Postnatal Odor Exposure Increases the Strength of Interglomerular Lateral Inhibition onto Olfactory Bulb Tufted Cells

Geramita, Matthew; Urban, Nathaniel N.

doi:10.1523/jneurosci.1991-16.2016

Cited by 17 publications

(13 citation statements)

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“…The lack of clear odor-specificity in changes following odor conditioning was surprising, given previous work showing specificity in anatomic changes following prenatal and early postnatal odorant exposure ( Todrank et al, 2011 ; Liu et al, 2016 ), previous work showing that an early postnatal conditioning paradigm increases lateral inhibition ( Geramita and Urban, 2016 ), and the observation that early postnatal odor conditioning results in a reduced response to conditioned but not other odors ( Wilson et al, 1985 ). However, 2-DG maps of glomerular activation in rats (Glomerular Activity Response Archive, Michael Leon, gara.bio.uci.edu/index.jsp) show that both MS and hexanal activate a large number of potentially overlapping glomeruli on the dorsal OB surface, so it is possible that the widespread nature of the changes we observe in odor-evoked MC excitatory responses are due to the widespread activation of dorsal glomeruli by these exposure odorants.…”

Section: Discussionmentioning

confidence: 99%

“…We show that this paradigm also promotes nonspecific changes to excitatory MC odor-evoked responses; these findings contrast with previous studies of odor-evoked MC responses following both acute and chronic odor exposure. However, the majority of studies analyzing experience-dependent changes to the structure and function of the OB rely on postnatal manipulations ( Benson et al, 1984 ; Laing, 1985 ; Panhuber and Laing, 1987 ; Saghatelyan et al, 2005 ; Kerr and Belluscio, 2006 ; Woo et al, 2006 ; Cavallin et al, 2010 ; Johnson et al, 2013 ; Morrison et al, 2015 ; Geramita and Urban, 2016 ). Starting exposure during gestation may trigger developmental changes distinct from those observed with postnatal odor experience.…”

Section: Discussionmentioning

confidence: 99%

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Prenatal and Early Postnatal Odorant Exposure Heightens Odor-Evoked Mitral Cell Responses in the Mouse Olfactory Bulb

Liu

Urban

2017

eNeuro

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Early sensory experience shapes the anatomy and function of sensory circuits. In the mouse olfactory bulb (OB), prenatal and early postnatal odorant exposure through odorized food (food/odorant pairing) not only increases the volume of activated glomeruli but also increases the number of mitral and tufted cells (M/TCs) connected to activated glomeruli. Given the importance of M/TCs in OB output and in mediating lateral inhibitory networks, increasing the number of M/TCs connected to a single glomerulus may significantly change odorant representation by increasing the total output of that glomerulus and/or by increasing the strength of lateral inhibition mediated by cells connected to the affected glomerulus. Here, we seek to understand the functional impact of this long-term odorant exposure paradigm on the population activity of mitral cells (MCs). We use viral expression of GCaMP6s to examine odor-evoked responses of MCs following prenatal and early postnatal odorant exposure to two dissimilar odorants, methyl salicylate (MS) and hexanal, which are both strong activators of glomeruli on the dorsal OB surface. Previous work suggests that odor familiarity may decrease odor-evoked MC response in rodents. However, we find that early food-based odorant exposure significantly changes MC responses in an unexpected way, resulting in broad increases in the amplitude, number, and reliability of excitatory MC responses across the dorsal OB.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Prenatal and Early Postnatal Odorant Exposure Heightens Odor-Evoked Mitral Cell Responses in the Mouse Olfactory Bulb

Liu

Urban

2017

eNeuro

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“…Mutations in the multidomain scaffold protein Shank3 are associated with autism spectrum disorders (ASDs), Phelan-McDermid syndrome, and intellectual disability (Betancur and Buxbaum, 2013). Animal models of Shank3 loss have revealed circuit defects in many brain regions that might contribute to these shankopathies (Bariselli et al, 2016;Bey et al, 2018;Bozdagi et al, 2010;Duffney et al, 2015;Geramita and Urban, 2016;Jaramillo et al, 2017;Kouser et al, 2013;Lee et al, 2015;Orefice et al, 2016;Peç a et al, 2011;Peixoto et al, 2016;Schmeisser et al, 2012;Speed et al, 2015;Wang et al, 2011;Yang et al, 2012;Zhou et al, 2019), but a unified view of how Shank3 loss disrupts circuit function is lacking. A common feature of several monogenic ASD rodent models is loss of cellular homeostatic plasticity mechanisms (Blackman et al, 2012;Bulow et al, 2019;Dani et al, 2005;Nelson and Valakh, 2015;Soden and Chen, 2010;Zhong et al, 2018), leading us to ask whether Shank3 loss compromises homeostatic compensation.…”

