The Laminar Organization of Piriform Cortex Follows a Selective Developmental and Migratory Program Established by Cell Lineage

Martín-López, Eduardo; Ishiguro, Kimiko; Greer, Charles A.

doi:10.1093/cercor/bhx291

“…Figure b shows the widths of layers 1a and 1b in APC and PPC, wherein layer 1a occupies close to 70% of layer 1 in APC and 45% in PPC. These estimates are consistent with previous studies that show that about 75% of APC and 40% of PPC layer 1 is devoted to layer 1a (Martin‐Lopez et al, ; Sarma et al, ). Due to the significant difference in the widths of layers 1a and 1b in APC and PPC, we wondered if these widths changed from the anterior to posterior in a graded fashion or abruptly.…”

Section: Resultssupporting

confidence: 93%

“…To determine the thicknesses of the sublayers of piriform layers 1a and 1b, we used the same method as those used in (Martin‐Lopez, Ishiguro, & Greer, ; Sarma et al, ) in three mice. We stained for MAP2 (1:100, anti‐Rabbit, Invitrogen, Carlsbad, CA; cat # PA5‐17646, RRID: AB_11006358) and Calretinin (1:1000, anti‐Goat, Millipore, Burlington, CA; cat # AB 1550, RRID: AB_90764), and identified layer 1a by the expression of Calretinin and MAP2, layer 1b by the expression of MAP2, and layer 2 by the expression of NeuN (1:250, anti‐mouse, Millipore cat # MAB377, RRID: AB_2298772).…”

Section: Methodsmentioning

confidence: 99%

The distributed circuit within the piriform cortex makes odor discrimination robust

Srinivasan

¹

,

Stevens

²

2018

J of Comparative Neurology

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Distributed circuits wherein connections between subcircuit components seem randomly distributed are common to the olfactory circuit, hippocampus, and cerebellum. In such circuits, activation patterns seem random too, showing no detectable spatial preference, and contrast with regions that have topographic connections between subcircuits and topographic activation patterns. Quantitative studies of topographic circuits in the neocortex have yielded common principles of organization. Whether distributed circuits share similar principles of organization is unknown because similar quantitative information is missing and understanding the way they encode information remains a challenge. We addressed these needs by providing a quantitative description of the mouse piriform cortex, a paleocortical distributed circuit that subserves olfaction. The quantitative information provided two insights. First, with a nearly parameter-free model of the olfactory circuit, we show that the piriform cortex robustly maintains odor information and discrimination ability present in the olfactory bulb. Second, the paleocortex is quantitatively different from the neocortex: it has a lower surface area density, which decreases from the anterior to posterior paleocortex contrasting with the uniform neuronal density of the neocortex. These insights might also apply to other distributed circuits.

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“…Layer 2 can be divided into layer 2a (upper third) and layer 2b (deep two-thirds) (Choy et al 2015;Martin-Lopez et al 2017). For analysis, the extent of layer 2 was delineated using a DAPI stain ( Fig.…”

Section: Layer Identification In Postnatal Developmentmentioning

confidence: 99%

“…Layer 2a contains superficial so-called semilunar cells (layer 2a neurons). Layer 2b harbors pyramidal cells (layer 2b neurons) (Choy et al 2015;Martin-Lopez et al 2017). The two cell types display differences in functional circuit incorporation.…”

Section: Introductionmentioning

confidence: 99%

Circuit-specific dendritic development in the piriform cortex

Moreno-Velasquez

¹

,

Kaehne

²

,

Lo

³

et al. 2019

Preprint

0

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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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“…Layer 2 is the main cellular layer of the olfactory cortex (Bekkers and Suzuki, 2013). Based on the distribution of genetic markers and somatic morphology, layer 2 can be divided into layer 2a (superficial third) and layer 2b (deeper two-thirds; Diodato et al, 2016;Choy et al, 2017;Bolding et al, 2019;Martin-Lopez et al, 2019). Layer 2a predominantly contains superficial so-called semilunar cells (layer 2a neurons).…”

Section: Introductionmentioning

confidence: 99%

Circuit-Specific Dendritic Development in the Piriform Cortex

Moreno-Velasquez

¹

,

Lo

²

,

Lenzi

³

et al. 2020

eNeuro

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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. In the three-layered anterior piriform cortex (aPCx), neurons in the sublayers 2a and 2b display vertical segregation of these two circuit motifs. Here, we combined electrophysiology, detailed morphometry, and Ca 21 imaging in acute mouse brain slices and modeling to study circuit-specific aspects of dendritic development. We observed that determination of branching complexity, dendritic length increases, and pruning occurred in distinct developmental phases. Layer 2a and layer 2b neurons displayed developmental phase-specific differences between their apical and basal dendritic trees related to differences in circuit incorporation. We further identified functional candidate mechanisms for circuit-specific differences in postnatal dendritic growth in sublayers 2a and 2b at the mesoscale and microscale levels. Already in the first postnatal week, functional connectivity of layer 2a and layer 2b neurons during early spontaneous network activity scales with differences in basal dendritic growth. During the early critical period of sensory plasticity in the piriform cortex, our data are consistent with a model that proposes a role for dendritic NMDA-spikes in selecting branches for survival during developmental pruning in apical dendrites. The different stages of the morphologic and functional developmental pattern differences between layer 2a and layer 2b neurons demonstrate the complex interplay between dendritic development and circuit specificity.

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The Laminar Organization of Piriform Cortex Follows a Selective Developmental and Migratory Program Established by Cell Lineage

Cited by 38 publications

References 69 publications

The distributed circuit within the piriform cortex makes odor discrimination robust

The distributed circuit within the piriform cortex makes odor discrimination robust

Circuit-specific dendritic development in the piriform cortex

Circuit-Specific Dendritic Development in the Piriform Cortex

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