Adult Neurogenesis in Humans Dogma Overturned Again and Again

Front Neurosci. 2017; xi: 420.

Evolutionary Shaping of Developed Hippocampal Neurogenesis in Mammals–Cognitive Gain or Developmental Priming of Personality Traits?

Hans-Peter Lipp

¹Institute of Evolutionary Medicine, University of Zurich, Zurich, Switzerland

^twoInstitute of Anatomy, University of Zurich, Zurich, Switzerland

^threeDepartment of Physiology, School of Laboratory Medicine, University of Kwazulu-Natal, Durban, Due south Africa

Received 2022 Mar 15; Accepted 2022 Jul 5.

Keywords: adult neurogenesis, natural selection, development, hippocampal functions, cognition, comparative, personality, genetic assimilation

Adult hippocampal neurogenesis (AHN) in mammals peaks in early postnatal/juvenile periods and is strongly downwardly-regulated thereafter. Depending on species, it may disappear rapidly in adult individuals, or persist at very low levels for a lifetime. Usually, college levels of AHN in mammals are thought to provide mental flexibility allowing for adapting to new ecological niches. Merely why does natural selection not prevent down-regulation of AHN, and why should a rudimentary proliferation charge per unit in humans provide reproductive fitness even for aged individuals? The problem is compounded past species-specific behavioral manifestations of hippocampal functions that depend on encephalon size and ecological niches. Moreover, in laboratory rodents, proliferation levels of AHN and behavioral covariates appear unpredictable and context-sensitive. Conversely, one might ask why evolutionary mechanisms tolerate in nearly all mammals a certain level of early postnatal or subadult AHN. Specifically, the hypothesis of cognitive flexibility appears odd in species in which AHN is massively reduced in early infancy such as in humans. I suggest that early but non late AHN plays a subconscious part in developing randomly different epigenetic personality traits in local populations. Such traits may counteract or enhance natural option of the underlying genetic architecture—a procedure known as genetic assimilation.

In mammals, protracted neurogenesis occurs in subventrical zones (SVZ) from which neuroblasts drift rostrally to the olfactory bulb (rostral migratory stream, RMS) and from a secondary proliferation zone in the dentate gyrus, the subgranular zone (SGZ). The ongoing postnatal proliferation there is denoted equally "adult" hippocampal neurogenesis (AHN). Molecular markers for migration and differentiation are often not correlated with basic levels of AHN in many species. For example, doublecortin (DCX) is a reasonable proxy for estimating proliferation rates in mice and rats. In other species such markers persist for long periods later on the cessation of proliferation or appear even generated de novo (Amrein, 2015; Penz et al., 2015; Lipp and Bonfanti, 2016). Therefore, AHN and its potential relation to natural selection will refer here to simple proliferation only. Later all, it is the dogma-breaking part of persisting neurogenesis that dominates the public view of AHN.

The main problems

The evolutionary role of AHN in mammals is not understood. The well-nigh straightforward caption shared by many has been offered by Kempermann (2012, 2016) who claims that AHN is an evolutionary contempo improver since information technology is linked with the mammalian hippocampus, which itself is unique for mammals. As the homo hippocampus is mediating complex forms of memory, the putative benign role of AHN for human being memory is extrapolated from rodent studies to humans and to other mammalian species. Thus, cognitive flexibility originating from AHN should provide mammalian species with superior abilities for adapting to new environments. This view bears some bug, namely the role of the hippocampus in mammalian behavior, the different levels of AHN in various species, the differential down-regulation of AHN across species, and the process of natural choice in small-scale populations.

Does natural selection act on behavioral traits depending on AHN?

To reply this, one would need to know what behaviors and abilities are clearly correlated with hippocampal structural traits including AHN. Perhaps surprisingly, the situation is not articulate since even laboratory rodents show a bewildering variety of hippocampus-dependent behaviors, mostly ignored by AHN inquiry. For one, they include natural behaviors such equally food burrowing and nest building (Deacon et al., 2002), and social behavior (Ely et al., 1976). Better known are many learning paradigms including elementary two-manner abstention (Lipp et al., 1989) and cerebral behaviors such every bit spatial navigation and design separation.

