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

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.

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Recurrent cortical circuits implement concentration-invariant odor coding

Science ◽

10.1126/science.aat6904 ◽

2018 ◽

Vol 361 (6407) ◽

pp. eaat6904 ◽

Cited By ~ 39

Author(s):

Kevin A. Bolding ◽

Kevin M. Franks

Keyword(s):

Olfactory Bulb ◽

Concentration Dependence ◽

Neural Circuit ◽

Feedback Inhibition ◽

Piriform Cortex ◽

Cortical Activity ◽

Cortical Circuits ◽

Odor Coding ◽

Recurrent Collateral ◽

The Impact

Animals rely on olfaction to find food, attract mates, and avoid predators. To support these behaviors, they must be able to identify odors across different odorant concentrations. The neural circuit operations that implement this concentration invariance remain unclear. We found that despite concentration-dependence in the olfactory bulb (OB), representations of odor identity were preserved downstream, in the piriform cortex (PCx). The OB cells responding earliest after inhalation drove robust responses in sparse subsets of PCx neurons. Recurrent collateral connections broadcast their activation across the PCx, recruiting global feedback inhibition that rapidly truncated and suppressed cortical activity for the remainder of the sniff, discounting the impact of slower, concentration-dependent OB inputs. Eliminating recurrent collateral output amplified PCx odor responses rendered the cortex steeply concentration-dependent and abolished concentration-invariant identity decoding.

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Context-driven activation of odor representations in the absence of olfactory stimuli in the olfactory bulb and piriform cortex

Frontiers in Behavioral Neuroscience ◽

10.3389/fnbeh.2014.00138 ◽

2014 ◽

Vol 8 ◽

Cited By ~ 16

Author(s):

Nathalie Mandairon ◽

Florence Kermen ◽

Caroline Charpentier ◽

Joelle Sacquet ◽

Christiane Linster ◽

...

Keyword(s):

Olfactory Bulb ◽

Piriform Cortex ◽

Olfactory Stimuli

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A transformation from temporal to ensemble coding in a model of piriform cortex

10.1101/118364 ◽

2017 ◽

Cited By ~ 1

Author(s):

Merav Stern ◽

Kevin A. Bolding ◽

L.F. Abbott ◽

Kevin M. Franks

Keyword(s):

Olfactory Bulb ◽

Olfactory System ◽

Feedback Inhibition ◽

Piriform Cortex ◽

Odor Coding ◽

System A ◽

Coding Strategies ◽

Concentration Changes ◽

Recurrent Collateral ◽

The Impact

ABSTRACTDifferent coding strategies are used to represent odor information at various stages of the mammalian olfactory system. A temporal latency code represents odor identity in olfactory bulb (OB), but this temporal information is discarded in piriform cortex (PCx) where odor identity is instead encoded through ensemble membership. We developed a spiking PCx network model to understand how this transformation is implemented. In the model, the impact of OB inputs activated earliest after inhalation is amplified within PCx by diffuse recurrent collateral excitation, which then recruits strong, sustained feedback inhibition that suppresses the impact of later-responding glomeruli. Simultaneous OB-PCx recordings indicate that indeed, over a single sniff, the earliest-active OB inputs are most effective at driving PCx activity. We model increasing odor concentrations by decreasing glomerulus onset latencies while preserving their activation sequences. This produces a multiplexed cortical odor code in which activated ensembles are robust to concentration changes while concentration information is encoded through population synchrony. Our model demonstrates how PCx circuitry can implement multiplexed ensemble-identity/temporal-concentration odor coding.

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Recurrent cortical circuits implement concentration-invariant odor coding

10.1101/294132 ◽

2018 ◽

Cited By ~ 4

Author(s):

Kevin A. Bolding ◽

Kevin M. Franks

Keyword(s):

Olfactory Bulb ◽

Concentration Dependence ◽

Neural Circuit ◽

Feedback Inhibition ◽

Piriform Cortex ◽

Cortical Activity ◽

Cortical Circuits ◽

Odor Coding ◽

Recurrent Collateral ◽

The Impact

Animals rely on olfaction to find food, attract mates and avoid predators. To support these behaviors, animals must reliably identify odors across different odorant concentrations. The neural circuit operations that implement this concentration invariance remain unclear. Here we demonstrate that, despite concentration-dependence in olfactory bulb (OB), representations of odor identity are preserved downstream, in piriform cortex (PCx). The OB cells responding earliest after inhalation drive robust responses in a sparse subset of PCx neurons. Recurrent collateral connections broadcast their activation across PCx, recruiting strong, global feedback inhibition that rapidly suppresses cortical activity for the remainder of the sniff, thereby discounting the impact of slower, concentration-dependent OB inputs. Eliminating recurrent collateral output dramatically amplifies PCx odor responses, renders cortex steeply concentration-dependent, and abolishes concentration-invariant identity decoding.

