GABAergic Circuits Control Input–Spike Coupling in the Piriform Cortex

Luna, Victor M.; Schoppa, Nathan E.

doi:10.1523/jneurosci.2385-08.2008

Cited by 95 publications

(131 citation statements)

References 31 publications

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“…Downstream neurons may be sensitive to coincident inputs due to short membrane time constants, high firing thresholds, or feedback inhibition. For these neurons (e.g., pyramidal cells in olfactory cortex) (46,47) increased correlation of input spike trains increases propagation efficacy.…”

Section: Discussionmentioning

confidence: 99%

Timescale-dependent shaping of correlation by olfactory bulb lateral inhibition

Giridhar

Doiron

Urban

2011

Proc. Natl. Acad. Sci. U.S.A.

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Neurons respond to sensory stimuli by altering the rate and temporal pattern of action potentials. These spike trains both encode and propagate information that guides behavior. Local inhibitory networks can affect the information encoded and propagated by neurons by altering correlations between different spike trains. Correlations introduce redundancy that can reduce encoding but also facilitate propagation of activity to downstream targets. Given this trade-off, how can networks maximize both encoding and propagation efficacy? Here, we examine this problem by measuring the effects of olfactory bulb inhibition on the pairwise statistics of mitral cell spiking. We evoked spiking activity in the olfactory bulb in vitro and measured how lateral inhibition shapes correlations across timescales. We show that inhibitory circuits simultaneously increase fast correlation (i.e., synchrony increases) and decrease slow correlation (i.e., firing rates become less similar). Further, we use computational models to show the benefits of fast correlation/slow decorrelation in the context of odor coding. Olfactory bulb inhibition enhances population-level discrimination of similar inputs, while improving propagation of mitral cell activity to cortex. Our findings represent a targeted strategy by which a network can optimize the correlation structure of its output in a dynamic, activity-dependent manner. This trade-off is not specific to the olfactory system, but rather our work highlights mechanisms by which neurons can simultaneously accomplish multiple, and sometimes competing, aspects of sensory processing.

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Section: Discussionmentioning

confidence: 99%

Timescale-dependent shaping of correlation by olfactory bulb lateral inhibition

Giridhar

Doiron

Urban

2011

Proc. Natl. Acad. Sci. U.S.A.

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“…These postsynaptic bursts have been observed with sensory and associative inputs to layer 2/3 pyramidal cells in the piriform cortex in vitro (Suzuki and Bekkers, 2006) and in vivo (Wilson, 1998). However, isolated layer 1a stimulation has been shown recently to recruit prominent perisomatic feedforward inhibition, and single APs are the predominant cellular output during suprathreshold extracellular stimulation in layer 1a (Luna and Schoppa, 2008). We asked how this tightly controlled output mode affects the integration of presynaptic and postsynaptic firing in layer 1b spines.…”

Section: Calcium Transients Measured During Subsequent Presynaptic Acmentioning

confidence: 94%

“…The output mode is regulated by the balance of excitation and inhibition resulting from synaptic and intrinsic currents. Luna and Schoppa (2008) observed a strong perisomatic inhibitory control exerted by single GABAergic interneurons. One could envision a mechanism in which GABAergic interneurons control the plasticity of excitatory synapses by controlling the output mode of the cell.…”

Section: Functional Implications For Learning In the Piriform Cortex mentioning

confidence: 96%

“…Recently, it has been shown in vitro that selective stimulation of the sensory lateral olfactory tract (LOT) input to layer 1a results in prominent feedforward inhibition, limiting the output mode to single action potentials. A reduction in inhibitory drive turned these single APs into short bursts (Luna and Schoppa, 2008). Bursting and single-spike firing modes of pyramidal cells in the piriform cortex appear tightly controlled by the ratio of excitation (synaptic and intrinsic) to inhibition.…”

Section: Introductionmentioning

confidence: 99%

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Dendritic Compartment and Neuronal Output Mode Determine Pathway-Specific Long-Term Potentiation in the Piriform Cortex

Johenning¹,

Beed²,

Trimbuch³

et al. 2009

J. Neurosci.

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The apical dendrite of layer 2/3 pyramidal cells in the piriform cortex receives two spatially distinct inputs: one projecting onto the distal apical dendrite in sensory layer 1a, the other targeting the proximal apical dendrite in layer 1b. We observe an expression gradient of A-type K ϩ channels that weakens the backpropagating action potential-mediated depolarization in layer 1a compared with layer 1b. We find that the pairing of presynaptic and postsynaptic firing leads to significantly smaller Ca 2ϩ signals in the distal dendritic spines in layer 1a compared with the proximal spines in layer 1b. The consequence is a selective failure to induce long-term potentiation (LTP) in layer 1a, which can be rescued by pharmacological enhancement of action potential backpropagation. In contrast, LTP induction by pairing presynaptic and postsynaptic firing is possible in layer 1b but requires bursting of the postsynaptic cell. This output mode strongly depends on the balance of excitation and inhibition in the piriform cortex. We show, on the single-spine level, how the plasticity of functionally distinct synapses is gated by the intrinsic electrical properties of piriform cortex layer 2 pyramidal cell dendrites and the cellular output mode.

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“…In addition to the potential artifacts caused by anesthesia, it had also been difficult to identify cell types in vivo. Recordings have described very different physiological properties of various types of cortical neurons (Protopapas and Bower, 2000;Luna and Schoppa, 2008;Poo and Isaacson, 2009;Stokes and Isaacson, 2010), suggesting that cell-type information be important for our understanding of circuit mechanisms underlying olfactory signal processing. These confounding factors are eliminated or substantially reduced by the approach of single-cell recording and juxtacellular labeling from head-restrained, awake GAD67-GFP mice.…”

Section: Odor Representation By Functionally Heterogeneous Populationmentioning

confidence: 99%

Diverse Patterns of Odor Representation by Neurons in the Anterior Piriform Cortex of Awake Mice

Zhan¹,

Luo²

2010

J. Neurosci.

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The mammalian piriform cortex receives direct synaptic input from the olfactory bulb and is likely the locus for the formation of odor percept. It remains unclear how individual cortical neurons encode olfactory information in unanesthetized animals. By single-cell recordings from head-restrained awake mice, we studied the odor response profiles of individual neurons in the anterior piriform cortex (aPCX). Neurons were juxtacellularly labeled, and their cell types were determined by their morphology and neurotransmitter phenotypes. We found a considerable level of variability in selectivity patterns among pyramidal neurons (PNs). Approximately one-quarter of PNs were broadly activated by structurally dissimilar odorants, whereas the excitations to the rest of PNs were highly selective. Broad inhibition was only observed from a subpopulation of PNs. GABAergic neurons displayed nonselective excitatory responses to test odorants and rarely exhibited inhibition. In contrast, non-GABAergic nonpyramidal neurons in the deep layer tended to be strongly inhibited by multiple different odorants. Our findings suggest that odor representation is accomplished by both broadly tuned and narrow-tuned PNs in the aPCX of awake animals. In addition, various types of interneurons may play different roles in the intracortical processing of olfactory information.

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GABAergic Circuits Control Input–Spike Coupling in the Piriform Cortex

Cited by 95 publications

References 31 publications

Timescale-dependent shaping of correlation by olfactory bulb lateral inhibition

Timescale-dependent shaping of correlation by olfactory bulb lateral inhibition

Dendritic Compartment and Neuronal Output Mode Determine Pathway-Specific Long-Term Potentiation in the Piriform Cortex

Diverse Patterns of Odor Representation by Neurons in the Anterior Piriform Cortex of Awake Mice

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