Target‐specific control of piriform cortical output via distinct inhibitory circuits

Jiang, Hehai; Guo, Anni; Chiu, Arthur; Li, Huanhuan; Lai, Cora Sau Wan; Lau, C. Geoffrey

doi:10.1096/fj.202100757r

Cited by 5 publications

(14 citation statements)

References 45 publications

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“…The age difference may affect the plasticity of synapse after NO. Furthermore, NO selectively enhanced PV, but not SST, inhibitory conductance ( Jiang et al, 2021 ). These results are consistent with our present study, where NO induced selective plasticity in PV but not SST neuron.…”

Section: Discussionmentioning

confidence: 99%

“…One limitation of our study is that synaptic protein expression indicates only structural but not functional change. Our group has recently shown that NO increased the conductance of spontaneous and evoked IPSCs in a subtype of principal neuron in APC ( Jiang et al, 2021 ). However, our current study shows that density of inhibitory synapses, especially PV + synapses, are decreased after NO.…”

Section: Discussionmentioning

confidence: 99%

“…Therefore, TNF-α modulates the relative contribution of excitatory and inhibitory synaptic transmission and plays a critical role in balancing excitation-inhibition (E-I) of neural circuits. Olfactory experience can regulate excitatory and inhibitory transmission in the APC ( Best and Wilson, 2003 ; Quinlan et al, 2004 ; Kim et al, 2006 ; Poo and Isaacson, 2007 ; Jiang et al, 2021 ). However, the role of TNF-α in regulating E-I ratio in APC is unexplored.…”

Section: Introductionmentioning

confidence: 99%

“…PV and SST neurons play different roles in regulating principal neuron activity as they impart perisomatic and dendritic inhibition, respectively. We recently showed that olfactory experience selectively regulates PV but not SST inhibition ( Jiang et al, 2021 ). However, it is unclear whether their plasticity is regulated by soluble signaling molecules.…”

Section: Introductionmentioning

confidence: 99%

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TNF-α Orchestrates Experience-Dependent Plasticity of Excitatory and Inhibitory Synapses in the Anterior Piriform Cortex

Guo

Lau

2022

Front. Neurosci.

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Homeostatic synaptic plasticity, which induces compensatory modulation of synapses, plays a critical role in maintaining neuronal circuit function in response to changing activity patterns. Activity in the anterior piriform cortex (APC) is largely driven by ipsilateral neural activity from the olfactory bulb and is a suitable system for examining the effects of sensory experience on cortical circuits. Pro-inflammatory cytokine tumor necrosis factor-α (TNF-α) can modulate excitatory and inhibitory synapses, but its role in APC is unexplored. Here we examined the role of TNF-α in adjusting synapses in the mouse APC after experience deprivation via unilateral naris occlusion. Immunofluorescent staining revealed that activity deprivation increased excitatory, and decreased inhibitory, synaptic density in wild-type mice, consistent with homeostatic regulation. Quantitative RT-PCR showed that naris occlusion increased the expression of Tnf mRNA in APC. Critically, occlusion-induced plasticity of excitatory and inhibitory synapses was completely blocked in the Tnf knockout mouse. Together, these results show that TNF-α is an important orchestrator of experience-dependent plasticity in the APC.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

TNF-α Orchestrates Experience-Dependent Plasticity of Excitatory and Inhibitory Synapses in the Anterior Piriform Cortex

Guo

Lau

2022

Front. Neurosci.

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“…The layer 2 (L2) of APC contains a dense region of principal neurons (semilunar, SL, and superficial pyramidal, SP) that form the major output of APC projecting to downstream areas, such as the entorhinal and orbitofrontal cortex and mediodorsal thalamus [ 17 ]. Our group and others have shown that SL and SP neurons form two distinct circuits for representing information in the APC [ 18 , 19 , 20 , 21 , 22 ]. Since the APC sends feedback projections to OB to modulate neural representation and learning [ 23 , 24 ], regulation of SL and SP neuronal output will significantly impact activity in APC as well as OB.…”

