scholarly journals Recurrent cortical circuits implement concentration-invariant odor coding

Science ◽  
2018 ◽  
Vol 361 (6407) ◽  
pp. eaat6904 ◽  
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.

scholarly journals Recurrent cortical circuits implement concentration-invariant odor coding

2018 ◽  
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.

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

2017 ◽  
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.

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

eLife ◽  
2018 ◽  
Vol 7 ◽  
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.

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

2017 ◽  
Vol 114 (9) ◽  
pp. 2407-2412 ◽  
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.

scholarly journals Diet-Induced Obesity Disrupts Trace Element Homeostasis and Gene Expression in the Olfactory Bulb

Nutrients ◽  
2020 ◽  
Vol 12 (12) ◽  
pp. 3909
Author(s):  
Melissa S. Totten ◽  
Derek M. Pierce ◽  
Keith M. Erikson
Keyword(s):  
Gene Expression ◽  
Olfactory Bulb ◽  
Trace Element ◽  
Alpha Synuclein ◽  
Divalent Metal Transporter 1 ◽  
Diet Induced Obesity ◽  
Mrna Gene ◽  
The Impact ◽  
Mrna Gene Expression ◽  
Obese Male

The aim of this study was to determine the impact of diet-induced obesity (DIO) on trace element homeostasis and gene expression in the olfactory bulb and to identify potential interaction effects between diet, sex, and strain. Our study is based on evidence that obesity and olfactory bulb impairments are linked to neurodegenerative processes. Briefly, C57BL/6J (B6J) and DBA/2J (D2J) male and female mice were fed either a low-fat diet or a high-fat diet for 16 weeks. Brain tissue was then evaluated for iron, manganese, copper, and zinc concentrations and mRNA gene expression. There was a statistically significant diet-by-sex interaction for iron and a three-way interaction between diet, sex, and strain for zinc in the olfactory bulb. Obese male B6J mice had a striking 75% increase in iron and a 50% increase in manganese compared with the control. There was an increase in zinc due to DIO in B6J males and D2J females, but a decrease in zinc in B6J females and D2J males. Obese male D2J mice had significantly upregulated mRNA gene expression for divalent metal transporter 1, alpha-synuclein, amyloid precursor protein, dopamine receptor D2, and tyrosine hydroxylase. B6J females with DIO had significantly upregulated brain-derived neurotrophic factor expression. Our results demonstrate that DIO has the potential to disrupt trace element homeostasis and mRNA gene expression in the olfactory bulb, with effects that depend on sex and genetics. We found that DIO led to alterations in iron and manganese predominantly in male B6J mice, and gene expression dysregulation mainly in male D2J mice. These results have important implications for health outcomes related to obesity with possible connections to neurodegenerative disease.

GABAA-Mediated IPSCs in Piriform Cortex Have Fast and Slow Components With Different Properties and Locations on Pyramidal Cells

1997 ◽  
Vol 78 (5) ◽  
pp. 2531-2545 ◽  
Author(s):  
A. Kapur ◽  
R. A. Pearce ◽  
W. W. Lytton ◽  
L. B. Haberly
Keyword(s):  
Time Course ◽  
Feedback Inhibition ◽  
Slow Component ◽  
Piriform Cortex ◽  
Pyramidal Cells ◽  
Long Term Potentiation ◽  
Companion Paper ◽  
Protective Role ◽  
Functional Roles ◽  
Term Potentiation

