Optogenetic Activation of Dorsal Raphe Serotonin Neurons Rapidly Inhibits Spontaneous But Not Odor-Evoked Activity in Olfactory Cortex

Lottem, Eran; Lőrincz, Magor L.; Mainen, Zachary F.

doi:10.1523/jneurosci.3008-15.2016

Cited by 67 publications

(77 citation statements)

References 60 publications

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“…The degree to which the influence of a single serotonergic neuron is conserved across processing stages is unknown, however work in mice suggests that the functional roles of serotonergic neurons can differ between networks. Raphe stimulation differentially affects the odor-evoked responses of mitral and tufted cells in the main olfactory bulb [103] yet only affects spontaneous activity rather than the odor-evoked responses of single units recorded in primary piriform cortex [106]. Consistent with the idea that serotonin may play different functional roles across processing stages, we found several differences in the general connectivity rules of a single serotonergic neuron between olfactory processing stages.…”

Section: Discussionsupporting

confidence: 76%

The wiring logic of an identified serotonergic neuron that spans sensory networks

Coates

Calle-Schuler

Helmick

et al. 2020

Preprint

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19Serotonergic neurons modulate diverse physiological and behavioral processes in a 20 context-dependent manner, based on their complex connectivity. However, their 21 connectivity has not been comprehensively explored at a single-cell resolution. Using a 22 whole-brain EM dataset we determined the wiring logic of a broadly projecting 23 serotonergic neuron (the "CSDn") in Drosophila. Within the antennal lobe (AL; first-order 24 olfactory region), the CSDn receives glomerulus-specific input and preferentially targets 25 distinct local interneuron subtypes. Furthermore, the wiring logic of the CSDn differs 26 between olfactory regions. The CSDn innervates the AL and lateral horn (LH), yet does 27 not maintain the same synaptic relationship with individual projection neurons that also 28 span both regions. Consistent with this, the CSDn has more distributed connectivity in 29 the LH relative to the AL, preferentially synapsing with principal neuron types based on 30 presumptive transmitter content. Lastly, we identify protocerebral neurons that provide 31 abundant synaptic input to the CSDn. Our study demonstrates how an individual 32 modulatory neuron can interact with local networks and integrate input from non-33 olfactory sources. 35Introduction 36 Every neural network receives modulatory input from a variety of sources [1, 2], 37 and in some cases from heterogeneous populations of neurons that release the same 38 modulatory transmitter [3][4][5]. In mammals, one ubiquitous neuromodulator, serotonin, is 39 released by tens of thousands to hundreds of thousands of neurons which originate in 40 the raphe nuclei and project throughout the brain [6, 7]. Serotonergic raphe neurons are 41 highly diverse in their projections, connectivity, and electrophysiological properties, and 42 2 are implicated in a wide breadth of behaviors and physiological processes [4,[8][9][10][11][12][13][14][15][16]. 43 Further, the raphe system receives monosynaptic input from up to 80 anatomical areas 44 [8, 9]. As a result, a significant amount of work has focused on disentangling the 45 functional and behavioral roles of serotonergic neurons. Several recent studies have 46 suggested that serotonergic raphe neurons may be organized into functional 47 subpopulations based on neuroanatomy, electrophysiology, and behavior [4, 12,[17][18][19][20][21]. 48For example, two parallel sub-systems of serotonergic raphe neurons collateralize 49 complimentarily and are both activated by reward, yet have opposing responses to 50 aversive stimuli and promote distinct behaviors [18]. Sparse neuron reconstructions in 51 mice show that a single serotonin neuron can interconnect the olfactory bulb, piriform 52 cortex, and anterior olfactory nucleus [19], demonstrating that a single serotonergic 53 neuron can arborize several processing stages within the same sensory modality. Thus, 54 determining the precise patterns of connectivity of single serotonergic neurons within 55 and across the brain regions will be critical for understanding t...

