Phylogenetic variation in cortical layer II immature neuron reservoir of mammals

Rosa, Chiara La; Cavallo, Francesca; Pecora, Alessandra; Chincarini, Matteo; Ala, Ugo; Faulkes, Chris G.; Nácher, Juan; Cozzi, Bruno; Sherwood, Chet C.; Amrein, Irmgard; Bonfanti, Luca

doi:10.7554/elife.55456

Cited by 46 publications

(98 citation statements)

References 67 publications

(111 reference statements)

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“…The actual lack of knowledge on their connectivity or their putative involvement in cognitive phenomena hinders understanding of their role in the adult brain. Taken that similar immature neurons populate most of the extension of the cerebral cortex of gyrencephalic species, including humans, complex cells may constitute a crucial resource for cortical plasticity [ 7 , 8 , 9 , 10 , 11 , 12 ] .…”

Section: Discussionmentioning

confidence: 99%

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PSA Depletion Induces the Differentiation of Immature Neurons in the Piriform Cortex of Adult Mice

Coviello

Benedetti

Jakubecova

et al. 2021

IJMS

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Immature neurons are maintained in cortical regions of the adult mammalian brain. In rodents, many of these immature neurons can be identified in the piriform cortex based on their high expression of early neuronal markers, such as doublecortin (DCX) and the polysialylated form of the neural cell adhesion molecule (PSA-NCAM). This molecule plays critical roles in different neurodevelopmental events. Taking advantage of a DCX-CreERT2/Flox-EGFP reporter mice, we investigated the impact of targeted PSA enzymatic depletion in the piriform cortex on the fate of immature neurons. We report here that the removal of PSA accelerated the final development of immature neurons. This was revealed by a higher frequency of NeuN expression, an increase in the number of cells carrying an axon initial segment (AIS), and an increase in the number of dendrites and dendritic spines on the immature neurons. Taken together, our results demonstrated the crucial role of the PSA moiety in the protracted development of immature neurons residing outside of the neurogenic niches. More studies will be required to understand the intrinsic and extrinsic factors affecting PSA-NCAM expression to understand how the brain regulates the incorporation of these immature neurons to the established neuronal circuits of the adult brain.

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Section: Discussionmentioning

confidence: 99%

“…In rodents, many of these immature neurons are located in the layer II of the piriform cortex (PCX) [ 4 , 5 , 6 ]. By contrast, mammals with more complex cerebral cortices, including humans, have more widespread distribution of these neurons throughout the neocortex [ 7 , 8 , 9 , 10 , 11 , 12 ].…”

Section: Introductionmentioning

confidence: 99%

PSA Depletion Induces the Differentiation of Immature Neurons in the Piriform Cortex of Adult Mice

Coviello

Benedetti

Jakubecova

et al. 2021

IJMS

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“…After the completion of classical developmental stages, are there other mechanisms by which the neuronal circuits can maintain flexibility, even at older ages? Recent studies have supported a possible avenue via the presence of immature-like neurons [ 155 , 156 , 157 ]. These investigations revealed regional-specific populations of DCX+ PSA-NCAM+ cells in the adult gyrencephalic brain.…”

Section: Maintaining a Population Of Immature Neurons In The Adult Brainmentioning

confidence: 99%

Implications of Extended Inhibitory Neuron Development

Kim

Paredes

2021

IJMS

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A prolonged developmental timeline for GABA (γ-aminobutyric acid)-expressing inhibitory neurons (GABAergic interneurons) is an amplified trait in larger, gyrencephalic animals. In several species, the generation, migration, and maturation of interneurons take place over several months, in some cases persisting after birth. The late integration of GABAergic interneurons occurs in a region-specific pattern, especially during the early postnatal period. These changes can contribute to the formation of functional connectivity and plasticity, especially in the cortical regions responsible for higher cognitive tasks. In this review, we discuss GABAergic interneuron development in the late gestational and postnatal forebrain. We propose the protracted development of interneurons at each stage (neurogenesis, neuronal migration, and network integration), as a mechanism for increased complexity and cognitive flexibility in larger, gyrencephalic brains. This developmental feature of interneurons also provides an avenue for environmental influences to shape neural circuit formation.

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“…Now, in eLife, Luca Bonfanti and colleagues – including Chiara La Rosa as first author – report new insights into this theory by describing immature neurons in the cortex of different mammals ( La Rosa et al, 2020 ). Although first classified in 2008, we still know little about these cortical immature neurons, especially about their functional relevance ( Gómez-Climent et al, 2008 ; Bonfanti and Nacher, 2012 ).…”

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confidence: 99%