Olfactory Cortex Generates Synchronized Top-Down Inputs to the Olfactory Bulb during Slow-Wave Sleep

Manabe, Hiroyuki; Kusumoto-Yoshida, Ikue; Ota, Mizuho; Mori, Kensaku

doi:10.1523/jneurosci.6578-10.2011

Cited by 61 publications

(91 citation statements)

References 46 publications

(77 reference statements)

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“…Baclofen suppresses SWS associated sharp wave amplitude Current source density analyses suggest an important role for intracortical association fiber synapses in SWS related sharp waves in piriform cortex (Manabe et al, 2011). To test whether baclofen had an effect on piriform cortical sharp wave activity, we analyzed average sharp wave amplitude during bouts of posttraining SWS in chronically implanted animals.…”

Section: Piriform Cortical Association Fiber Evoked Synaptic Responsementioning

confidence: 99%

“…Both REM and non-REM or slow-wave sleep (SWS) have been implicated in memory consolidation. SWS is characterized by slow oscillations (1-5 Hz) in widespread thalamic and neocortical neurons (Buzsáki, 1996;Steriade, 2006) and coincident sharp-wave ripples in both the hippocampal formation and piriform cortex (Mölle et al, 2006;Manabe et al, 2011). During SWS, sensory cortices are hyporesponsive to external stimuli (Murakami et al, 2005;Issa and Wang, 2011), thus consolidation can occur with limited interference from ongoing events.…”

Section: Introductionmentioning

confidence: 99%

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Slow-Wave Sleep-Imposed Replay Modulates Both Strength and Precision of Memory

2014

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Odor perception is hypothesized to be an experience-dependent process involving the encoding of odor objects by distributed olfactory cortical ensembles. Olfactory cortical neurons coactivated by a specific pattern of odorant evoked input become linked through association fiber synaptic plasticity, creating a template of the familiar odor. In this way, experience and memory play an important role in odor perception and discrimination. In other systems, memory consolidation occurs partially via slow-wave sleep (SWS)-dependent replay of activity patterns originally evoked during waking. SWS is ideal for replay given hyporesponsive sensory systems, and thus reduced interference. Here, using artificial patterns of olfactory bulb stimulation in a fear conditioning procedure in the rat, we tested the effects of imposed post-training replay during SWS and waking on strength and precision of pattern memory. The results show that imposed replay during post-training SWS enhanced the subsequent strength of memory, whereas the identical replay during waking induced extinction. The magnitude of this enhancement was dependent on the timing of imposed replay relative to cortical sharp-waves. Imposed SWS replay of stimuli, which differed from the conditioned stimulus, did not affect conditioned stimulus memory strength but induced generalization of the fear memory to novel artificial patterns. Finally, post-training disruption of piriform cortex intracortical association fiber synapses, hypothesized to be critical for experience-dependent odor coding, also impaired subsequent memory precision but not strength. These results suggest that SWS replay in the olfactory cortex enhances memory consolidation, and that memory precision is dependent on the fidelity of that replay.

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Section: Piriform Cortical Association Fiber Evoked Synaptic Responsementioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Slow-Wave Sleep-Imposed Replay Modulates Both Strength and Precision of Memory

2014

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“…The OB has been suggested to have a specific role in enhancing olfactory discrimination and learning (Shimshek et al 2005;Escanilla et al 2010). Learning-induced changes within the PC seem to not only modify the responses of the cortical neuron directly but also shape subsequent mitral and tufted cell-response patterns (Manabe et al 2011;Markopoulos et al 2012). Understanding of how OB stimulation influences these properties may give insight into the neurobiology of odor memory and perception.…”

Section: Electrical Stimulation Of Ob Enhances Rule Learningmentioning

confidence: 99%

Differential Modifications of Synaptic Weights During Odor Rule Learning: Dynamics of Interaction Between the Piriform Cortex with Lower and Higher Brain Areas

