Humans and Dolphins: Decline and Fall of Adult Neurogenesis.

Roberta Parolisi,Luca Bonfanti,Bruno Cozzi

doi:10.3389/fnins.2018.00497

Roberta Parolisi, Luca Bonfanti + Show 1 more

Open Access

https://doi.org/10.3389/fnins.2018.00497

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Abstract

Pre-clinical research is carried out on animal models, mostly laboratory rodents, with the ultimate aim of translating the acquired knowledge to humans. In the last decades, adult neurogenesis (AN) has been intensively studied since it is viewed as a tool for fostering brain plasticity, possibly repair. Yet, occurrence, location, and rate of AN vary among mammals: the capability for constitutive neuronal production is substantially reduced when comparing small-brained, short living (laboratory rodents) and large-brained, long-living species (humans, dolphins). Several difficulties concerning scarce availability of fresh tissues, technical limits and ethical concerns did contribute in delaying and diverting the achievement of the picture of neurogenic plasticity in large-brained mammals. Some reports appeared in the last few years, starting to shed more light on this issue. Despite technical limits, data from recent studies mostly converge to indicate that neurogenesis is vestigial, or possibly absent, in regions of the adult human brain where in rodents neuronal addition continues into adult life. Analyses carried out in dolphins, mammals devoid of olfaction, but descendant of ancestors provided with olfaction, has shown disappearance of neurogenesis in both neonatal and adult individuals. Heterogeneity in mammalian structural plasticity remains largely underestimated by scientists focusing their research in rodents. Comparative studies are the key to understand the function of AN and the possible translational significance of neuronal replacement in humans. Here, we summarize comparative studies on AN and discuss the evolutionary implications of variations on the recruitment of new neurons in different regions and different species.

Highlights

After long debate since its first demonstration (Altman and Das, 1965), adult neurogenesis (AN) became accepted in birds in the 1980s by the direct illustration of long-range neuronal migration and the demonstration that the new cells had physiological properties of functional neurons (Paton and Nottebohm, 1984)
If basic neuronal stem cell biology can be similar in all mammals, the behavior of their differentiated neuronal progeny can substantially vary in brains whose neuroanatomies and development/postnatal growth differ (Workman et al, 2013)
Since the subventricular zone (SVZ) of the lateral ventricles provides neuronal progeny destined for the olfactory bulb (OB) and linked to olfactory discrimination (Lledo and Valley, 2016; Zhuo et al, 2016), we investigated the periventricular region of neonatal and adult dolphins in search for neurogenic activity

Summary

INTRODUCTION

After long debate since its first demonstration (Altman and Das, 1965), adult neurogenesis (AN) became accepted in birds in the 1980s by the direct illustration of long-range neuronal migration and the demonstration that the new cells had physiological properties of functional neurons (Paton and Nottebohm, 1984). Mammals are often considered homogeneous in their capability to undergo structural plasticity, the occurrence, location and rate of neurogenesis substantially differ when comparing laboratory rodents with large-brained, long-living species (Lipp and Bonfanti, 2016; Paredes et al, 2016; Parolisi et al, 2017). This fact is still underestimated by many scientists working in the field. A wider, systematic analysis involving different mammalian orders is lacking

ABSENCE OF POSTNATAL NEUROGENESIS IN THE DOLPHIN BRAIN

WHY IS ADULT NEUROGENESIS HIGHLY REDUCED OR ABSENT IN SOME MAMMALS?

Findings

CONCLUSIONS AND FUTURE PERSPECTIVES