Kapur, A., R. A. Pearce, W. W. Lytton, and L. B. Haberly.GABAA-mediated IPSCs in piriform cortex have fast and slow components with different properties and locations on pyramidal cells. J. Neurophysiol. 78: 2531–2545, 1997. A recent study in piriform (olfactory) cortex provided evidence that, as in hippocampus and neocortex, γ-aminobutyric acid-A (GABAA)-mediated inhibition is generated in dendrites of pyramidal cells, not just in the somatic region as previously believed. This study examines selected properties of GABAA inhibitory postsynaptic currents (IPSCs) in dendritic and somatic regions that could provide insight into their functional roles. Pharmacologically isolated GABAA-mediated IPSCs were studied by whole cell patch recording in slices. To compare properties of IPSCs in distal dendritic and somatic regions, local stimulation was carried out with tungsten microelectrodes, and spatially restricted blockade of GABAA-mediated inhibition was achieved by pressure-ejection of bicuculline from micropipettes. The results revealed that largely independent circuits generate GABAA inhibition in distal apical dendritic and somatic regions. With such independence, a selective decrease in dendritic-region inhibition could enhance integrative or plastic processes in dendrites while allowing feedback inhibition in the somatic region to restrain system excitability. This could allow modulatory fiber systems from the basal forebrain or brain stem, for example, to change the functional state of the cortex by altering the excitability of interneurons that mediate dendritic inhibition without increasing the propensity for regenerative bursting in this highly epileptogenic system. As in hippocampus, GABAA-mediated IPSCs were found to have fast and slow components with time constants of decay on the order of 10 and 40 ms, respectively, at 29°C. Modeling analysis supported physiological evidence that the slow time constant represents a true IPSC component rather than an artifactual slowing of the fast component from voltage clamp of a dendritic current. The results indicated that, whereas both dendritic and somatic-region IPSCs have both fast and slow GABAA components, there is a greater proportion of the slow component in dendrites. In a companion paper, the hypothesis is explored that the resulting slower time course of the dendritic IPSC increases its capacity to regulate the N-methyl-d-aspartate component of EPSPs. Finally, evidence is presented that the slow GABAA-mediated IPSC component is regulated by presynaptic GABAB inhibition whereas the fast is not. Based on the requirement for presynaptic GABAB-mediated block of inhibition for expression of long-term potentiation, this finding is consistent with participation of the slow GABAA component in regulation of synaptic plasticity. The lack of susceptibility of the fast GABAA component to the long-lasting, activity-induced suppression mediated by presynaptic GABAB receptors is consistent with a protective role for this process in preventing seizure activity.

scholarly journals Kappa-opioid receptor-dependent changes in dopamine and affective behavior occur differentially across the nucleus accumbens shell rostro-caudal axis

2020 ◽  
Author(s):  
Breanne E. Pirino ◽  
Mary B. Spodnick ◽  
Andrew T. Gargiulo ◽  
Genevieve R. Curtis ◽  
Jessica R. Barson ◽  
...  
Keyword(s):  
Nucleus Accumbens ◽  
Opioid Receptor ◽  
Dopamine Release ◽  
Neural Circuit ◽  
Ex Vivo ◽  
Kappa Opioid Receptor ◽  
Affective Behavior ◽  
Kappa Opioid ◽  
Affective Behaviors ◽  
The Impact

ABSTRACTNeural circuit engagement within the nucleus accumbens (NAc) shell is implicated in the regulation of both negative and positive affect. Classically, the dynorphin/kappa opioid receptor (KOR) system in the NAc was believed to promote dysphoric behavior, while dopamine was viewed as interacting with reward behavior, and KOR activation was known to inhibit dopamine release. Recently, however, both the KOR and dopamine systems have, separately, been shown to have differential effects across the rostro-caudal axis of the NAc shell on hedonic responses. Whether or not this is due to interactions between KORs and dopamine, and if it extends to other affective behaviors, remains to be determined. In this study, we examined in rats the relationship between the KOR and dopamine systems in both the rostral and caudal NAc shell using ex vivo fast scan cyclic voltammetry and the impact of KOR activation on affective behavior using approach-avoidance assays. We report here that activation of KORs in the caudal NAc shell significantly inhibits dopamine release, stimulates novelty-induced rearing behavior, increases avoidance behavior, and reduces locomotor activity. In contrast, activation of KORs in the rostral NAc shell inhibits dopamine release to a lesser extent and instead increases approach behavior. Taken together, these results indicate that there is heterogeneity across the rostro-caudal axis of the NAc shell in the effects of KOR stimulation on affective behaviors, and they suggest that this might be due to differences in KOR control over dopamine release.

scholarly journals Differential impacts of repeated sampling on odor representations by genetically-defined mitral and tufted cell subpopulations in the mouse olfactory bulb

2020 ◽  
Author(s):  
Thomas P. Eiting ◽  
Matt Wachowiak
Keyword(s):  
Information Processing ◽  
Olfactory Bulb ◽  
High Frequency ◽  
Response Patterns ◽  
Repeated Sampling ◽  
Tufted Cell ◽  
Cell Subpopulations ◽  
Genetic Targeting ◽  
The Impact ◽  
Over Time