Why is such diversity not known for humans? The human hippocampus interacts chiefly with higher-social club association cortex more often than not lacking in rodents (Figures 1A,B), see also Dong (2008). In addition, the rodent hippocampus integrates less "cerebral" input with subcortical limbic structures (Figures 1B,D). In both species (Figures 1C,D), the hippocampal loops form the ultimate associative cortex. Even so, in rodents this structure must likewise handle functions relegated to specialized cortex regions in humans (Bergmann et al., 2016), being therefore multifunctional. Furthermore, the rodent hippocampus blends hypothalamic and basal forebrain activity into input/output loops connecting to fronto-limbic cortical areas. Thus, the hippocampus is probable to be involved in modulation of many species-typical behaviors. The prevailing uncritical bidirectional extrapolation from human hippocampal functions to rodents and vice versa has led to some ill-founded views.

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(A) Proportions of associative and sensori-motor clan cortex differ in humans and rodents, encounter too (Dong, 2008). (B) Associative cortex in rodents is formed by and large past the hippocampal formation. (C) Human hippocampal loops receive reduced columnar activity patterns from cortex areas, adjustment them to parallel ("trisynaptic") loops that permit transformation of input/out patterns by Schaffer collaterals in CA3 and CA1. Unlike colors of rectangles signal a progressive reduction of cortical action design for representation in the hippocampal germination (Lipp, 2015). (D) Corresponding view in rodents in which the input to the hippocampal loop system originates chiefly from non-associative cortex regions but also from subcortical structures. Random dispersal of newly built-in cells in the dentate gyrus may prime number the early postnatal development into different behavioral phenotypes and personalities.

For instance, many researchers and editors believe now that AHN is specifically disquisitional for complex tests involving blueprint separation, the human being ability to memorize fine-grained differences in spatial or contextual environments (Sahay et al., 2011). Yet the behavioral prove for this conclusion is shaky every bit information technology was obtained in mice exposing them to examination situations requiring gradually recognizing subtle differences in spatial arrangements of threatening situations. Merely small rodents cannot afford to discriminate subtleties of threats such as the colour and size of a cat and must react immediately. Evidently, AHN-dependent blueprint separation is useful for survival of rodents just if information technology works at once, and this sit-in is withal lacking.

Tin can variable structural traits in granule cells and mossy fibers mediate behavior and existence targeted past natural selection?

The extent of the so-chosen intra/infrapyramidal mossy fiber projection (IIP-MF) correlates genetically and individually with behavioral traits, not all of them beingness considered as "hippocampal" (Lipp et al., 1989). Variations of IIP-MF in mice co-vary positively with predictability of ongoing behaviors, and respond speedily to selective breeding and natural selection (Lipp and Wolfer, 1995, 2002, 2013). Therefore, developmental variations in the distribution of the granule prison cell axons can predict behavioral traits of adults.

On the other hand, it is difficult to find in rodents consequent correlations between private numbers of newly generated neurons and individual behaviors. A likely reason is that the extent of the IIP-MF is adamant during the first postnatal days of rodent pups, and remains rather stable during adulthood. Conversely, AHN in rodents is extremely sensitive to environmental changes, activity and stress levels, and appears influenced past about 190 genes (Kempermann et al., 2006). Information technology besides changes strongly during life history as explained beneath. Thus, functional relations between AHN and behaviors in mice and rats are masked past excessive temporal variability of the structural substrate, possible interactions with learning, and by the multi-functionality of the rodent hippocampus. This may explain the huge number of behavioral AHN studies with discordant results (Lipp and Bonfanti, 2016). Exceptions with more than predictable result are some naturalistic behaviors. Genetic suppression of AHN resulted in impairments of species-typical behaviors and sucrose preference in mice (Jedynak et al., 2012) and rats (Snyder et al., 2016). Studies of individual correlations showed positive correlations of AHN levels with sucrose preference (Hu et al., 2016), and with roaming in big enclosures (Freund et al., 2013). Conversely, reactions to novelty correlated negatively with the number of proliferating neurons (van Dijk et al., 2016). Only even for species-typical behaviors, their relation to AHN appears unpredictable. Yet natural choice requires that behavioral phenotype and genotype should be strongly linked. It is thus difficult to see how natural choice could act on cerebral or species-typical behaviors linked unpredictably to AHN, and even more than hard to imagine selective force per unit area on increased AHN in species in which it is already sparse early on in life.

