing during sniffing regardless of odor presentation, whereas stimulation of GABAergic terminals decreased spontaneous mitral cell firing and increased firing during sniffing only when odors were presented. Together, these findings imply that basal forebrain cholinergic and GABAergic neurons mediate distinct features of top-down regulation, and that both types of basal forebrain projections modulate olfactory bulb odor and sniff responses.…”

Section: Discussionmentioning

confidence: 99%

“…Importantly, cholinergic and GABAergic neurons in the basal forebrain work together to modulate downstream circuit function (Dannenberg et al, 2015;Böhm et al, 2020). An outstanding question is how parallel cholinergic and GABAergic output pathways are coordinated during behavior at the level of the basal forebrain.…”

Section: Discussionmentioning

confidence: 99%

“…GABAergic neurons in the HDB express cholinergic receptors and respond to local acetylcholine release (Yang et al, 2014;Xu et al, 2015). At the same time, GABAergic output from the HDB mediates distinct forms of top-down regulation important for state-dependent active sensing and odor discrimination (Nunez-Parra et al, 2013;Böhm et al, 2020). Having found that local cholinergic tone is dynamically regulated during performance of an olfactorycued go/no-go task, we next examined whether changes in local cholinergic tone corresponded to changes in basal forebrain GABAergic neuronal activity.…”

Section: Odor-evoked Activity and Reward-related Suppression Of Basalmentioning

confidence: 99%

“…Parallel cholinergic and GABAergic projections from the basal forebrain to the olfactory bulb mediate distinct features of top-down regulation (Böhm et al, 2020). Separately, the cholinergic and GABAergic projections control gain, signal-to-noise ratio, habituation, and oscillatory activity, and odor discrimination (Ma and Luo, 2012;Nunez-Parra et al, 2013;Rothermel et al, 2014;Ogg et al, 2018;Villar et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

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Dynamic cholinergic tone in the basal forebrain reflects reward-seeking and reinforcement during olfactory behavior

Hanson¹,

Brandel-Ankrapp

Arenkiel³

2020

Preprint

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Sensory perception underlies how we internalize and interact with the external world. In order to adapt to changing circumstances and interpret signals in a variety of contexts, sensation needs to be reliable, but perception of sensory input needs to be flexible. An important mediator of this flexibility is top-down regulation from the cholinergic basal forebrain. Basal forebrain projection neurons serve as pacemakers and gatekeepers for downstream neural networks, modulating circuit activity across diverse neuronal populations. This top-down control is necessary for sensory cue detection, learning, and memory, and is disproportionately disrupted in neurodegenerative diseases associated with cognitive decline. Intriguingly, cholinergic signaling acts locally within the basal forebrain to sculpt the activity of basal forebrain output neurons. To determine how local cholinergic signaling impacts basal forebrain output pathways that participate in top-down regulation, we sought to define the dynamics of cholinergic signaling within the basal forebrain during motivated behavior and learning. Towards this, we utilized fiber photometry and the genetically encoded acetylcholine indicator GAChR2.0 to define temporal patterns of cholinergic signaling in the basal forebrain during olfactory-guided, motivated behaviors and learning. We show that cholinergic signaling reliably increased during reward seeking behaviors but was strongly suppressed by reward delivery in a go/no-go, olfactory-cued discrimination task. The observed transient reduction in cholinergic tone was mirrored by a suppression in basal forebrain GABAergic neuronal activity. Together, these findings suggest that cholinergic tone in the basal forebrain changes rapidly to reflect reward-seeking behavior and positive reinforcement to impact basal forebrain circuit activity.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Odor-evoked Activity and Reward-related Suppression Of Basalmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Dynamic cholinergic tone in the basal forebrain reflects reward-seeking and reinforcement during olfactory behavior

Hanson¹,

Brandel-Ankrapp

Arenkiel³

2020

Preprint

View full text Add to dashboard Cite

show abstract

“…Moreover, it was shown that stimulation of HDB ACh neurons can sharpen the odor responses of MOB M/TCs [41,42]. Since we had obtained whole brains from the exposure experiments (water, rat urine, conspecific), we next investigated the activity of ACh neurons in the HDB.…”

Section: Cholinergic Cells In the Hdb Are Activated During Social Intmentioning

confidence: 99%

Top-down acetylcholine contributes to social discrimination via enabling action potentials in olfactory bulb vasopressin cells

Suyama

Egger

Lukas

2020

Preprint

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Social discrimination in rats requires activation of the intrinsic bulbar vasopressin system, but it is unclear how this system comes into operation. Here we show that a higher number of bulbar vasopressin cells (VPC) is activated by stimulation with a conspecific compared to rat urine, indicating that VPC activation depends on more than olfactory cues during social interaction. In-vitro slice electrophysiology combined with pharmacology and immunohistochemistry then demonstrated that centrifugal cholinergic inputs from the diagonal band of Broca can enable olfactory nerve-evoked action potentials in VPCs via muscarinic neuromodulation. Finally, such muscarinic activation of the vasopressin system is essential for vasopressin-dependent social discrimination, since recognition of a known rat could be blocked by a muscarinic antagonist and rescued by additional application of vasopressin. For the first time, we demonstrated that top-down cholinergic modulation of bulbar VPC activity in a social context is crucial for individual social discrimination in rats.

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Extrinsic neuromodulation in the rodent olfactory bulb

Brunert

Rothermel

2020

Cell Tissue Res

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Evolutionarily, olfaction is one of the oldest senses and pivotal for an individual’s health and survival. The olfactory bulb (OB), as the first olfactory relay station in the brain, is known to heavily process sensory information. To adapt to an animal’s needs, OB activity can be influenced by many factors either from within (intrinsic neuromodulation) or outside (extrinsic neuromodulation) the OB which include neurotransmitters, neuromodulators, hormones, and neuropeptides. Extrinsic sources seem to be of special importance as the OB receives massive efferent input from numerous brain centers even outweighing the sensory input from the nose. Here, we review neuromodulatory processes in the rodent OB from such extrinsic sources. We will discuss extrinsic neuromodulation according to points of origin, receptors involved, affected circuits, and changes in behavior. In the end, we give a brief outlook on potential future directions in research on neuromodulation in the OB.

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Input dependent modulation of olfactory bulb activity by HDB GABAergic projections

Cited by 38 publications

References 122 publications

Dynamic cholinergic tone in the basal forebrain reflects reward-seeking and reinforcement during olfactory behavior

Dynamic cholinergic tone in the basal forebrain reflects reward-seeking and reinforcement during olfactory behavior

Top-down acetylcholine contributes to social discrimination via enabling action potentials in olfactory bulb vasopressin cells

Extrinsic neuromodulation in the rodent olfactory bulb

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