Cohen¹,

Wilson²,

Barkai³

2013

Cerebral Cortex

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Learning of a complex olfactory discrimination (OD) task results in acquisition of rule learning after prolonged training. Previously, we demonstrated enhanced synaptic connectivity between the piriform cortex (PC) and its ascending and descending inputs from the olfactory bulb (OB) and orbitofrontal cortex (OFC) following OD rule learning. Here, using recordings of evoked field postsynaptic potentials in behaving animals, we examined the dynamics by which these synaptic pathways are modified during rule acquisition. We show profound differences in synaptic connectivity modulation between the 2 input sources. During rule acquisition, the ascending synaptic connectivity from the OB to the anterior and posterior PC is simultaneously enhanced. Furthermore, post-training stimulation of the OB enhanced learning rate dramatically. In sharp contrast, the synaptic input in the descending pathway from the OFC was significantly reduced until training completion. Once rule learning was established, the strength of synaptic connectivity in the 2 pathways resumed its pretraining values. We suggest that acquisition of olfactory rule learning requires a transient enhancement of ascending inputs to the PC, synchronized with a parallel decrease in the descending inputs. This combined short-lived modulation enables the PC network to reorganize in a manner that enables it to first acquire and then maintain the rule.

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“…Because of its comparatively simple anatomy, together with the fact that its afferent inputs (i.e., the outputs of the bulb) are increasingly well understood, the PC has attracted attention as a model system for the study of cortical sensory processing (Neville and Haberly, 2004;Isaacson, 2005, 2006;Bekkers, 2006, 2011;Barnes et al, 2008;Luna and Schoppa, 2008;Bathellier et al, 2009;Johenning et al, 2009;Poo and Isaacson, 2009;Stettler and Axel, 2009;Stokes and Isaacson, 2010;Wilson, 2010;Davison and Ehlers, 2011;Franks et al, 2011;Poo and Isaacson, 2011;Wiegand et al, 2011). In particular, synaptic inhibition in the PC is of interest because of its likely relevance to olfactory coding and oscillations (Wilson and Bower, 1992;Kay et al, 2009;Isaacson, 2009, 2011;Kay and Beshel, 2010;Zhan and Luo, 2010;Manabe et al, 2011;Zelano et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

Microcircuits Mediating Feedforward and Feedback Synaptic Inhibition in the Piriform Cortex

Suzuki¹,

Bekkers²

2012

J. Neurosci.

109

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Local inhibition by GABA-releasing neurons is important for the operation of sensory cortices, but the details of these inhibitory circuits remain unclear. We addressed this question in the olfactory system by making targeted recordings from identified classes of inhibitory and glutamatergic neurons in the piriform cortex (PC) of mice. First, we looked for feedforward synaptic inhibition provided by interneurons located in the outermost layer of the PC, layer Ia, which is the unique recipient of afferent fibers from the olfactory bulb. We found two types of feedforward inhibition: a fast-rising, spatially restricted kind that was generated by horizontal cells, and a slow-rising, more diffuse kind generated by neurogliaform cells. Both cell types targeted the distal apical dendrites of layer II principal neurons. Next, we studied feedback synaptic inhibition in isolation by making a tissue cut across layer I to selectively remove feedforward inhibitory connections. We identified a powerful type of feedback inhibition of layer II neurons, mostly generated by soma-targeting fast-spiking multipolar cells in layer III, which in turn were driven by feedforward excitation from layer II semilunar cells. Dynamic clamp simulation of feedback inhibition revealed differential effects of this inhibition on the two main types of layer II principal neurons. Thus, our results articulate the connectivity and functions of two important classes of inhibitory microcircuits in the PC. Feedforward and feedback inhibition generated by these circuits is likely to be required for the operation of this sensory paleocortex during the processing of olfactory information.

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Olfactory Cortex Generates Synchronized Top-Down Inputs to the Olfactory Bulb during Slow-Wave Sleep

Cited by 61 publications

References 46 publications

Slow-Wave Sleep-Imposed Replay Modulates Both Strength and Precision of Memory

Slow-Wave Sleep-Imposed Replay Modulates Both Strength and Precision of Memory

Differential Modifications of Synaptic Weights During Odor Rule Learning: Dynamics of Interaction Between the Piriform Cortex with Lower and Higher Brain Areas

Microcircuits Mediating Feedforward and Feedback Synaptic Inhibition in the Piriform Cortex

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