Spatially segregated feedforward and feedback neurons support differential odor processing in the lateral entorhinal cortex

Leitner, Frauke C.; Melzer, Sarah; Lütcke, Henry; Pinna, Roberta; Seeburg, Peter H.; Helmchen, Fritjof; Monyer, Hannah

doi:10.1038/nn.4303

Cited by 142 publications

(196 citation statements)

References 53 publications

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“…Gradients in odor concentration at the edges of the plume may be efficiently encoded by "on" and "off" responses, whereas a more stable concentration within the plume may be represented by the neurons that exhibit persistent excitation or suppression. Interestingly, a similar diversity of odor-evoked responses was recently reported in the lateral entorhinal cortex (44), suggesting that it may be a general feature of odor-processing circuits.…”

Section: Discussionsupporting

confidence: 71%

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: 71%

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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“…The reported clustering of calbindin-positive neurons is particularly striking in limited parts of MEC and is more striking in mice than in rats or other species. Only in mouse MEC the calbindin-positive neurons are located superficial to the reelin positive neurons (Figure 1A; Tunon et al, 1992; Fujimaru and Kosaka, 1996; Wouterlood, 2002; Ramos-Moreno et al, 2006; Kitamura et al, 2014; Ray et al, 2014; Leitner et al, 2016). EC in humans is known for its wart-like bumps or verrucae (Retzius, 1896; Klinger, 1948; Solodkin and Vanhoesen, 1996; Naumann et al, 2016), which in the largest part of EC, located centrally along the anteroposterior and lateromedial axes, are composed of the large multipolar reelin positive layer II cells, described as the pre-alfa neurons by Braak (Braak and Braak, 1985; Tunon et al, 1992; Kobro-Flatmoen et al, 2016; Naumann et al, 2016).…”

Section: Connectivity Of the Two Entorhinal Subdivisionsmentioning

confidence: 98%

“…In our view, it is therefore confusing to refer to calbindin-positive cells in layer II as island cells embedded in an ocean of reelin-positive cells (Kitamura et al, 2014), since this organization is likely opposite for the larger part of EC. Reelin-positive cells in both entorhinal areas project to the dentate gyrus and CA3, whereas calbindin-positive neurons project to several other targets including the CA1 and the contralateral EC, the olfactory bulb and piriform cortex (Varga et al, 2010; Kitamura et al, 2014; Fuchs et al, 2016; Leitner et al, 2016; Ohara et al, 2016). The two chemically defined cell groups are composed of several morphological subgroups that can be distinguished based on somatic and dendritic features (Canto and Witter, 2012a,b; Fuchs et al, 2016; Leitner et al, 2016).…”

Section: Connectivity Of the Two Entorhinal Subdivisionsmentioning

confidence: 99%

Architecture of the Entorhinal Cortex A Review of Entorhinal Anatomy in Rodents with Some Comparative Notes

Witter

Doan

Jacobsen

et al. 2017

Front. Syst. Neurosci.

303

337

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The entorhinal cortex (EC) is the major input and output structure of the hippocampal formation, forming the nodal point in cortico-hippocampal circuits. Different division schemes including two or many more subdivisions have been proposed, but here we will argue that subdividing EC into two components, the lateral EC (LEC) and medial EC (MEC) might suffice to describe the functional architecture of EC. This subdivision then leads to an anatomical interpretation of the different phenotypes of LEC and MEC. First, we will briefly summarize the cytoarchitectonic differences and differences in hippocampal projection patterns on which the subdivision between LEC and MEC traditionally is based and provide a short comparative perspective. Second, we focus on main differences in cortical connectivity, leading to the conclusion that the apparent differences may well correlate with the functional differences. Cortical connectivity of MEC is features interactions with areas such as the presubiculum, parasubiculum, retrosplenial cortex (RSC) and postrhinal cortex, all areas that are considered to belong to the “spatial processing domain” of the cortex. In contrast, LEC is strongly connected with olfactory areas, insular, medial- and orbitofrontal areas and perirhinal cortex. These areas are likely more involved in processing of object information, attention and motivation. Third, we will compare the intrinsic networks involving principal- and inter-neurons in LEC and MEC. Together, these observations suggest that the different phenotypes of both EC subdivisions likely depend on the combination of intrinsic organization and specific sets of inputs. We further suggest a reappraisal of the notion of EC as a layered input-output structure for the hippocampal formation.

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“…High acetylcholine levels suppress intracortical association fiber synapses (Hasselmo & Bower, 1992). This suppression might shift the relative effectiveness of input to the cortex toward the olfactory bulb (and ongoing odor input from the environment) and away from top-down input from the lateral entorhinal cortex known to be less odor selective (Leitner et al, 2016). During subsequent periods of low arousal or especially during post-training slow-wave sleep, the balance of input effectiveness can then shift away from the nose and back to top-down signals as those synapses are released from suppression.…”

Section: Extended Olfactory Networkmentioning

confidence: 99%

The Olfactory Mosaic: Bringing an Olfactory Network Together for Odor Perception

Courtiol

Wilson

2016

Perception

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Olfactory perception and its underlying neural mechanisms are not fixed, but rather vary over time, dependent on various parameters such as state, task or learning experience. In olfaction, one of the primary sensory areas beyond the olfactory bulb is the piriform cortex. Due to an increasing number of functions attributed to the piriform cortex, it has been argued to be an associative cortex rather than a simple primary sensory cortex. In fact, the piriform cortex plays a key role in creating olfactory percepts, helping form configural odor objects from the molecular features extracted in the nose. Moreover, its dynamic interactions with other olfactory and non-olfactory areas are also critical in shaping the olfactory percept and resulting behavioral responses. In this brief review, we will describe the key role of the piriform cortex in the larger olfactory perceptual network, some of the many actors of this network, and the importance of the dynamic interactions among the piriform-trans-thalamic and limbic pathways.

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Spatially segregated feedforward and feedback neurons support differential odor processing in the lateral entorhinal cortex

Cited by 142 publications

References 53 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

Architecture of the Entorhinal Cortex A Review of Entorhinal Anatomy in Rodents with Some Comparative Notes

The Olfactory Mosaic: Bringing an Olfactory Network Together for Odor Perception

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