Odor coding in piriform cortex: mechanistic insights into distributed coding

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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Strategies for Odor Coding in the Piriform Cortex

Journal of Neuroscience ◽

10.1523/jneurosci.5593-06.2007 ◽

2007 ◽

Vol 27 (6) ◽

pp. 1237-1238

Author(s):

J. H. Brann ◽

S. R. Saideman ◽

M. T. Valley ◽

D. Wiedl

Keyword(s):

Piriform Cortex ◽

Odor Coding

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

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1620939114 ◽

2017 ◽

Vol 114 (9) ◽

pp. 2407-2412 ◽

Cited By ~ 20

Author(s):

Malinda L. S. Tantirigama ◽

Helena H.-Y. Huang ◽

John M. Bekkers

Keyword(s):

Olfactory Bulb ◽

Spontaneous Activity ◽

Dynamic Range ◽

Piriform Cortex ◽

Spontaneous Firing ◽

Odor Coding ◽

Layer 2 ◽

Olfactory Stimuli ◽

External Stimuli ◽

Odor Representation

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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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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Coding of odor stimulus features among secondary olfactory structures

Journal of Neurophysiology ◽

10.1152/jn.00902.2014 ◽

2015 ◽

Vol 114 (1) ◽

pp. 736-745 ◽

Cited By ~ 6

Author(s):

Christina Z. Xia ◽

Stacey Adjei ◽

Daniel W. Wesson

Keyword(s):

Olfactory System ◽

Piriform Cortex ◽

Odor Stimulus ◽

Odor Perception ◽

Odor Coding ◽

Network Function ◽

Complex Functions ◽

Odor Exposure ◽

Stimulus Features ◽

The Brain

Sensory systems must represent stimuli in manners dependent upon a wealth of factors, including stimulus intensity and duration. One way the brain might handle these complex functions is to assign the tasks throughout distributed nodes, each contributing to information processing. We sought to explore this important aspect of sensory network function in the mammalian olfactory system, wherein the intensity and duration of odor exposure are critical contributors to odor perception. This is a quintessential model for exploring processing schemes given the distribution of odor information by olfactory bulb mitral and tufted cells into several anatomically distinct secondary processing stages, including the piriform cortex (PCX) and olfactory tubercle (OT), whose unique contributions to odor coding are unresolved. We explored the coding of PCX and OT neuron responses to odor intensity and duration. We found that both structures similarly partake in representing descending intensities of odors by reduced recruitment and modulation of neurons. Additionally, while neurons in the OT adapt to odor exposure, they display reduced capacity to adapt to either repeated presentations of odor or a single prolonged odor presentation compared with neurons in the PCX. These results provide insights into manners whereby secondary olfactory structures may, at least in some cases, uniquely represent stimulus features.

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Robust odor coding across states in piriform cortex requires recurrent circuitry: evidence for pattern completion in an associative network

10.1101/694331 ◽

2019 ◽

Author(s):

Kevin A. Bolding ◽

Shivathmihai Nagappan ◽

Bao-Xia Han ◽

Fan Wang ◽

Kevin M. Franks

Keyword(s):

Neural Activity ◽

Neural Circuits ◽

Activity Patterns ◽

Piriform Cortex ◽

Network Models ◽

Theoretical Studies ◽

Odor Coding ◽

Pattern Completion ◽

Attractor Dynamics ◽

Cortical Circuit

AbstractPattern completion, or the ability to retrieve stable neural activity patterns from noisy or partial cues, is a fundamental feature of memory. Theoretical studies indicate that recurrently connected auto-associative or discrete attractor network models can perform this process. Although phenomenological evidence for pattern completion and attractor dynamics have been described in various recurrent neural circuits, the crucial role that recurrent circuitry plays in implementing these processes has not been shown. Here we show that although odor representations in mouse olfactory bulb degrade under anesthesia, responses in downstream piriform cortex remain robust. Recurrent connections are required to stabilize cortical odor representations across states. Moreover, piriform odor representations exhibit attractor dynamics, both within and across trials, and these are also abolished when recurrent circuitry is eliminated. Thus, an auto-associative cortical circuit stabilizes output in response to degraded input, and the recurrent circuitry that defines these networks is required for this stabilization.

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