Global and regional brain metabolic scaling and its functional consequences

Karbowski, Jan

doi:10.1186/1741-7007-5-18

Cited by 137 publications

(186 citation statements)

References 104 publications

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“…Given that primate M BR scales linearly to its number of neurons (2, 3), a relationship that also applies to humans, great apes, and thus supposedly to extinct hominins (1,4), the finding that brain metabolism scales linearly with its number of neurons implies that, in primates, brain metabolism also scales linearly with brain size (8). This is in contrast to earlier reports that brain metabolism scaled more slowly than M BR , the results of which were skewed by combining primates and other mammals in the analysis under the assumption, now known to be wrong, that M BR scaled hypermetrically with number of neurons across all species (17,30). Because this is a much faster rate of scaling of brain metabolism than thus far acknowledged, it raises the possibility that metabolism may indeed have been a much more limiting factor than previously suspected to increasing numbers of brain neurons in evolution, particularly given that, across non-great-ape primates, M BR can scale linearly with M BD (2,3).…”

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confidence: 55%

“…The energetic viability of a nonhibernating primate species depends on the balance between the energy requirements associated to its M BD and its brain size, and its daily caloric intake (E IN ) during the hours available for eating. It has previously been considered that the energetic cost of the brain scales more slowly than M BR , varying with M BR 0.85 (29,30). Given that the metabolic cost of the body also scales less than linearly, with M BD 0.75 , and that M BR scales linearly at most, if not less than linearly, with M BD (3), it would suffice for the daily E IN to scale with M BD raised to an exponent of at least 0.85 for metabolism not to be a limiting factor to brain and body expansion in primate evolution-as long as there were enough hours in the day available for feeding.…”

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confidence: 99%

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Metabolic constraint imposes tradeoff between body size and number of brain neurons in human evolution

Fonseca-Azevedo

Herculano‐Houzel

2012

Proc. Natl. Acad. Sci. U.S.A.

154

120

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Despite a general trend for larger mammals to have larger brains, humans are the primates with the largest brain and number of neurons, but not the largest body mass. Why are great apes, the largest primates, not also those endowed with the largest brains? Recently, we showed that the energetic cost of the brain is a linear function of its numbers of neurons. Here we show that metabolic limitations that result from the number of hours available for feeding and the low caloric yield of raw foods impose a tradeoff between body size and number of brain neurons, which explains the small brain size of great apes compared with their large body size. This limitation was probably overcome in Homo erectus with the shift to a cooked diet. Absent the requirement to spend most available hours of the day feeding, the combination of newly freed time and a large number of brain neurons affordable on a cooked diet may thus have been a major positive driving force to the rapid increased in brain size in human evolution.encephalization | expensive tissue hypothesis | brain metabolism T he human brain is a linearly scaled-up primate brain in its relationship between brain size and number of neurons (1), having evolved while being subjected to the same cellular scaling rules that apply to primates as a whole (2, 3), including great apes (4). With the largest brain among primates, humans thus have the largest number of neurons among these and possibly all mammals (5), a number that we estimate to be close to three times larger than in gorillas and orangutans, owners of the next largest brains among extant primates (4). We are not outstanding primates, on the contrary, in body size: gorillas can grow to be three times larger than humans. This discrepancy between body and brain size led to the predominant view that encephalization (that is, a larger brain size than expected for body size) is the main characteristic that sets humans apart from other primates and mammals as a whole (6). Although a relatively large brain compared with body size is expected to bring cognitive advantages (6), and despite the well-documented evidence for an increase in brain size during human evolution (7), there is still no consensus on what mechanisms or reasons led to brain enlargement in the Homo lineage.Why are the largest primates not those endowed with the largest brains as well? Rather than evidence that humans are an exception among primates, we consider this disparity to be a clue that, in primate evolution, developing a very large body and a very large brain have been mutually excluding strategies, probably because of metabolic reasons (4, 8). The brain is the third most energy-expensive organ in the human body, ranking in total organ metabolic cost below only skeletal muscle and liver (9). Accordingly, several studies have suggested that the main constraints to increasing primate brain size in evolution are metabolic in nature (10-18). The human brain, in particular, has come to cost ∼20% of the total body resting metabolic rate, even though it ...