Section: Introductionmentioning

confidence: 99%

Autism-Associated Shank3 Is Essential for Homeostatic Compensation in Rodent V1

Tatavarty

Pacheco

Kuhnle

et al. 2020

Neuron

125

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Mutations in Shank3 are strongly associated with autism spectrum disorders and neural circuit changes in several brain areas, but the cellular mechanisms that underlie these defects are not understood. Homeostatic forms of plasticity allow central circuits to maintain stable function during experience-dependent development, leading us to ask whether loss of Shank3 might impair homeostatic plasticity and circuit-level compensation to perturbations. We found that Shank3 loss in vitro abolished synaptic scaling and intrinsic homeostatic plasticity, deficits that could be rescued by treatment with lithium. Further, Shank3 knockout severely compromised the in vivo ability of visual cortical circuits to recover from perturbations to sensory drive. Finally, lithium treatment ameliorated a repetitive self-grooming phenotype in Shank3 knockout mice. These findings demonstrate that Shank3 loss severely impairs the ability of central circuits to harness homeostatic mechanisms to compensate for perturbations in drive, which, in turn, may render them more vulnerable to such perturbations.

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“…; Economo et al . ; Geramita & Urban, ; Liu et al . ) and multiple basal dendrites coursing laterally in the EPL to receive synaptic inhibition from GCs (Isaacson & Strowbridge, ; Shepherd et al .…”

Section: Resultsmentioning

confidence: 99%

Cholecystokinin selectively activates short axon cells to enhance inhibition of olfactory bulb output neurons

Liu

2018

The Journal of Physiology

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Neuropeptides such as cholecystokinin (CCK) are important for many brain functions, including sensory processing. CCK is predominantly present in a subpopulation of excitatory neurons and activation of CCK receptors is implicated in olfactory signal processing in the olfactory bulb (OB). However, the cellular and circuit mechanisms underlying the actions of CCK in the OB remain elusive. In the present study, we characterized the effects of CCK on synaptic inhibition of the principal OB output neurons mitral/tufted cells (MTCs) followed by mechanistic analyses at both circuit and cellular levels. First, we found that CCK via CCK-B receptors enhances the GABA receptor-mediated spontaneous IPSCs in MTCs. Second, CCK does not affect the action potential independent miniature IPSCs in MTCs. Third, CCK potentiates glomerular inhibition resulting in increased GABA receptor-mediated presynaptic inhibition of olfactory nerve terminals and enhanced spontaneous IPSCs in MTCs and glomerular neurons. Fourth, CCK enhances miniature IPSCs in the excitatory external tufted cells, although neither in the inhibitory short axon cells (SACs) nor in periglomerular cells (PGCs). Finally, CCK excites all tested SACs and a very small minority of GABAergic neurons in the granule cell layer or in periglomerular cells, but not in deep SACs. These results demonstrate that CCK selectively activates SACs to engage the SAC-formed interglomerular circuit and thus elevates inhibition broadly in the OB glomerular layer. This modulation may prevent the system from saturating in response to a high concentration of odourants or facilitate the detection of weak stimuli by increasing signal-to-noise ratio.

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Postnatal Odor Exposure Increases the Strength of Interglomerular Lateral Inhibition onto Olfactory Bulb Tufted Cells

Cited by 17 publications

References 50 publications

Prenatal and Early Postnatal Odorant Exposure Heightens Odor-Evoked Mitral Cell Responses in the Mouse Olfactory Bulb

Prenatal and Early Postnatal Odorant Exposure Heightens Odor-Evoked Mitral Cell Responses in the Mouse Olfactory Bulb

Autism-Associated Shank3 Is Essential for Homeostatic Compensation in Rodent V1

Cholecystokinin selectively activates short axon cells to enhance inhibition of olfactory bulb output neurons

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