AbstractSniffing—the active control of breathing beyond passive respiration—is used by mammals to modulate olfactory sampling. Sniffing allows animals to make odor-guided decisions within ~200 ms, but animals routinely engage in bouts of high-frequency sniffing spanning several seconds; the impact of such repeated odorant sampling on odor representations remains unclear. We investigated this question in the mouse olfactory bulb, where mitral and tufted cells (MTCs) form parallel output streams of odor information processing. To test the impact of repeated odorant sampling on MTC responses, we used two-photon imaging in anesthetized male and female mice to record activation of MTCs while precisely varying inhalation frequency. A combination of genetic targeting and viral expression of GCaMP6 reporters allowed us to access mitral (MC) and superficial tufted cell (sTC) subpopulations separately. We found that repeated odorant sampling differentially affected responses in MCs and sTCs, with MCs showing more diversity than sTCs over the same time period. Impacts of repeated sampling among MCs included both increases and decreases in excitation, as well as changes in response polarity. Response patterns across ensembles of simultaneously-imaged MCs reformatted over time, with representations of different odorants becoming more distinct. MCs also responded differentially to changes in inhalation frequency, whereas sTC responses were more uniform over time and across frequency. Our results support the idea that MCs and TCs comprise functionally distinct pathways for odor information processing, and suggest that the reformatting of MC odor representations by high-frequency sniffing may serve to enhance the discrimination of similar odors.

scholarly journals A dominant role for the beta 4 nicotinic receptor subunit in nicotinic modulation of glomerular microcircuits in the mouse olfactory bulb

2018 ◽  
Vol 120 (4) ◽  
pp. 2036-2048 ◽  
Author(s):  
Michael S. Spindle ◽  
Pirooz V. Parsa ◽  
Spencer G. Bowles ◽  
Rinaldo D. D’Souza ◽  
Sukumar Vijayaraghavan
Keyword(s):  
Olfactory Bulb ◽  
Nicotinic Acetylcholine Receptors ◽  
Information Transfer ◽  
Time Course ◽  
Feedback Inhibition ◽  
Dominant Role ◽  
Receptor Gene ◽  
Gaba Release ◽  
Cell Types ◽  
Receptor Activation

Nicotinic acetylcholine receptors (nAChRs) regulate information transfer across the main olfactory bulb by instituting a high-pass intensity filter allowing for the filtering out of weak inputs. Excitation-driven inhibition of the glomerular microcircuit via GABA release from periglomerular cells appears to underlie this effect of nAChR activation. The multiplicity of nAChR subtypes and cellular locations raises questions about their respective roles in mediating their effects on the glomerular output. In this study, we address this issue by targeting heteromeric nAChRs using receptor knockouts (KOs) for the two dominant nAChR β-subunit genes known to be expressed in the central nervous system. KOs of the β2-nAChR subunit did not affect nAChR currents from mitral cells (MCs) but attenuated those from the external tufted (ET) cells. In slices from these animals, activation of nAChRs still effectively inhibited excitatory postsynaptic currents (EPSCs) and firing on MCs evoked by the olfactory nerve (ON) stimulation, thereby indicating that the filter mechanism was intact. On the other hand, recordings from β4-KOs showed that nAChR responses from MCs were abolished and those from ET cells were attenuated. Excitation-driven feedback was abolished as was the effect of nAChR activation on ON-evoked EPSCs. Experiments using calcium imaging showed that one possible consequence of the β2-subunit activation might be to alter the time course of calcium transients in juxtaglomerular neurons suggesting a role for these receptors in calcium signaling. Our results indicate that nAChRs containing the β4-subunit are critical in the filtering of odor inputs and play a determinant role in the cholinergic modulation of glomerular output. NEW & NOTEWORTHY In this study, using receptor gene knockouts we examine the relative contributions of heteromeric nAChR subtypes located on different cell types to this effect of receptor activation. Our results demonstrate that nAChRs containing the β4-subunit activate MCs resulting in feedback inhibition from glomerular interneurons. This period of inhibition results in the selective filtering of weak odor inputs providing one mechanism by which nAChRs can enhance discrimination between two closely related odors.

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