Top-down modulation of olfactory-guided behaviours by the anterior olfactory nucleus pars medialis and ventral hippocampus

Aqrabawi, Afif J; Browne, Caleb J.; Dargaei, Zahra; Garand, Danielle; Khademullah, C. Sahara; Woodin, Melanie A.; Kim, Jun Chul

doi:10.1038/ncomms13721

Cited by 53 publications

(43 citation statements)

References 29 publications

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“…Additionally, there might also be "state-dependent" AON activation by higher brain areas which might be spatiotemporally much broader, thereby potentially more closely reflecting the here applied optical stimulation. In line with our results, activation of a subregion of the AON (medial AON, potentially driven by hippocampal inputs) using a chemogenetic approach was recently reported to reduce olfactory sensitivity as well as to impair the performance of olfaction-dependent behaviors (Aqrabawi et al, 2016). However, due to the slow nature of the chemogenetic approach, the temporal component of this effect could not be investigated.…”

Section: Functional Role Of Modulating Aon Activitysupporting

confidence: 64%

Dynamic inhibition of sensory responses mediated by an olfactory corticofugal system

Quintela

Bauer

Wallhorn

et al. 2020

Preprint

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Processing of sensory information is substantially modulated by centrifugal projections from higher cortical areas, yet their behavioral relevance and underlying neural mechanisms remain unclear in most cases. The anterior olfactory nucleus (AON) is part of the olfactory cortex and its extensive connections to lower and higher brain centers put it in a prime position to modulate early sensory information in the olfactory system. Here, we show that optogenetic activation of AON neurons in awake animals was not perceived as an odorant equivalent cue. However, AON activation during odorant presentation reliably suppressed odor responses. This AON mediated effect was fast and constant across odors and concentrations. Likewise, activation of glutamatergic AON projections to the olfactory bulb (OB) transiently inhibited the excitability of mitral/tufted cells (MTCs) that relay olfactory input to cortex. Single-unit MTC recordings revealed that optogenetic activation of glutamatergic AON terminals in the OB transiently decreased sensory-evoked MTC spiking, regardless of the strength or polarity of the sensory response. These findings suggest that glutamatergic AON projections to the OB suppress early olfactory processing by inhibiting OB output neurons and that the AON can dynamically gate sensory throughput to the cortex.Significance StatementThe anterior olfactory nucleus (AON) as an olfactory information processing area sends extensive projections to lower and higher brain centers but the behavioral consequences of its activation have been scarcely investigated. Using behavioral tests in combination with optogenetic manipulation we show that in contrast to what has been suggested previously, the AON does not seem to form odor percepts but instead suppresses odor responses across odorants and concentrations. Furthermore, this study shows that glutamatergic cortical projections to the olfactory bulb suppress olfactory processing by inhibiting output neurons, pointing to a potential mechanisms by which the olfactory cortex can actively and dynamically gate sensory throughput to higher brain centers.HighlightsAON stimulation suppresses odor responses across odorants and concentrationsAON activation is not perceived as an odorant equivalent cueThe AON dynamically shapes olfactory bulb output on a fast timescaleAON input to the olfactory bulb strongly suppresses mitral/tufted cells firing

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Section: Functional Role Of Modulating Aon Activitysupporting

confidence: 64%

Dynamic inhibition of sensory responses mediated by an olfactory corticofugal system

Quintela

Bauer

Wallhorn

et al. 2020

Preprint

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“…The hippocampus‐reuniens‐cortical network may be important for the consolidation of olfactory memory traces during exploratory behavior (Varela, Kumar, Yang, & Wilson, ). Thus, rodents routinely forage to find sources of caloric food in their environment, and this behavior might rely on hippocampal‐dependent spatial memory (Aqrabawi et al, ; Kulkarni, Stolberg, Sullivan, & Ferris, ).…”

Section: Discussionmentioning

confidence: 99%

Centrifugal projections to the main olfactory bulb revealed by transsynaptic retrograde tracing in mice