Section: Introductionmentioning

confidence: 99%

Acute Fasting Modulates Food-Seeking Behavior and Neural Signaling in the Piriform Cortex

Ngo

Zhang

et al. 2022

Nutrients

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It is well known that the state of hunger can modulate hormones and hypothalamic neural circuits to drive food-seeking behavior and consumption. However, the role the sensory cortex plays in regulating foraging is much less explored. Here, we investigated whether acute fasting in mice can alter an odor-guided foraging behavior and how it can alter neurons and synapses in the (olfactory) piriform cortex (PC). Acute hunger enhances the motivation of a mouse to search for food pellets and increases food intake. The foraging behavior strongly activates the PC, as revealed by c-Fos immunostaining. The activation of PC is accompanied by an increase in excitation–inhibition ratio of synaptic density. Fasting also enhances the phosphorylation of AMP kinase, a biochemical energy regulator. Taken together, our results uncover a new regulatory brain region and implicate the PC in controlling foraging behavior.

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Suppression of piriform cortex alters brain-wide dynamics and alleviates seizures in temporal lobe epilepsy

Zhang,

Chiu,

Jiang

et al. 2023

Preprint

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Temporal lobe epilepsy (TLE) is a pathological state that involves altered excitation-inhibition (E-I) in the brain and exhibits recurrent seizures. Many circuit studies of TLE have focused on the hippocampus. Anterior piriform cortex (APC) is also a limbic area closely associated with TLE, but is understudied. In the APC, parvalbumin-expressing (PV+) interneurons provide strong inhibition and help maintain E-I balance. However, whether APCPVneurons play a causal role in TLE is unclear.We used the systemic pilocarpine and intrahippocampal kainic acid (KA) mouse models, which showed pathological changes and spontaneous recurrent seizures (SRSs) akin to those observed in patients with TLE. Whole-cell patch clamp recording and immunohistochemistry were used to examine inhibitory synaptic transmission in the pilocarpine model. Then, using chemogenetics and multi-site local field potential (LFP) recording, we manipulated APCPVneurons at different periods, before applying convulsant, during status epilepticus (SE) and in chronic epileptic phase, and examined the efficacy of APCPVneuronal activation on seizures. For chronic period experiments, KA-injected mice underwent four-site longitudinal LFP recordings. We quantified SRSs based on the frequency and duration of epileptic discharges (> 2 Hz, 10 seconds). For the underlying functional network dynamics, we analyzed the power of each recording site and functional connectivity of each pair of regions in four epileptic states, preictal, ictal, postictal and interictal.In the pilocarpine model, we found impaired synaptic inhibition and loss of PV synapses in the APC. APCPVneuronal pre-activation decreased seizure susceptibility and mortality, but could not stop an ongoing SE. In the chronic KA model, activation of APCPVneurons reduced the frequency and duration of SRSs in the hippocampus. Interestingly, APCPVneuronal activation altered the brain-wide dynamics of seizure network and afforded differential modulation based on epileptic states, brain regions and frequency bands.Our work demonstrates the causal role of APCPVin TLE and provides detailed functional characterization of mechanisms underlying the effectiveness of APCPVactivation. We reveal how a cortical microcircuit can alter neural activity in multiple brain regions and exert antiepileptic benefits. These findings strengthen the idea that large-scale connections from APC play a key role in maintaining the E-I balance of the entire seizure network and thus provide the basis for future circuit-based therapies.

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Target‐specific control of piriform cortical output via distinct inhibitory circuits

Abstract: This is an open access article under the terms of the Creat ive Commo ns Attri butio n NonCo mmercial License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes.

Cited by 5 publications

References 45 publications

TNF-α Orchestrates Experience-Dependent Plasticity of Excitatory and Inhibitory Synapses in the Anterior Piriform Cortex

TNF-α Orchestrates Experience-Dependent Plasticity of Excitatory and Inhibitory Synapses in the Anterior Piriform Cortex

Acute Fasting Modulates Food-Seeking Behavior and Neural Signaling in the Piriform Cortex

Suppression of piriform cortex alters brain-wide dynamics and alleviates seizures in temporal lobe epilepsy

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