Elsevier

Journal of Human Evolution

Volume 77, December 2014, Pages 88-98
Journal of Human Evolution

Energetic and nutritional constraints on infant brain development: Implications for brain expansion during human evolution

https://doi.org/10.1016/j.jhevol.2014.05.001Get rights and content

Abstract

The human brain confronts two major challenges during its development: (i) meeting a very high energy requirement, and (ii) reliably accessing an adequate dietary source of specific brain selective nutrients needed for its structure and function. Implicitly, these energetic and nutritional constraints to normal brain development today would also have been constraints on human brain evolution. The energetic constraint was solved in large measure by the evolution in hominins of a unique and significant layer of body fat on the fetus starting during the third trimester of gestation. By providing fatty acids for ketone production that are needed as brain fuel, this fat layer supports the brain's high energy needs well into childhood. This fat layer also contains an important reserve of the brain selective omega-3 fatty acid, docosahexaenoic acid (DHA), not available in other primates. Foremost amongst the brain selective minerals are iodine and iron, with zinc, copper and selenium also being important. A shore-based diet, i.e., fish, molluscs, crustaceans, frogs, bird's eggs and aquatic plants, provides the richest known dietary sources of brain selective nutrients. Regular access to these foods by the early hominin lineage that evolved into humans would therefore have helped free the nutritional constraint on primate brain development and function. Inadequate dietary supply of brain selective nutrients still has a deleterious impact on human brain development on a global scale today, demonstrating the brain's ongoing vulnerability. The core of the shore-based paradigm of human brain evolution proposes that sustained access by certain groups of early Homo to freshwater and marine food resources would have helped surmount both the nutritional as well as the energetic constraints on mammalian brain development.

Introduction

The adult human brain weighs about 1350 g or about three pounds (Allen et al., 2002), which is about three times more than in either Australopithecus afarensis or large apes today (Table 1). The human brain is large not only in absolute size but, at ∼2% of adult body weight, is also large in proportion to body size. The hominin fossil record provides few clues to explain how and why the brain of Homo sapiens evolved to become so much larger and so much more cognitively developed than in non-human primates.

Normal brain development in the infant is a prerequisite for optimal brain function in the adult so potential constraints on brain development have implicit significance for understanding constraints on evolving higher functionality of the primate brain. The brain in newborn humans represents about 13% of lean body weight, which is about 30% more than for the newborn chimpanzee (Table 1). It also has a very high energy requirement, greatly exceeding that of the rest of the body combined (Fig. 1). This remarkable situation provides insight into the uniqueness of human brain evolution: how did so much energy metabolism get focused on the neonatal brain when it is not really able to contribute to survival until the child is at least five to six years old, i.e., long after the age at which other primates are semi- if not totally autonomous?

To expand three-fold over the past two to three million years, the early hominin brain had to overcome at least two constraints: (i) an energetic constraint: increasing energy requirements as the brain size increased, and (ii) a nutritional constraint: increasing requirements for nutrients that play a specific role in mammalian brain structure, development and function. The energetic constraint is synonymous with the ‘metabolic’ constraint described in earlier publications (Cunnane, 2010) but ‘energetic’ is perhaps the more appropriate term given that it refers exclusively to meeting energy requirements. Similarly, the nutritional constraint is synonymous with the ‘structural’ constraint described elsewhere because the nutrients tend to be needed for cellular structure and function. Nevertheless, the distinction between these two constraints is imperfect because they have a certain degree of overlap with each other, especially during infancy. Either constraint alone can delay and/or permanently foreshorten cognitive development in infants today, so it is important to emphasise that surmounting just one of these two constraints alone would not have been sufficient to push human brain evolution forwards. Therefore, the path towards hominin brain expansion involved a long period of investment in overcoming the energetic and nutritional vulnerability of the brain during infant development, a vulnerability that is greater in humans than other species and remains with us to the present day.

The shore-based paradigm of human brain evolution proposes that hominins destined to become humans surmounted the brain's developmental vulnerability by exploiting shore-based habitats that provided abundant and sustained access to a wide selection of foods rich in brain selective nutrients. This paradigm also proposes that occupying the shore-based habitat was associated the evolution of neonatal body fat reserves, which were just as important for optimal human brain development. Deposits of subcutaneous body fat are not unusual in adult mammals but, with the exception of humans, are not present in the neonates of non-human primates. The particularly high energy needs of the developing human brain suggest that fuel stored as body fat in the newborn plays a critical role in early brain development. By providing access to an enriched dietary source of brain selective nutrients and by permitting evolution of body fat, a shore-based habitat masked the neurodevelopmental vulnerability that is still a hallmark of human infants today. Together, these two developments in early hominins led eventually to evolution of the modern human brain.