AHN is strongly downward-regulated but is bottoming out after two years, independent of species

AHN diminishes with age, initially considered every bit a normal aging process. Nonetheless, studies in mice showed that AHN is exponentially decreasing after 7 weeks of age till well-nigh iv months—during acme conditions for reproduction—and leveling off subsequently (Ben Abdallah et al., 2010). A strong refuse during the kickoff twelvemonth of life has now been documented repeatedly for humans (Knoth et al., 2010; Dennis et al., 2016, 2017). Weissleder et al. (2016) accept reported a further decrease from years 21 till 91, yet starting from a low level. Other markers of proliferative activity in the human hippocampus did non show an age-dependent decline. Thus it makes sense to distinguish early vs. late AHN.

The belief in a functional role of AHN in aged humans is supported solely by a widely cited study past Spalding et al. (2013) even though it remains controversial among experts. Using the decay of radioactive C14 in human hippocampi, they calculated daily turnover rates of 700 cells per day among 20 millions granule cells. However, they miscalculated proliferation levels in mice and concluded—widely cited also—that AHN in 40 year-old humans is comparable in proliferation levels to correspondingly aged mice (for details see Lipp and Bonfanti, 2016).

In comparative terms, the work of Amrein et al. (2011) has shown that stiff down-regulation of AHN occurs in many species regardless of life bridge and ecological conditions. A bottom in proliferative activeness is reached in both mice and men after about 2 years, and AHN is standing at minimal rates independent of the life span of the species. These findings make cantankerous-species comparability of AHN and life history questionable.

For example, nosotros had hypothesized that the disuse of AHN in humans might follow a much slower pace, bottoming out at the age of almost thirty years (Amrein and Lipp, 2009). This view might take explained some typical transitions in human life history such as the emergence of long-term memory at the expense of short-term memory in children (Yim et al., 2013; Akers et al., 2014). Likewise, it would have fitted the transition from exuberant and reckless juvenile behavior to cautious adult behavior—a characteristic of the maturation of the hippocampus as postulated by Altman et al. (1973). The general thought was that the input-output patterns of the hippocampal germination between the loops crossing the hippocampal germination (Figures 1C,D) would initially be kept malleable by the AHN-dependent production of juvenile excitable granule cells. The downwardly-regulation of AHN would then entail a fixation of input-output relations associated with acquired and species-typical behaviors optimal for a given environment. This concept would make sense in species in which the initial reduction of AHN covers pre- and post-puberty and early adulthood such as in mice or rats. In these species, the altered hippocampal physiology might exist of evolutionary adaptive value. Therefore, natural selection might favor strong early AHN followed by a period of fixing behavioral traits. Yet, in humans the decay flow falls into a time window with reduced behavioral expression and cognitive abilities. Moreover, it is accompanied by an enormous (non-proliferative) growth of dendrites and connections in the forebrain. This raises the question whether early peaking of AHN and down-regulation with belatedly bottoming-out is useful for humans at all.

Why is belatedly man AHN not enhanced by natural selection?

The most parsimonious reply is that continuing low-level AHN does non matter at all, assuming that the add-on of 700 new cells per twenty-four hour period (if this can exist proved) has a negligible bear upon on adult on human being hippocampal functions. Nowadays, this view has go almost heretical. But one might rightly enquire why a putative benign structural trait has been curtailed in humans and non increased past natural choice. Now there is no answer. A conceptually related question is why natural selection has (regrettably) not increased the intelligence caliber in humans from an boilerplate of 100 to one of 140 points. Plain, reproductive fitness—a benchmark of evolution—is not strongly correlated with cognitive abilities. Its reproductive reward is counteracted past competing traits such equally physical attractiveness and, amid males, physical strength and aggression, not infrequently at the disadvantage of courtship academics. For human being AHN, the reasons are less obvious. Maybe, the emergence of highly excitable young neurons may interfere with the orchestrated development of other granule cell functions (Drew et al., 2016), or it is even impairing normal cerebral function (Walton et al., 2012). Alternatively, hippocampal functionality and granule prison cell excitability is regulated by other mechanisms than simple proliferation. Whatever reasons, it would seem that AHN in humans is suppressed early in ontogeny, in parallel with neurogenesis in the SVZ, probably too in other primate species (Lipp and Bonfanti, 2016). It is thus difficult to see why natural choice should preserve a pocket-size and dwindling prison cell population in the human dentate gyrus. This would require showing that late human AHN has a conspicuously benign effect on reproductive fitness or is advantageous for the survival of the group members.

But why is early postnatal AHN maintained fifty-fifty in humans?