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Section: Discussionsupporting

confidence: 76%

The wiring logic of an identified serotonergic neuron that spans sensory networks

Coates

Calle-Schuler

Helmick

et al. 2020

Preprint

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“…Facilitated by this circuitry, 5-HT and its receptors modulate olfactory system function (McLean et al, 1993; Aungst and Shipley, 2005; Hardy et al, 2005; Petzold et al, 2009; Liu et al, 2011a; Schmidt and Strowbridge, 2014; Brill et al, 2016; Brunert et al, 2016; Kapoor et al, 2016; Linster and Cleland, 2016; Lottem et al, 2016). For instance, electrical stimulation of the raphe nuclei modulates the level of odor information input into the olfactory bulb (Petzold et al, 2009).…”

Section: Introductionmentioning

confidence: 99%

Preservation of Essential Odor-Guided Behaviors and Odor-Based Reversal Learning after Targeting Adult Brain Serotonin Synthesis

Carlson

Whitney

Gadziola

et al. 2016

eNeuro

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“…As a phylogenetically "old" structure, the PC is also likely to express canonical cortical circuits that have been conserved across evolution (18). Spontaneous spiking has been reported in the PC of rodents breathing odor-free air (19)(20)(21)(22)(23), but these studies used unit recordings, which provide a biased estimate of firing rates (2), and none of them identified the drivers or roles of this activity. Here we use two-photon calcium imaging and whole-cell patch clamping from identified PC neurons in vivo to measure the properties of stimulus-decoupled spiking.…”

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confidence: 99%

Spontaneous activity in the piriform cortex extends the dynamic range of cortical odor coding

Tantirigama

Huang

Bekkers

2017

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

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Neurons in the neocortex exhibit spontaneous spiking activity in the absence of external stimuli, but the origin and functions of this activity remain uncertain. Here, we show that spontaneous spiking is also prominent in a sensory paleocortex, the primary olfactory (piriform) cortex of mice. In the absence of applied odors, piriform neurons exhibit spontaneous firing at mean rates that vary systematically among neuronal classes. This activity requires the participation of NMDA receptors and is entirely driven by bottom-up spontaneous input from the olfactory bulb. Odor stimulation produces two types of spatially dispersed, odor-distinctive patterns of responses in piriform cortex layer 2 principal cells: Approximately 15% of cells are excited by odor, and another approximately 15% have their spontaneous activity suppressed. Our results show that, by allowing odor-evoked suppression as well as excitation, the responsiveness of piriform neurons is at least twofold less sparse than currently believed. Hence, by enabling bidirectional changes in spiking around an elevated baseline, spontaneous activity in the piriform cortex extends the dynamic range of odor representation and enriches the coding space for the representation of complex olfactory stimuli.T he brain remains intensely active even under conditions when overt external stimuli are absent (1). At first glance this behavior can seem puzzling. Pyramidal neurons in primary sensory neocortex, for example, typically fire spontaneously at approximately 1 Hz when the relevant stimuli are not present (2), raising the possibility that this background activity is noise that must be mitigated by signal averaging (3). On the other hand, spontaneous cortical activity is often structured (4) and can reflect the global state of the animal (5), suggesting that it is not simply an impediment but may serve a useful computational role. Indeed, such activity may be important for gating sensory inputs (4, 6), establishing and maintaining sensory maps (7-9), and extending the dynamic range of sensory-evoked responses (10, 11). The significance of spontaneous activity is also supported by theoretical studies showing that it emerges naturally from balanced neural networks with desirable information-processing characteristics (9, 12).Given that spontaneous spiking is likely to be a key element of cortical function, it is important to study its prevalence and properties in different cortical areas. The piriform cortex (PC) is a sensory paleocortex in mammals that is critical for recognizing and remembering odors (13-17). The PC offers a number of advantages for the study of neural information processing, including a simple trilaminar architecture and well-defined afferent input from the olfactory bulb (OB) (16, 17). As a phylogenetically "old" structure, the PC is also likely to express canonical cortical circuits that have been conserved across evolution (18). Spontaneous spiking has been reported in the PC of rodents breathing odor-free air (19-23), but these studies used unit r...

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Optogenetic Activation of Dorsal Raphe Serotonin Neurons Rapidly Inhibits Spontaneous But Not Odor-Evoked Activity in Olfactory Cortex

Cited by 67 publications

References 60 publications

The wiring logic of an identified serotonergic neuron that spans sensory networks

The wiring logic of an identified serotonergic neuron that spans sensory networks

Preservation of Essential Odor-Guided Behaviors and Odor-Based Reversal Learning after Targeting Adult Brain Serotonin Synthesis

Spontaneous activity in the piriform cortex extends the dynamic range of cortical odor coding

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