Section snippets

Vulnerability of the developing brain

Brain development passes through a series of processes that, in essence, starts with overproduction of neurons, followed by their migration to specific layers within the brain, then pruning of excess neurons, followed by myelination. This highly regulated and complex process involves a sequence of critical periods in brain development such that successful completion of a given period depends on (and is therefore vulnerable to) the successful completion of the preceding period. Deficits and

Challenging aspects of brain energy metabolism

Several challenges for brain energy metabolism arose in mammals and became more acute in species with larger brains. First is the brain's high metabolic rate, i.e., its high energy needs (Table 2). In order to regenerate its cellular fuel, adenosine triphosphate, the brain has to process glucose through the tricarboxylic cycle. In addition, the amino acid, glutamate, is a key neurotransmitter but it can also trigger undesirable signals if its concentration in the brain rises too much. A large

High brain energy requirement: the first key constraint

The brain's energy requirement is essentially constant regardless of the cognitive effort being expended at any particular moment (Magistretti, 2004). On a normal pattern of food intake (three meals per day), the brain runs almost exclusively on the six carbon sugar: glucose. The adult human brain consumes ∼3–4 mg of glucose per 100 g of brain tissue per minute or about 100 g (a quarter pound) of glucose per day. Thus, the adult brain's energy requirement is equivalent to about 20–23% of the

Nutrients for brain structure and function: the second key constraint

Certain nutrients must be present in the diet to assure optimal mammalian development, maturation and reproduction. These nutrients include a number of amino acids, vitamins, minerals and fatty acids. ‘Brain selective nutrients’ is a term that was coined to signify those nutrients that are needed for optimal brain development and that would therefore have facilitated human brain evolution (Cunnane and Crawford, 2003). Of course, it does not imply that these nutrients exist only in the brain or

The classical paradigm

Classically, hominin brain expansion has been linked to the development of the skills needed to efficiently make stone tools and use them for scavenging or hunting. The fresh meat thus acquired would have provided a better quality diet than in other primates. Stone tool making is generally acknowledged to have been common about two million years ago in Homo habilis. For some time now, it has also been generally understood that the brain has a high energy requirement, and that brain expansion

Shortcomings of the classical paradigm

Additional meat intake unquestionably increases the nutrient density of the diet, but the classical paradigm still has several important short-comings:

  • (i)

    Cart before the horse: A bigger brain clearly does need a better supply of dietary energy but something had to start the ball rolling; something must have permitted a degree of hominin brain expansion before (as well as after) the development of stone tools and hunting. What stimulated brain expansion enough to permit the conceptualisation of

Brain selective nutrients in the shore-based diet

A shore-based diet provided a richer supply of brain selective nutrients and thus helped relieve the nutritional constraint on hominin brain expansion because foods available on or near shores are generally excellent sources of DHA, iodine, iron, zinc, copper, selenium, vitamin A, and vitamin D. Shore-based foods include a large variety of nutritious plants, shallow freshwater fish such as catfish, crustaceans, shellfish, amphibians, and eggs of birds nesting on or near shorelines. Most

Shore-based habitat in the hominin fossil record

Starting at least two million years ago in East Africa, the fossil record shows that hominins destined to evolve larger brains on their way to becoming humans started to occupy shore-based habitats along freshwater lakes, marshes, rivers, estuaries and possibly some sea coasts (Cunnane and Stewart, 2010). Further examples of early hominins subsisting on shore-based foods, particularly freshwater fish and shellfish, are emerging from the work of several experienced groups of

Changes in other organ systems facilitated brain evolution

The hominin brain did not evolve in isolation from the rest of the body. Indeed, at least four other physiologic and/or metabolic changes helped pave the way for the modern human brain. First was the evolution of neonatal subcutaneous body fat, which was a crucial development before human brain evolution was possible (see previous section: Body fat: The infant brain's unique energy reserve). Amongst primates, fetal/neonatal body fat is unique to humans so, of these changes favouring brain

Discussion

Expansion of the hominin brain came at the cost of increasing neurodevelopmental vulnerability. Without evolving a way to mask or circumvent the increasing vulnerability of the developing hominin brain as it expanded, its evolution might have started but would not have been sustainable. The hominin fossil record shows that at least two million years ago, some populations of H. habilis were living around the big lakes and other water bodies of East Africa and frequently eating fish and shellfish

Acknowledgements

The ideas expressed here are our own, particularly the aspects linking human brain evolution to brain energetics, ketone metabolism and neonatal body fat. We coined the term ‘brain selective nutrients,’ but this aspect, especially in relation to DHA, is more interwoven with concepts discussed and distilled on many occasions with others. Continued support from Leo Standing (Bishop's University, Lennoxville, Quebec) has been most encouraging. Numerous students, collaborators and colleagues around

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