Cortical Feedback Decorrelates Olfactory Bulb Output in Awake Mice

Otazu, Gonzalo H.; Chae, Honggoo; Davis, Michael F.; Albeanu, Dinu F.

doi:10.1016/j.neuron.2015.05.023

Cited by 155 publications

(243 citation statements)

References 76 publications

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“…S4). Two recent reports have described spontaneous calcium transients in boutons on corticobulbar axons in the OB (33,34). Their presence implies that the sources of those axons, SP cells in the anterior PC (42), are also spontaneously active, consistent with our findings.…”

Section: Discussionsupporting

confidence: 92%

“…However, it remains possible that intracortical and descending inputs could contribute to spontaneous activity in the awake state. The anterior PC also sends corticobulbar axons back to the OB (32,33,41), but, again, we found no evidence for the contribution of a reciprocal OB ↔ PC loop in the generation of spontaneous excitation in the PC (Fig. S4).…”

Section: Discussioncontrasting

confidence: 55%

“…S4 B and C). This result suggests that only OB → PC connections are important for spontaneous spiking in the PC and that connections in the reverse direction (PC → OB) are not involved (32)(33)(34).…”

Section: Resultsmentioning

confidence: 91%

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

Tantirigama

Huang

Bekkers

2017

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

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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.T he brain remains intensely active even under conditions when overt external stimuli are absent (1). At first glance this behavior can seem puzzling. Pyramidal neurons in primary sensory neocortex, for example, typically fire spontaneously at approximately 1 Hz when the relevant stimuli are not present (2), raising the possibility that this background activity is noise that must be mitigated by signal averaging (3). On the other hand, spontaneous cortical activity is often structured (4) and can reflect the global state of the animal (5), suggesting that it is not simply an impediment but may serve a useful computational role. Indeed, such activity may be important for gating sensory inputs (4, 6), establishing and maintaining sensory maps (7-9), and extending the dynamic range of sensory-evoked responses (10, 11). The significance of spontaneous activity is also supported by theoretical studies showing that it emerges naturally from balanced neural networks with desirable information-processing characteristics (9, 12).Given that spontaneous spiking is likely to be a key element of cortical function, it is important to study its prevalence and properties in different cortical areas. The piriform cortex (PC) is a sensory paleocortex in mammals that is critical for recognizing and remembering odors (13-17). The PC offers a number of advantages for the study of neural information processing, including a simple trilaminar architecture and well-defined afferent input from the olfactory bulb (OB) (16, 17). As a phylogenetically "old" structure, the PC is also likely to express canonical cortical circuits that have been conserved across evolution (18). Spontaneous spiking has been reported in the PC of rodents breathing odor-free air (19-23), but these studies used unit r...

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Section: Discussionsupporting

confidence: 92%

Section: Discussioncontrasting

confidence: 55%

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

Tantirigama

Huang

Bekkers

2017

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

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“…Anesthesia affects olfactory circuits in nuanced ways that may not be equivalent to simple scaling of responses in individual cells (Kato et al, 2012; Otazu et al, 2015). Therefore, we directly compared the responses of young and mature abGC dendrites in the awake versus the anesthetized state to odor set C (Figures 6A, 6B).…”

Section: Resultsmentioning

confidence: 99%

Development and Refinement of Functional Properties of Adult-Born Neurons

Wallace

Wienisch

Murthy

2017

Neuron

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Summary New neurons appear only in a few regions of the adult mammalian brain and become integrated into existing circuits. Little is known about the functional development of individual neurons in vivo. We examined the functional life history of adult-born granule cells (abGCs) in the olfactory bulb using multiphoton imaging in awake and anesthetized mice. We found that abGCs can become responsive to odorants soon after they arrive in the olfactory bulb. Tracking identified abGCs over weeks revealed that the robust and broadly-tuned responses of most newly arrived abGCs gradually become more selective over a period of ~4 weeks, but a small fraction achieves broader tuning with maturation. Enriching the olfactory environment of mice prolonged the period over which abGCs were strongly and broadly responsive to odorants. Our data offer direct support for rapid integration of adult-born neurons into existing circuits, followed by experience-dependent refinement of their functional connectivity.

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“…We hypothesize that the proximity of centrifugally projecting neurons to each another allows them to interact through local inhibitory connections (Poo and Isaacson, 2009; Suzuki and Bekkers, 2010). By synthesizing the activity of local ensembles of neurons (Zelano et al, 2011), clustered feedback may further sparsen incoming odor representations in the MOB (Otazu et al, 2015). In addition, recent theoretical work has shown that clustered connectivity can give rise to complex temporal patterns of activity on long time scales (Litwin-Kumar and Doiron, 2012).…”

Section: Discussionmentioning

confidence: 99%

Diverse Representations of Olfactory Information in Centrifugal Feedback Projections

Padmanabhan

Osakada

Tarabrina

et al. 2016

Journal of Neuroscience

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Although feedback or centrifugal projections from higher processing centers of the brain to peripheral regions have long been known to play essential functional roles, the anatomical organization of these connections remains largely unknown. Using a virus-based retrograde labeling strategy and 3D whole-brain reconstruction methods, we mapped the spatial organization of centrifugal projections from two olfactory cortical areas, the anterior olfactory nucleus (AON) and the piriform cortex, to the granule cell layer of the main olfactory bulb in the mouse. Both regions are major recipients of information from the bulb and are the largest sources of feedback to the bulb, collectively constituting circuits essential for olfactory coding and olfactory behavior. We found that, although ipsilateral inputs from the AON were uniformly distributed, feedback from the contralateral AON had a strong ventral bias. In addition, we observed that centrifugally projecting neurons were spatially clustered in the piriform cortex, in contrast to the distributed feedforward axonal inputs that these cells receive from the principal neurons of the bulb. Therefore, information carried from the bulb to higher processing structures by anatomically stereotypic projections is likely relayed back to the bulb by organizationally distinct feedback projections that may reflect different coding strategies and therefore different functional roles.

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Cortical Feedback Decorrelates Olfactory Bulb Output in Awake Mice

Cited by 155 publications

References 76 publications

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

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

Development and Refinement of Functional Properties of Adult-Born Neurons

Diverse Representations of Olfactory Information in Centrifugal Feedback Projections

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