Metabolic trajectories in developing human neocortical neurons

G Gianmarco Ferri (Fondazione Pisana per la Scienza ONLUS) F Francesco Finamore (Fondazione Pisana per la Scienza ONLUS) F Francesco Greco (Fondazione Pisana per la Scienza ONLUS) A Alessio Zanelli (Department of Biology Unit of Cell, Molecular and Developmental Biology, University of Pisa) F Fabrizia Carli (Institute of Clinical Physiology, National Research Council) A Alessandro Passera (Fondazione Pisana per la Scienza ONLUS) E Elisa Degl’Innocenti (Fondazione Pisana per la Scienza ONLUS) F Francesco Olimpico (Fondazione Pisana per la Scienza ONLUS) R Riccardo Ducoli (Institute of Clinical Physiology, National Research Council) A Agnese Sgalippa (Fondazione Pisana per la Scienza ONLUS) G Gian Carlo Demontis (Department of Pharmacy, University of Pisa) A Amalia Gastaldelli (Institute of Clinical Physiology, National Research Council) F Francesco Cardarelli (National Enterprise for nanoScience and nanoTechnology Laboratory, Scuola Normale Superiore) M Marco Onorati (Department of Biology, University of Pisa, via Luca Ghini 13, Pisa 56126, Italy) L Liam A. McDonnell (Fondazione Pisana per la Scienza ONLUS) M Maria Teresa Dell’Anno (Fondazione Pisana per la Scienza ONLUS)

Abstract

The shift from glycolysis to oxidative phosphorylation is a key step in neural differentiation. Yet, the timing of metabolic rewiring in the development from progenitors to neurons remains elusive, especially in human corticogenesis. To bridge this gap, here we adopted a unique cell platform based on neocortex-derived human neuroepithelial stem cells, modeling their physiological transition into functional neurons in a 4-mo longitudinal study and until the acquisition of electrophysiological competence. Using quantitative proteomics, combined with NAD(P)H fluorescence lifetime imaging and metabolomics, we investigated the entire differentiation process and describe how metabolic pathways drive cortical neuron maturation. The prevalent metabolic adaptations were then confirmed in a human neocortical specimen. This study provides a spatiotemporal map of neocortical metabolism during development and offers a framework to investigate human neurometabolic disorders.

Article Details

Volume / Issue Vol. 123, Issue 14
Published April 07, 2026
ISSN 0027-8424
Publisher National Academy of Sciences

Authors (16)

G

Gianmarco Ferri

Fondazione Pisana per la Scienza ONLUS

F

Francesco Finamore

Fondazione Pisana per la Scienza ONLUS

F

Francesco Greco

Fondazione Pisana per la Scienza ONLUS

A

Alessio Zanelli

Department of Biology Unit of Cell, Molecular and Developmental Biology, University of Pisa

F

Fabrizia Carli

Institute of Clinical Physiology, National Research Council

A

Alessandro Passera

Fondazione Pisana per la Scienza ONLUS

E

Elisa Degl’Innocenti

Fondazione Pisana per la Scienza ONLUS

F

Francesco Olimpico

Fondazione Pisana per la Scienza ONLUS

R

Riccardo Ducoli

Institute of Clinical Physiology, National Research Council

A

Agnese Sgalippa

Fondazione Pisana per la Scienza ONLUS

G

Gian Carlo Demontis

Department of Pharmacy, University of Pisa

A

Amalia Gastaldelli

Institute of Clinical Physiology, National Research Council

F

Francesco Cardarelli

National Enterprise for nanoScience and nanoTechnology Laboratory, Scuola Normale Superiore

M

Marco Onorati

Department of Biology, University of Pisa, via Luca Ghini 13, Pisa 56126, Italy

L

Liam A. McDonnell

Fondazione Pisana per la Scienza ONLUS

M

Maria Teresa Dell’Anno

Fondazione Pisana per la Scienza ONLUS