Extended neocortical maturation time encompasses speciation, fatty acid and lateralization theories of the evolution of schizophrenia and creativity

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Summary

I suggest that the extended maturation time of some regions of the human neocortex is the uniquely human factor which allows the development of language, creativity and madness. The genetic event or events which contribute to the long delay to final maturation occurred at or after the speciation of Homo sapiens sapiens. Neocortical growth may follow the previously detailed “balloon model”, which suggests that intra- and subcortical myelin production during development physically stretches each local area of the cortex tangentially to the pial surface, thereby causing neuronal columns to become more disjoint and more functionally independent, thereby increasing the functional capacity of the area [Seldon HL. Does brain white matter growth expand the cortex like a balloon? Hypothesis and consequences. Laterality 2005;10(1):81–95]. This occurs in addition to Hebbian synaptic modeling. Therefore, the size and functional capacity of each cytoarchitectonic area of each individual adult neocortex are the outcomes of partly deterministic (e.g., genetic) and partly statistical growth processes with numerous factors including environmental stimuli and fatty acid content in diets. The possible functional capacity and variation among growth outcomes increase with the length of time allowed to “finalize” synaptic weights, myelination and other plastic processes. For example, acquisition of quite differing linguistic skills becomes possible only in Homo sapiens because of the extended, decades-long plasticity of temporal lobe areas; in contrast, tactile skills vary little among human races and cultures, or even among higher primates, because of the faster maturation of the somatomotor areas. Some of the statistically extreme variations of the neocortical growth processes lead to abnormal cognition and behavior called “madness” or “genius”. This maturation hypothesis overcomes some problems with those based purely on fatty acid metabolism or on functional asymmetry (non-human species show functional asymmetry, but no language. Neanderthals had brains comparable in size and shape to ours, but failed to develop language or creativity). This hypothesis implies that the search for genetic factors should include those which influence the temporal regulation of neuronal and myelin growth, but it also allows the development of unusual creativity or madness as a statistical extreme in the absence of any deterministic factors. It has implications about our attitudes toward mental “disorders” and about potential approaches to treating some of them – for example, attempting communication and conditioning via those senses and cortical areas which show less variation and are less affected.

Introduction

There are currently two main interesting theories linking schizophrenia (or language, creativity and madness) to the origin of Homo sapiens sapiens. One is Crow’s theory that the speciation event was the origin of functional laterality in the neocortex, that the event involved a sex-linked gene (with different sequences on the X and Y chromosomes), and that functional asymmetry is necessary for the development of language and schizophrenia. Actually, this hypothesis can be re-stated more generally: there is an “average” functional topography of the human neocortex, over both hemispheres, and deviations from this may lead to enhancement or reduction of particular functions. Hemispheric asymmetry is one measure of the cortical topography. Reports too numerous to list here support a link between schizophrenia and anatomical and functional asymmetry [1], [2], [3], as well as gender differences in laterality.

Another theory, with proponents like Gibson [4] and Horrobin [5], [6], is that speciation was linked with a dramatic improvement in the metabolism of fatty acids, in particular of DHA and EPA. This happened about 130,000 years ago and led to a massive increase in the production of cell membranes in brain neurons and thus in the size and functional capacity of the brain. Disturbances in these metabolic pathways can lead to (less membrane production and) schizophrenia or “madness”. This hypothesis does imply a link between brain size and functional capacity.

However, it is contended that both of these hypotheses are necessary, but not sufficient prerequisites for the development of language, creativity, etc. Non-human species show evidence of functional lateralization, implying that lateralization pre-dated the origin of Homo sapiens and that lateralization does not always lead to language (e.g., [7], [8]). Sun et al. [9] have found numerous genes with asymmetric expression in the human brain, but it is not known if the one proposed by Crow is among them. Against the fatty acid metabolism hypothesis is evidence from Neanderthals. Neanderthal men (Homo sapiens neanderthalensis) had brains at least as large as those of Homo sapiens on average, yet there are few signs that they mastered “creativity” or language [10], [11]. If they had, then it would be difficult to imagine any adaptive advantage of Homo sapiens over them, and thus no explanation of why Homo sapiens replaced them. They also apparently diverged from the Homo sapiens line more than 130,000 years ago, implying that the event which led to large brains either was older than that or was duplicated in both lines. Regardless, in the Neanderthal line the “large brain” event did not lead to creativity and language, thus negating the sufficiency of the fatty acid hypothesis. In addition, all of the arguments against a linear relationship between brain size and functionality would also apply against this model. Those arguments include the male–female differences, the Oliver Cromwell – Anatole France differential, etc.

There is a third, relevant hypothesis. This is the balloon model proposed by Harasty et al. [12] and Seldon [13], [14], but actually already implied by Kaes [15]. It provides a mechanism linking fatty acid metabolism, or more specifically myelin production, with cortical functional capacity. According to this, myelin growth, both subcortical and intracortical, stretches the cortex tangentially to the surface, like a balloon; the stretching disentangles neighboring neuronal columns and enables the affected cortex to better differentiate afferent signal patterns. Because the balloon model describes cortical growth, it is affected by all putative factors – genetics, environment, nutrition, and even time. It should be emphasized that the balloon model is not a “cause” of anything, but a mechanism combining input factors into more or less stretched areas of cortex with more or less functional capacity.

Can all of these theories be accommodated? Is there something unique to Homo sapiens, which could explain uniquely human functions like language and madness, which allows for the roles of lateralization and of myelination or fatty acid metabolism, and which can account for large (Neanderthal) brains without language (or madness)?

Section snippets

Hypothesis

We hypothesize that there was a saltatory event in the evolution of Homo sapiens which post-dated functional lateralization, improved fatty acid metabolism, and the separation of the Neanderthal line. Whether it was the speciation event or happened later is not possible to tell, but it is only important that it happened in the Homo sapiens sapiens line. That event was to delay the end of neocortex maturation for years beyond its previous limit. Homo sapiens sapiens would, as far as cortical

Evaluation

The hypothesis contends that language, creativity and madness can arise from extended variable and plastic growth of cortical areas, which are asymmetric between the hemispheres anatomically and functionally. The keywords are variability and plasticity. Enormous variability in neocortical structure is a fact. The variations of structure and borders of cytoarchitectonic areas were described in great detail by von Economo and Koskinas [16]; von Economo and Horn [17] expanded on this for the

Consequences

Because of its statistical nature, the balloon model suggests that a small number of “extreme” outcomes may be expected without any deterministic cause. Metabolic or lateralization abnormalities would be sufficient, but not necessary causes of madness. For any given set of parameters, the stretching of a cortical area will yield a normal (gaussian) distribution in a population, with the vast majority of outcomes around the average, but with a small number of “extreme” cases at either end

Acknowledgement

This hypothesis is a direct consequence of a thought-provoking and fruitful correspondence with Prof. T.J. Crow, to whom should go much of the credit.

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