TY - JOUR
T1 - Active perception during angiogenesis
T2 - filopodia speed up Notch selection of tip cells in silico and in vivo
AU - Zakirov, Bahti
AU - Charalambous, Georgios
AU - Thuret, Raphael
AU - Aspalter, Irene M.
AU - Van-Vuuren, Kelvin
AU - Mead, Thomas
AU - Harrington, Kyle
AU - Regan, Erzsébet Ravasz
AU - Herbert, Shane Paul
AU - Bentley, Katie
N1 - Publisher Copyright:
© 2021 The Authors.
Copyright:
Copyright 2021 Elsevier B.V., All rights reserved.
PY - 2021/3/29
Y1 - 2021/3/29
N2 - How do cells make efficient collective decisions during tissue morphogenesis? Humans and other organisms use feedback between movement and sensing known as 'sensorimotor coordination' or 'active perception' to inform behaviour, but active perception has not before been investigated at a cellular level within organs. Here we provide the first proof of concept in silico/in vivo study demonstrating that filopodia (actin-rich, dynamic, finger-like cell membrane protrusions) play an unexpected role in speeding up collective endothelial decisions during the time-constrained process of 'tip cell' selection during blood vessel formation (angiogenesis). We first validate simulation predictions in vivo with live imaging of zebrafish intersegmental vessel growth. Further simulation studies then indicate the effect is due to the coupled positive feedback between movement and sensing on filopodia conferring a bistable switch-like property to Notch lateral inhibition, ensuring tip selection is a rapid and robust process. We then employ measures from computational neuroscience to assess whether filopodia function as a primitive (basal) form of active perception and find evidence in support. By viewing cell behaviour through the 'basal cognitive lens' we acquire a fresh perspective on the tip cell selection process, revealing a hidden, yet vital time-keeping role for filopodia. Finally, we discuss a myriad of new and exciting research directions stemming from our conceptual approach to interpreting cell behaviour. This article is part of the theme issue 'Basal cognition: multicellularity, neurons and the cognitive lens'.
AB - How do cells make efficient collective decisions during tissue morphogenesis? Humans and other organisms use feedback between movement and sensing known as 'sensorimotor coordination' or 'active perception' to inform behaviour, but active perception has not before been investigated at a cellular level within organs. Here we provide the first proof of concept in silico/in vivo study demonstrating that filopodia (actin-rich, dynamic, finger-like cell membrane protrusions) play an unexpected role in speeding up collective endothelial decisions during the time-constrained process of 'tip cell' selection during blood vessel formation (angiogenesis). We first validate simulation predictions in vivo with live imaging of zebrafish intersegmental vessel growth. Further simulation studies then indicate the effect is due to the coupled positive feedback between movement and sensing on filopodia conferring a bistable switch-like property to Notch lateral inhibition, ensuring tip selection is a rapid and robust process. We then employ measures from computational neuroscience to assess whether filopodia function as a primitive (basal) form of active perception and find evidence in support. By viewing cell behaviour through the 'basal cognitive lens' we acquire a fresh perspective on the tip cell selection process, revealing a hidden, yet vital time-keeping role for filopodia. Finally, we discuss a myriad of new and exciting research directions stemming from our conceptual approach to interpreting cell behaviour. This article is part of the theme issue 'Basal cognition: multicellularity, neurons and the cognitive lens'.
KW - active perception
KW - angiogenesis
KW - basal cognition
KW - filopodia
KW - morphogenesis
KW - Notch lateral inhibition
UR - http://www.scopus.com/inward/record.url?scp=85101329904&partnerID=8YFLogxK
U2 - 10.1098/rstb.2019.0753
DO - 10.1098/rstb.2019.0753
M3 - Article
C2 - 33550953
AN - SCOPUS:85101329904
SN - 0962-8436
VL - 376
SP - 20190753
JO - Philosophical transactions of the Royal Society of London. Series B, Biological sciences
JF - Philosophical transactions of the Royal Society of London. Series B, Biological sciences
IS - 1821
M1 - 20190753
ER -