On the other paw, comparative assay across mammals (Amrein, 2015; Patzke et al., 2015) suggests that an initial level of AHN is maintained in most species, at least in those in which historic period-dependency could exist investigated. Differences between orders and species emerge primarily in the time course of the disuse within a span of 2 years, and in the molecular differentiation of the newly generated cells (Amrein, 2015). Up to at present, a coherent movie of how species differences in AHN chronicle to ecological atmospheric condition must remain speculative, chiefly because of depression sample sizes and problems in quantifying historic period levels. Still, the typical fourth dimension course of AHN in mammals must provide some variable advantages in terms of natural selection, perhaps more than in short-living rodents than in primates and other species.

Early hippocampal neurogenesis may prime randomly the development of personality traits

The problem in humans is to find a useful role for early on postnatal neurogenesis during a menstruum of reduced cognition. This role ought to provide a target for natural selection in adults in social club to maintain this developmental trait. One might argue that hippocampal neurogenesis in such an early on postnatal stage could help in organizing the development of forebrain circuitry underlying cognitive processing, eastward.k., the emergence of language. But this should have consequences for developed beliefs many years later. Nevertheless it remains questionable whether individual differences in linguistic communication development do have an touch on on evolutionary relevant developed behavior.

On the other paw, personality traits such every bit take chances-taking behavior or food preferences must accept been obvious targets for rapid natural selection during human evolution, specifically in small-scale populations. In larger populations, genetic variation balances competing traits, permitting rapid natural selection of carriers plumbing equipment into a changed environment. However, in smaller groups natural option, for instance for timidity, might rapidly eliminate genetic variation supporting risk-taking behavior. This can reduce the power of genetically adapting to new environments of a sudden favoring adventure-takers.

Loss of evolutionary plasticity due to natural selection is a common problem for small populations in many species. A possible mechanism counteracting such processes is the early on development of personality traits in absence of genetic variation. The unpredictable occurrence of correlations between AHN and personality traits in isogenic rodents suggests that such personality traits emerge randomly. For example, sucrose preference shows strong genetic variability in mice and humans (Reed et al., 1997). Yet testing inbred mice for sucrose preference shows ofttimes a minority of individuals with initial taste neophobia, indicating that this long-lasting trait tin develop purely epigenetically, remaining correlated in rats with individual levels of AHN (Hu et al., 2016). Sweet preference is an adaptive trait that seemingly deserves to exist naturally selected, fixing information technology rapidly genetically. All the same, this might be fatal for a population as soon every bit sucrose becomes associated with toxins. Just if there are epigenetic traits for sense of taste neophobia, these individuals will not be eliminated rapidly and natural selection might showtime selecting alleles promoting gustation neophobia, a process known as genetic absorption (Renn and Schumer, 2013).

This idea is in line with recent findings of an elegant study using a chemogenetic arroyo to inactivate selectively perinatally and postnatally born olfactory neurons in mice (Muthusamy et al., 2017). They found that perinatally built-in neurons were controlling innate fear responses to predator scent, while neurons built-in 6 weeks later appeared to control the acquisition of novel appetitive odors. Thus, newly added neurons may prime novel preferences without erasing critical responses for survival. A second case is the private propensity for roaming, oft taken equally a measure for risk-taking behavior. Once again, individual correlations between levels of AHN and "exploratory" activities take been reported for inbred mice (Freund et al., 2013; van Dijk et al., 2016). Therefore, developmental randomization of behavioral traits by means of AHN at very early ages might predict later gustatory and olfactory preferences, plus roaming activity, not only in mice but as well in humans. After all, from 110,000 years ago humans had to survive evolutionary critical bottlenecks past switching to a mussel diet (Marean, 2016)—certainly not the preferred food of most primates. As well, the presence of roamers and not-roamers in a population helps to find new habitats. Thus, the evolutionary gain of AHN in most mammalian species including humans might not be noesis only regulating the degree of genetic assimilation of behavioral traits of central importance for adaptation to new habitats.

Writer contributions

The author confirms beingness the sole contributor of this work and approved information technology for publication.

Conflict of interest statement

The writer declares that the research was conducted in the absenteeism of any commercial or financial relationships that could be construed as a potential conflict of interest.

Acknowledgments

I thank Irmgard Amrein and David Wolfer for critical reading, and Irina Lipp for administrative support.

Footnotes

Funding. Writing of this newspaper was supported past intramural funds of the Academy of Zurich.

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