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Specific contribution of neurons from the Dbx1 lineage to the piriform cortex

Scientific Reports ◽

10.1038/s41598-021-86512-8 ◽

2021 ◽

Vol 11 (1) ◽

Author(s):

Thando Shabangu ◽

Hung-Lun Chen ◽

Zi-hui Zhuang ◽

Alessandra Pierani ◽

Chien-Fu F. Chen ◽

...

Keyword(s):

Olfactory Bulb ◽

Orbitofrontal Cortex ◽

Piriform Cortex ◽

Neural Progenitors ◽

Developmental Origins ◽

Cortical Processing ◽

Neuron Development ◽

Layer 2 ◽

Specific Association ◽

Specific Contribution

AbstractThe piriform cortex (PC) is a major cortical processing center for the sense of smell that receives direct inputs from the olfactory bulb. In mice, the PC consists of three neuronal layers, which are populated by cells with distinct developmental origins. One origin of PC neurons is the pool of Dbx1-expressing neural progenitors located in the ventral pallium at the pallial-subpallial boundary. Since the precise mechanisms of PC neuron development are largely unknown, we sought to define the distribution, timing of neurogenesis, morphology and projection patterns of PC neurons from the Dbx1 lineage. We found that Dbx1-lineage neurons are preferentially distributed in layer 2 and enriched in the ventral portion of the PC. Further, Dbx1 neurons are early-born neurons and contribute to most neuronal subtypes in the PC. Our data also revealed an enrichment of Dbx1-lineage neurons in the ventral anterior PC that project to the orbitofrontal cortex. These findings suggest a specific association between the developmental origin of PC neurons and their neuronal properties.

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A transformation from temporal to ensemble coding in a model of piriform cortex

eLife ◽

10.7554/elife.34831 ◽

2018 ◽

Vol 7 ◽

Cited By ~ 10

Author(s):

Merav Stern ◽

Kevin A Bolding ◽

LF Abbott ◽

Kevin M Franks

Keyword(s):

Olfactory Bulb ◽

Olfactory System ◽

Feedback Inhibition ◽

Piriform Cortex ◽

Odor Coding ◽

System A ◽

Coding Strategies ◽

Concentration Changes ◽

Recurrent Collateral ◽

The Impact

Different coding strategies are used to represent odor information at various stages of the mammalian olfactory system. A temporal latency code represents odor identity in olfactory bulb (OB), but this temporal information is discarded in piriform cortex (PCx) where odor identity is instead encoded through ensemble membership. We developed a spiking PCx network model to understand how this transformation is implemented. In the model, the impact of OB inputs activated earliest after inhalation is amplified within PCx by diffuse recurrent collateral excitation, which then recruits strong, sustained feedback inhibition that suppresses the impact of later-responding glomeruli. We model increasing odor concentrations by decreasing glomerulus onset latencies while preserving their activation sequences. This produces a multiplexed cortical odor code in which activated ensembles are robust to concentration changes while concentration information is encoded through population synchrony. Our model demonstrates how PCx circuitry can implement multiplexed ensemble-identity/temporal-concentration odor coding.

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Specific Contribution of Neurons From the Dbx1 Lineage to The Piriform Cortex

10.21203/rs.3.rs-126014/v1 ◽

2020 ◽

Author(s):

Thando Shabangu ◽

Hung-Lun Chen ◽

Zi-hui Zhuang ◽

Alessandra Pierani ◽

Chien-Fu Chen ◽

...

Keyword(s):

Olfactory Bulb ◽

Orbitofrontal Cortex ◽

Piriform Cortex ◽

Neural Progenitors ◽

Developmental Origins ◽

Cortical Processing ◽

Neuron Development ◽

Layer 2 ◽

Specific Association ◽

Specific Contribution

Abstract The piriform cortex (PC) is a major cortical processing center for the sense of smell that receives direct inputs from the olfactory bulb. In mice, the PC consists of three neuronal layers, which are populated by cells with distinct developmental origins. One of developmental origins of PC is the Dbx1-expressing neural progenitors located in the ventral pallium at the pallial-subpallial boundary. Since the precise mechanisms of PC neuron development are largely unknown, we sought to define the distribution, timing of neurogenesis, morphology and projection patterns of PC neurons from the Dbx1 lineage. We found that Dbx1-lineage neurons are preferentially distributed in layer 2 and enriched in the ventral portion of the PC. Further, Dbx1 neurons are early-born neurons that contribute to most neuronal subtypes in the PC. Our data also revealed an enrichment of Dbx1-lineage neurons located in the ventral anterior PC that project to the orbitofrontal cortex. These findings suggest a specific association between developmental origin of PC neurons and their neuronal properties.

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