Functional Integration of Neuronal Precursors in the Adult Murine Piriform Cortex

Benedetti, Bruno; Dannehl, Dominik; König, Richard; Coviello, Simona; Kreutzer, Christina; Zaunmair, Pia; Jakubecova, Dominika; Weiger, Thomas; Aigner, Ludwig; Nácher, Juan; Engelhardt, Maren; Couillard‐Després, Sébastien

doi:10.1093/cercor/bhz181

Cited by 40 publications

(71 citation statements)

References 53 publications

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“…In contrast to DCX+ cells in the MOB, these cells are nonproliferative immature neurons of embryonic origin. 41 The pool of these cells decreases during aging due to continuous neuronal differentiation following new olfactory demands, 42 and we showed that this process is impaired in lean T2D rats. 22 Whether or not obesity-induced T2D affects these cells in the PC is unknown.…”

Section: Introductionmentioning

confidence: 67%

Western Diet Accelerates the Impairment of Odor-Related Learning and Olfactory Memory in the Mouse

Lietzau

Nyström

Wang

et al. 2020

ACS Chem. Neurosci.

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Olfactory dysfunction could be an early indicator of cognitive decline in type 2 diabetes (T2D). However, whether obesity affects olfaction in people with T2D is unclear. This question needs to be addressed, because most people with T2D are obese. Importantly, whether different contributing factors leading to obesity (e.g., different components of diet or gain in weight) affect specific olfactory functions and underlying mechanisms is unknown. We examined whether two T2D-inducing obesogenic diets, one containing a high proportion of fat (HFD) and one with moderate fat and high sugar (Western diet, WD), affect odor detection/discrimination, odor-related learning, and olfactory memory in the mouse. We also investigated whether the diets impair adult neurogenesis, GABAergic interneurons, and neuroblasts in the olfactory system. Here, we further assessed olfactory cortex volume and cFos expression-based neuronal activity. The WD-fed mice showed declined odor-related learning and olfactory memory already after 3 months of diet intake ( p = 0.046), although both diets induced similar hyperglycemia and weight gain compared to those of standard diet-fed mice ( p = 0.0001 and p < 0.0001, respectively) at this time point. Eight months of HFD and WD diminished odor detection ( p = 0.016 and p = 0.045, respectively), odor-related learning ( p = 0.015 and p = 0.049, respectively), and olfactory memory. We observed no changes in the investigated cellular mechanisms. We show that the early deterioration of olfactory parameters related to learning and memory is associated with a high content of sugar in the diet rather than with hyperglycemia or weight gain. This finding could be exploited for understanding, and potentially preventing, cognitive decline/dementia in people with T2D. The mechanisms behind this finding remain to be elucidated.

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Section: Introductionmentioning

confidence: 67%

Western Diet Accelerates the Impairment of Odor-Related Learning and Olfactory Memory in the Mouse

Lietzau

Nyström

Wang

et al. 2020

ACS Chem. Neurosci.

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“…According to this view, AN in large-brained mammals would fall in the general rule of critical periods: temporal windows in which it is allowed, followed by the complete development of neural circuits (Semënov, 2019). It has been shown recently that mouse cINs can mature and be integrated into circuits at different ages (Benedetti et al, 2019), likely achieving a sort of "delayed neurogenesis." A recent report showing an abundance of INs in the sheep brain (Piumatti et al, 2018) supports the hypothesis that these cells might represent an evolutionary choice in large-brained mammals, as an alternative/parallel form of plasticity (Palazzo et al, 2018).…”

Section: Outcomementioning

confidence: 99%

Brain Structural Plasticity: From Adult Neurogenesis to Immature Neurons

2020

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Brain structural plasticity is an extraordinary tool that allows the mature brain to adapt to environmental changes, to learn, to repair itself after lesions or disease, and to slow aging. A long history of neuroscience research led to fascinating discoveries of different types of plasticity, involving changes in the genetically determined structure of nervous tissue, up to the ultimate dream of neuronal replacement: a stem cell-driven "adult neurogenesis" (AN). Yet, this road does not seem a straight one, since mutable dogmas, conflicting results and conflicting interpretations continue to warm the field. As a result, after more than 10,000 papers published on AN, we still do not know its time course, rate or features with respect to other kinds of structural plasticity in our brain. The solution does not appear to be behind the next curve, as differences among mammals reveal a very complex landscape that cannot be easily understood from rodents models alone. By considering evolutionary aspects, some pitfalls in the interpretation of cell markers, and a novel population of undifferentiated cells that are not newly generated [immature neurons (INs)], we address some conflicting results and controversies in order to find the right road forward. We suggest that considering plasticity in a comparative framework might help assemble the evolutionary, anatomical and functional pieces of a very complex biological process with extraordinary translational potential.

