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

Stern, Merav; Bolding, Kevin A.; Abbott, L. F.; Franks, Kevin M.

doi:10.7554/elife.34831

Cited by 55 publications

(45 citation statements)

References 85 publications

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“…Odor information is then diffusely projected from OB to PCx, so that individual PCx neurons can integrate inputs from different combinations of OB glomeruli, producing odor-specific ensembles of neurons distributed across PCx whose concerted activity encodes odor identity (16)(17)(18)(19)(20). Theoretical studies have suggested that PCx can form concentration-invariant odor representations by selectively responding to the earliest-active OB inputs while ignoring the contribution of inputs arriving later, which may reflect more spurious activation of lower-affinity receptors (21)(22)(23). However, whether this occurs, and how such a temporal filter would be implemented within PCx, are not known.…”

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confidence: 99%

Recurrent cortical circuits implement concentration-invariant odor coding

Bolding

Franks

2018

Preprint

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122

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Although the ability to reliably identify objects over a large range of stimulus intensities is a fundamental feature of all sensory systems, the neural circuit mechanisms that implement intensity invariance remain poorly understood. In mammals, odors are detected by individual olfactory sensory neurons expressing just one out of ~1,000 different types of odorant receptor, each of which projects to a specific pair of glomeruli in the olfactory bulb (OB). At low concentrations, odorants selectively bind high-affinity receptors, activating a sparse combination of responsive glomeruli. However, receptor activation, and thus glomerular activation, becomes less specific at higher odorant concentrations (1-4), potentially degrading the representation of odor identity. However, psychophysical studies indicate that odors retain their perceptual identities while concentration varies over several orders of magnitude (5-7). The olfactory system must therefore transform these concentration-dependent odor responses at early stages of processing into concentration-invariant representations of odor identity.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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confidence: 99%

Recurrent cortical circuits implement concentration-invariant odor coding

Bolding

Franks

2018

Preprint

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122

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“…This sheds new light on how the 'multiplexed representation of odor concentration and identity' (Stern et al 2018) in aPCx can be explained by cell-type specific differences in dendritic integration.…”

Section: Discussionmentioning

confidence: 83%

“…In contrast, identity coding/concentration invariant neurons display uniform short onset latencies of the spiking response. This early onset population also contains the relevant information on odor identity (Roland et al 2017;Bolding et al 2017;Stern et al 2018). When considering our model, the larger range of onset delays in nonlinearly integrating layer 2a neurons suggests that they could constitute the population of concentration variant neurons.…”

Section: Functional Implications Of Differences Between Layer 2a and mentioning

confidence: 96%

“…The time course of this intrinsic parameter approximates hyperpolarizing synaptic input from feedback interneurons that terminates neuronal hyperpolarization in the aPCx (Stern et al 2018).…”

Section: Modellingmentioning

confidence: 99%

“…The nonlinear dendritic integration behavior of non-linear IFB neurons is captured by incorporating a membrane potential-dependent conductance for the synaptic current. Odor intensity is relayed by shifts of response latencies in the olfactory bulb population output (Stern et al 2018). We know there is a fixed time interval in which aPCx principal neurons are responsive to excitatory bulb input before inhibition dominates.…”

Section: Functional Consequences Of Differences In Nonlinear Integratmentioning

confidence: 99%

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Circuit-specific dendritic development in the piriform cortex

Moreno-Velasquez

Kaehne

et al. 2019

Preprint

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Dendritic geometry is largely determined during postnatal development and has a substantial impact on neural function. In sensory processing, postnatal development of the dendritic tree is affected by two dominant circuit motifs, ascending sensory feedforward inputs and descending and local recurrent connections. Two subtypes of layer 2 neurons in the three-layered anterior piriform cortex, layer 2a and layer 2b neurons, display a clear vertical segregation of these two circuit motifs. Here, we combined electrophysiology, detailed morphometry and Ca 2+ imaging -both of neuronal networks as well as of subcellular structures-in acute mouse brain slices and modeling. This allowed us to compare the functional implications of distinct circuit-specific postnatal dendritic growth patterns in these two neuronal subtypes. We observed that determination of branching complexity, dendritic length increases and pruning occurred in distinct growth phases. Layer 2a and layer 2b neurons displayed growth phase specific developmental differences between their apical and basal dendritic trees. This was reflected by compartment-specific differences in Ca 2+ signaling. The morphological and functional developmental pattern differences between layer 2a and layer 2b neurons dendrites provide further evidence that they constitute two functionally distinct streams of olfactory information processing. Materials and Methods Slice preparationAcute brain slices were prepared from C57Bl6N mice except for population Ca 2+ imaging experiments with GCaMP (Fig. 4), where Ai95-NexCre mice were used. In experiments for Figs. 1-6, the horizontal slicing orientation was chosen because it best preserves rostrocaudal association fibers (Demir et al. 2001). For dendritic spike measurements in Fig. 7, we used coronal slices. All procedures were in accordance with the national and institutional guidelines and approved by the local health authority and the local ethics committee (Landesamt für Gesundheit und Soziales, Berlin; animal license number T100/03). For electrophysiological characterization and morphological reconstruction, acute brain slices were prepared at 4 age intervals: p1-2, p6-8, p12-14 and p30-40. For measurements of NMDA-spikes, coronal slices were prepared at p14-21. Brains from p30-40 mice and from mice used for dendritic spike measurements were prepared in ice-cold artificial cerebrospinal fluid (ACSF; pH 7.4) containing (in mM): 87 NaCl, 26 NaHCO3, 10 Glucose, 2.5 KCl, 3 MgCl2, 1.25 NaH2PO4, 0.5 CaCl2 and 50 sucrose. Slices were cut at 400 µm thickness, and incubated at 35°C for 30 min. The slices were then transferred to standard ACSF containing (in mM): 119 NaCl, 26 NaHCO3, 10 Glucose, 2.5 KCl, 2.5 CaCl2, 1.3 MgCl2, and 1 NaH2PO4. Slices from other age groups were cut in ice-cold standard ACSF and incubated for 30 min in standard ACSF at 35°C. The slices were then stored in standard ACSF at room temperature in a submerged chamber for 0.5-6 h before being transferred to the recording chamber. For dendritic spike measurements in Fig. ...

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Introduction: How Should One Think About Nervous Systems?

Traub,

Draguhn

2024

Brain Leitmotifs

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

Cited by 55 publications

References 85 publications

Recurrent cortical circuits implement concentration-invariant odor coding

Recurrent cortical circuits implement concentration-invariant odor coding

Circuit-specific dendritic development in the piriform cortex

Introduction: How Should One Think About Nervous Systems?

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