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Review
. 2022 Jan;27(1):383-402.
doi: 10.1038/s41380-021-01172-4. Epub 2021 Jun 8.

A Baldwin interpretation of adult hippocampal neurogenesis: from functional relevance to physiopathology

Djoher Nora Abrous #  1 , Muriel Koehl #  2 , Maël Lemoine #  3
Affiliations
Review

A Baldwin interpretation of adult hippocampal neurogenesis: from functional relevance to physiopathology

Djoher Nora Abrous et al. Mol Psychiatry. 2022 Jan.

Abstract

Hippocampal adult neurogenesis has been associated to many cognitive, emotional, and behavioral functions and dysfunctions, and its status as a selected effect or an "appendix of the brain" has been debated. In this review, we propose to understand hippocampal neurogenesis as the process underlying the "Baldwin effect", a particular situation in evolution where fitness does not rely on the natural selection of genetic traits, but on "ontogenetic adaptation" to a changing environment. This supports the view that a strong distinction between developmental and adult hippocampal neurogenesis is made. We propose that their functions are the constitution and the lifelong adaptation, respectively, of a basic repertoire of cognitive and emotional behaviors. This lifelong adaptation occurs through new forms of binding, i.e., association or dissociation of more basic elements. This distinction further suggests that a difference is made between developmental vulnerability (or resilience), stemming from dysfunctional (or highly functional) developmental hippocampal neurogenesis, and adult vulnerability (or resilience), stemming from dysfunctional (or highly functional) adult hippocampal neurogenesis. According to this hypothesis, developmental and adult vulnerability are distinct risk factors for various mental disorders in adults. This framework suggests new avenues for research on hippocampal neurogenesis and its implication in mental disorders.

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Conflict of interest statement

The authors declare no competing interests.

Figures

Fig. 1
Fig. 1. Schematic representation of maturation of behavioral capacities in relation to developmental milestones in rodents.
The different ontogenetic stages illustrated are: the early postnatal period (first 3 weeks of life) divided into the neonatal period (first 2 weeks), the juvenile period (2nd and 3rd week postnatal), and the adolescent period (4th–8th week postnatal). Learning capacity emerges sequentially from the simple to the complex. This succession of distinct competencies are adaptive at a particular period characterized by the state of maturity of sensorimotor functions, hormonal system, and of cerebral structures. The hippocampal formation, and the DG in particular, a key structure involved in episodic memory, presents a protracted development. The red square represents the end of maturation of Boundary cells (PND16), Head direction cells (PND 19), Grid cells (PND 20) and Place cells (P50) in the hippocampal formation. Adapted from [, , , –226].
Fig. 2
Fig. 2. Developmental trajectories leading to mental health or mental disorders.
Trajectories of individuals’ adapted (mental health) or maladapted (mental disorder) behavior follow three stages. The first one relies on DHN, and the second one on AHN. Both depend on genetics (that determine the shape of a Waddingtonian landscape) and environmental factors (determining the initial position of the ball and the direction it actually takes on forking paths). However, they do not depend on the same genes or events. They respectively end down in developmental or adult resilience/vulnerability to maladaptation. The probability to be oriented toward a given phenotype is indicated by the lines format (high probability: solid lines; low probability: dashed lines). The third stage gathers exposure to a series of mostly random triggering events of mental disorders, represented as nails in a Galtonian quincunx. Depending on both its previous trajectory and its reactions to these obstacles, the ball is more likely to fall on the left-hand or on the right-hand of the quincunx, following a Gaussian distribution law.
See this image and copyright information in PMC

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