The Human Brain in Numbers: A Linearly Scaled-Up Primate Brain (Herculano-Houzel 2009) PDF

REVIEW ARTICLE published: 09 November 2009 HUMAN NEUROSCIENCE doi: 10.3389/neu...

REVIEW ARTICLE published: 09 November 2009 HUMAN NEUROSCIENCE doi: 10.3389/neuro.09.031.2009 The human brain in numbers: a linearly scaled-up primate brain Suzana Herculano-Houzel* Instituto de Ciências Biomédicas, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brasil Edited by: The human brain has often been viewed as outstanding among mammalian brains: the most Andreas Jeromin, cognitively able, the largest-than-expected from body size, endowed with an overdeveloped Allen Institute for Brain Science, USA cerebral cortex that represents over 80% of brain mass, and purportedly containing 100 billion Reviewed by: Karl Herrup, neurons and 10× more glial cells. Such uniqueness was seemingly necessary to justify the Case Western University, USA superior cognitive abilities of humans over larger-brained mammals such as elephants and whales. Robert Barton, However, our recent studies using a novel method to determine the cellular composition of the University of Durham, UK brain of humans and other primates as well as of rodents and insectivores show that, since *Correspondence: different cellular scaling rules apply to the brains within these orders, brain size can no longer Suzana Herculano-Houzel, Laboratório de Neuroanatomia Comparada, be considered a proxy for the number of neurons in the brain. These studies also showed that Instituto de Ciências Biomédicas, the human brain is not exceptional in its cellular composition, as it was found to contain as many Universidade Federal do Rio de neuronal and non-neuronal cells as would be expected of a primate brain of its size. Additionally, Janeiro, Rua Carlos Chagas Filho 373, the so-called overdeveloped human cerebral cortex holds only 19% of all brain neurons, a 21950-902 Rio de Janeiro, Rio de Janeiro, Brazil. fraction that is similar to that found in other mammals. In what regards absolute numbers of e-mail: [email protected] neurons, however, the human brain does have two advantages compared to other mammalian brains: compared to rodents, and probably to whales and elephants as well, it is built according to the very economical, space-saving scaling rules that apply to other primates; and, among economically built primate brains, it is the largest, hence containing the most neurons. These findings argue in favor of a view of cognitive abilities that is centered on absolute numbers of neurons, rather than on body size or encephalization, and call for a re-examination of several concepts related to the exceptionality of the human brain. Keywords: brain scaling, number of neurons, human, encephalization INTRODUCTION to such great lengths to affirm, and teach, that evolution is the THE HUMAN BRAIN AS A SPECIAL BRAIN origin of diversity in life, and to find trends and laws that apply to What makes us human? Is our brain, the only one known to study kingdoms, phyla and orders as a whole, why then insist that what- other brains, special in any way? According to a recent popular ever scaling rules apply to other primates must not apply to us? account of what makes us unique, “we have brains that are bigger than In view of the vexing size inferiority in brain size and of the lack expected for an ape, we have a neocortex that is three times bigger of information about what our brains are actually made of – and than predicted for our body size, we have some areas of the neocortex how that compares to other brains, particularly those of whales and and the cerebellum that are larger than expected, we have more white elephants – resorting to a quest for uniqueness may have seemed matter” – and the list goes on (Gazzaniga, 2008). Most specialists as a necessary, natural step to justify the cognitive superiority of seem to agree (for example, Marino, 1998; Rilling, 2006; Sherwood the human brain. et al., 2006). Since ours is obviously not the largest brain on Earth, our Recently, a novel quantitative tool developed in our lab superior cognitive abilities cannot be accounted for by something as (Herculano-Houzel and Lent, 2005) has finally made the num- simple as brain size, the most readily measurable parameter regarding bers of neurons and non-neuronal cells that compose the brains the brain. Emphasis is thus placed on an exceptionality that is, curi- of various mammals, humans included, available for comparative ously, not brain-centered, but rather body-centered: With a smaller analysis. This review will focus on such a quantitative, compara- body but a larger brain than great apes, the human species deviates tive analysis, with emphasis on the numbers that characterize the from the relationship between body and brain size that applies to human brain: what they are, how they have been viewed in the past, other primates, great apes included, boasting a brain