Schneider

Chaudy

Epstein

et al. 2020

J of Comparative Neurology

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A wide range of evidence indicates that olfactory perception is strongly involved in food intake. However, the polysynaptic circuitry linking the brain areas involved in feeding behavior to the olfactory regions is not well known. The aim of this article was to examine such circuits. Thus, we described, using hodological tools such as transsynaptic viruses (PRV152) transported in a retrograde manner, the long-distance indirect projections (two to three synapses) onto the main olfactory bulb (MOB). The ß-subunit of the cholera toxin which is a monosynaptic retrograde tracer was used as a control to be able to differentiate between direct and indirect projections. Our tracing experiments showed that the arcuate nucleus of the hypothalamus, as a major site for regulation of food intake, sends only very indirect projections onto the MOB. Indirect projections to MOB also originate from the solitary nucleus which is involved in energy homeostasis. Other indirect projections have been evidenced in areas of the reward circuit such as VTA and accumbens nucleus. In contrast, direct projections to the MOB arise from melaninconcentrating hormone and orexin neurons in the lateral hypothalamus. Functional significances of these projections are discussed in relation to the role of food odors in feeding and reward-related behavior.Abbreviations: 3V, third ventricle; 4V, fourth ventricle; Acb, accumbens nucleus; ACo, anterior cortical amygdaloid area; AHi, amygdalohippocampal area; AHiPM, amygdalohippocampal area, posteromedial part; AID, agranular insular cortex, dorsal part; AIP, agranular insular cortex, posterior part; AIV, agranular insular cortex, ventral part; AON, anterior olfactory nucleus; aPir, piriform cortex anterior part; Arc, arcuate hypothalamic nucleus; Au1, primary auditory cortex; AuD, secondary auditory cortex, dorsal area; AuV, secondary auditory cortex, ventral area; BLA, basolateral amygdaloid nucleus, anterior part; BLP, basolateral amygdaloid nucleus, posterior part; BMA, basomedial amygdaloid nucleus, anterior part; BMP, basomedial amygdaloid nucleus, posterior part; CA1, field CA1 of the hippocampus; CA2, field CA2 of the hippocampus; CA3, field CA3 of the hippocampus; Ce, central amygdaloid

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“…Besides, although the innervation from the ventral HIP to the PC has rarely been studied, perhaps this is due to the low infection efficiency of the traditional tracers and the difficulty to distinguish the axon terminal with pass-by fibers in axons tracing studies. The ventral HIP has been found to innervate strongly to the AON and modulate olfactory sensitivity (Aqrabawi et al, 2016). In addition, the LEC, ventral HIP and AMY are all known to be susceptible to seizures (Mohapel et al, 1996;Vismer et al, 2015;Bui et al, 2018), and all of them connect closely with the PPC, implying that the PPC may be one of the key nodes for seizure spreading (Vismer et al, 2015).…”

Section: Input Patterns To Distinct Subareas Of the Pcmentioning

confidence: 99%

Cell-Type-Specific Whole-Brain Direct Inputs to the Anterior and Posterior Piriform Cortex

Wang

Zhang

Chen

et al. 2020

Front. Neural Circuits

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The piriform cortex (PC) is a key brain area involved in both processing and coding of olfactory information. It is implicated in various brain disorders, such as epilepsy, Alzheimer's disease, and autism. The PC consists of the anterior (APC) and posterior (PPC) parts, which are different anatomically and functionally. However, the direct input networks to specific neuronal populations within the APC and PPC remain poorly understood. Here, we mapped the whole-brain direct inputs to the two major neuronal populations, the excitatory glutamatergic principal neurons and inhibitory γ-aminobutyric acid (GABA)-ergic interneurons within the APC and PPC using the rabies virus (RV)mediated retrograde trans-synaptic tracing system. We found that for both types of neurons, APC and PPC share some similarities in input networks, with dominant inputs originating from the olfactory region (OLF), followed by the cortical subplate (CTXsp), isocortex, cerebral nuclei (CNU), hippocampal formation (HPF) and interbrain (IB), whereas the midbrain (MB) and hindbrain (HB) were rarely labeled. However, APC and PPC also show distinct features in their input distribution patterns. For both types of neurons, the input proportion from the OLF to the APC was higher than that to the PPC; while the PPC received higher proportions of inputs from the HPF and CNU than the APC did. Overall, our results revealed the direct input networks of both excitatory and inhibitory neuronal populations of different PC subareas, providing a structural basis to analyze the diverse PC functions.

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Top-down modulation of olfactory-guided behaviours by the anterior olfactory nucleus pars medialis and ventral hippocampus

Cited by 53 publications

References 29 publications

Dynamic inhibition of sensory responses mediated by an olfactory corticofugal system

Dynamic inhibition of sensory responses mediated by an olfactory corticofugal system

Centrifugal projections to the main olfactory bulb revealed by transsynaptic retrograde tracing in mice

Cell-Type-Specific Whole-Brain Direct Inputs to the Anterior and Posterior Piriform Cortex

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