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“…The distribution and morphology of these cells are identical to those described previously by us and others in rats ( Bonfanti et al, 1992 ; Nacher et al, 2002 ). Most of the immature neurons in the adult rat PCX layer II have been generated during embryonic development ( Gómez-Climent et al, 2008 ) and progressively mature into functional excitatory neurons in this layer ( Rotheneichner et al, 2018 ; Benedetti et al, 2019 ), although the factors triggering or modulating these final steps of differentiation are still far from being understood.…”

Section: Discussionmentioning

confidence: 99%

“…In the last two decades, many studies have been conducted to characterize a population of immature neurons, which is densely distributed in the layer II of the adult rodent piriform cortex (PCX). Most, if not all, of these immature neurons are postmitotic cells generated during embryonic development ( Castillo-Gómez et al, 2008 ; Rubio et al, 2016 ), which progressively mature into typical excitatory neurons of the PCX ( Rotheneichner et al, 2018 ; Benedetti et al, 2019 ). These immature neurons transiently express the polysialylated form of the neural cell adhesion molecule (PSA-NCAM) ( Seki and Arai, 1991 ; Bonfanti et al, 1992 ), a plasticity molecule involved in different neurodevelopmental processes, such as neuronal migration, neurite extension, or synaptogenesis ( Rutishauser, 2008 ; Hildebrandt and Dityatev, 2013 ), which may also act as an insulating agent on these cells, preventing or limiting the formation of synaptic contacts ( Gómez-Climent et al, 2008 ).…”

Section: Introductionmentioning

confidence: 99%

Effects of Dopamine on the Immature Neurons of the Adult Rat Piriform Cortex

et al. 2020

Self Cite

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The layer II of the adult piriform cortex (PCX) contains a numerous population of immature neurons. Interestingly, in both mice and rats, most, if not all, these cells have an embryonic origin. Moreover, recent studies from our laboratory have shown that they progressively mature into typical excitatory neurons of the PCX layer II. Therefore, the adult PCX is considered a “non-canonical” neurogenic niche. These immature neurons express the polysialylated form of the neural cell adhesion molecule (PSA-NCAM), a molecule critical for different neurodevelopmental processes. Dopamine (DA) is a relevant neurotransmitter in the adult CNS, which also plays important roles in neural development and adult plasticity, including the regulation of PSA-NCAM expression. In order to evaluate the hypothetical effects of pharmacological modulation of dopaminergic neurotransmission on the differentiation of immature neurons of the adult PCX, we studied dopamine D2 receptor (D2r) expression in this region and the relationship between dopaminergic fibers and immature neurons (defined by PSA-NCAM expression). In addition, we analyzed the density of immature neurons after chronic treatments with an antagonist and an agonist of D2r: haloperidol and PPHT, respectively. Many dopaminergic fibers were observed in close apposition to PSA-NCAM-expressing neurons, which also coexpressed D2r. Chronic treatment with haloperidol significantly increased the number of PSA-NCAM immunoreactive cells, while PPHT treatment decreased it. These results indicate a prominent role of dopamine, through D2r and PSA-NCAM, on the regulation of the final steps of development of immature neurons in the adult PCX.

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Functional Integration of Neuronal Precursors in the Adult Murine Piriform Cortex

Cited by 40 publications

References 53 publications

Western Diet Accelerates the Impairment of Odor-Related Learning and Olfactory Memory in the Mouse

Western Diet Accelerates the Impairment of Odor-Related Learning and Olfactory Memory in the Mouse

Brain Structural Plasticity: From Adult Neurogenesis to Immature Neurons

Effects of Dopamine on the Immature Neurons of the Adult Rat Piriform Cortex

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