that is 5–7× too and how they change our view of where the human brain fits into large for its body size (Jerison, 1973; Marino, 1998). Recent efforts the diversity of the mammalian nervous system. to support this uniqueness have focused on finding genetic differ- ences between humans and other primates (reviewed in Vallender, THE HUMAN BRAIN IN NUMBERS 2008), as well as cellular particularities such as the presence and How many neurons does the human brain have, and how does distribution of Von Economo neurons (Nimchinsky et al., 1999; but that compare to other species? Many original articles, reviews and see Butti et al., 2009; Hakeem et al., 2009). textbooks affirm that we have 100 billion neurons and 10 times To regard the human brain as unique requires considering it more glial cells (Kandel et al., 2000; Ullian et al., 2001; Doetsch, to be an outlier: an exception to the rule, whatever that rule is. 2003; Nishiyama et al., 2005; Noctor et al., 2007; Allen and Barres, This makes little sense, however, in light of evolution. If we go 2009), usually with no references cited. This leaves the reader with Frontiers in Human Neuroscience www.frontiersin.org November 2009 | Volume 3 | Article 31 | 1 Herculano-Houzel The human brain in numbers the impression that the cellular composition of the human brain has However, the correlation between absolute brain size and long been determined. Indeed, an informal survey with senior neu- cognitive abilities breaks down when species of similar brain size are roscientists that we ran in 2007 showed that most believed that the compared across orders. Monkeys, for instance, possess brains that number of cells in the human brain was indeed already known: that are much smaller than those of ungulates, but the higher cognitive we have about 100 billion neurons, outnumbered by about 10 times and behavioral flexibility of monkeys over ungulates is anecdotally more glial cells – but none of the consulted scientists could cite an evident to any observer who compares the ingenious and complex original reference for these numbers (Herculano-Houzel and Lent, abilities of macaques to those of cows or horses, even though the unpublished observations). Curiously, the widespread concept that latter have 4–5× larger brains than macaques. For similar-sized neurons represent about 10% of all cells in the human brain might brains, rodents also perform more poorly than primates: With a be one of the arguments behind the popular, but mistaken, notion brain of only 52 g, the behavioral, social and cognitive repertoire of that we only use 10% of our brain (Herculano-Houzel, 2002). the capuchin monkey is outstanding compared to the capybara, a The reason for such lack of references is that indeed there was, giant Amazonian rodent (MacDonald, 1981), even though the latter to our knowledge, no actual, direct estimate of numbers of cells has a larger brain of 75 g. This is reminiscent of the most striking and or of neurons in the entire human brain to be cited until 2009. troubling discrepancy regarding brain size and cognitive abilities: A reasonable approximation was provided by Williams and Herrup that between humans and larger-brained species such as whales and (1988), from the compilation of partial numbers in the literature. elephants. If the latter have brains that are up to six times larger than These authors estimated the number of neurons in the human brain a human brain, why should we be more cognitively able? Answering at about 85 billion: 12–15 billion in the telencephalon (Shariff, this question requires a direct examination of the numbers of neu- 1953), 70 billion in the cerebellum, as granule cells (based on Lange, rons that compose the brains of humans and other species. 1975), and fewer than 1 billion in the brainstem. With more recent estimates of 21–26 billion neurons in the cerebral cortex (Pelvig BRAIN AND BODY SCALING: THE TRADITIONAL VIEW et al., 2008) and 101 billion neurons in the cerebellum (Andersen ASSUMPTION 1: BODY SIZE MATTERS et al., 1992), however, the total number of neurons in the human If the smaller size of the human brain compared to elephant and brain would increase to over 120 billion neurons. whale brains (Figure 1) translates into a smaller number of neu- As to the 10 times more numerous glial cells in the human rons in the human brain than in the latter, then what makes the brain, that seems to be the case only in subcortical nuclei such as human brain outstanding in its cognitive abilities? In the absence the thalamus (17 glial cells per neuron) and the ventral pallidum of direct estimates of numbers of neurons in these and other spe- (12 glial cells per neuron; Pakkenberg and Gundersen, 1988). In the cies, the search for a neural correlate for human capacities has gray matter of the cerebral cortex, glial cells outnumber neurons placed emphasis on the characteristic that most undisputedly places by a factor of