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confidence: 55%

mentioning

confidence: 99%

Metabolic constraint imposes tradeoff between body size and number of brain neurons in human evolution

Fonseca-Azevedo

Herculano‐Houzel

2012

Proc. Natl. Acad. Sci. U.S.A.

154

120

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“…Once numbers of neurons composing different rodent and primate brains were available, it became possible to estimate how the average metabolic cost per neuron scales with brain size and neuronal density. Contrary to expectations, dividing total glucose use per minute in the cerebral cortex or whole brain (69) by the number of brain neurons revealed a remarkably constant average glucose use per neuron across the mouse, rat, squirrel, monkey, baboon, and human, with no significant relationship to neuronal density and, therefore, to average neuronal size (70). This is in contrast to the decreasing average metabolic cost of other cell types in mammalian bodies with increasing cell size (71)(72)(73), with the single possible exception of muscle fibers (74).…”

Section: Scaling Of Glia/neuron Ratios and Metabolismmentioning

confidence: 96%

“…Second, the constant average energetic cost per neuron across species implies that larger neurons must compensate for the obligatory increased metabolic cost related to repolarizing the increased surface area of the cell membrane. This compensation could be implemented by a decreased number of synapses and/or decreased rates of excitatory synaptic transmission (69). Synaptic homeostasis and elimination of excess synapses [e.g., during sleep (77)], the bases of synaptic plasticity, might thus be necessary consequences of a tradeoff imposed by the need to constrain neuronal energetic expenditure (70).…”

Section: Scaling Of Glia/neuron Ratios and Metabolismmentioning

confidence: 99%

The remarkable, yet not extraordinary, human brain as a scaled-up primate brain and its associated cost

Herculano‐Houzel

2012

Proc. Natl. Acad. Sci. U.S.A.

493

372

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Neuroscientists have become used to a number of “facts” about the human brain: It has 100 billion neurons and 10- to 50-fold more glial cells; it is the largest-than-expected for its body among primates and mammals in general, and therefore the most cognitively able; it consumes an outstanding 20% of the total body energy budget despite representing only 2% of body mass because of an increased metabolic need of its neurons; and it is endowed with an overdeveloped cerebral cortex, the largest compared with brain size. These facts led to the widespread notion that the human brain is literally extraordinary: an outlier among mammalian brains, defying evolutionary rules that apply to other species, with a uniqueness seemingly necessary to justify the superior cognitive abilities of humans over mammals with even larger brains. These facts, with deep implications for neurophysiology and evolutionary biology, are not grounded on solid evidence or sound assumptions, however. Our recent development of a method that allows rapid and reliable quantification of the numbers of cells that compose the whole brain has provided a means to verify these facts. Here, I review this recent evidence and argue that, with 86 billion neurons and just as many nonneuronal cells, the human brain is a scaled-up primate brain in its cellular composition and metabolic cost, with a relatively enlarged cerebral cortex that does not have a relatively larger number of brain neurons yet is remarkable in its cognitive abilities and metabolism simply because of its extremely large number of neurons.

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Thermodynamic constraints on fiber diameter, neural activity, and brain temperature

Karbowski

2009

BMC Neurosci

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There have been suggestions that heat caused by cerebral metabolic activity may constrain mammalian brain evolution, architecture, and function [1][2][3][4]. This study [5] investigates physical limits on brain wiring and corresponding changes in brain temperature that are imposed by thermodynamics of heat balance determined mainly by Na/KATPase, cerebral blood flow, and heat conduction. It is found that even moderate firing rates cause significant intracellular Na build-up, and the ATP consumption rate associated with pumping out these ions grows nonlinearly with frequency. Surprisingly, the power dissipated by the Na/K pump depends biphasically on frequency, which can lead to the biphasic dependence of brain temperature on frequency as well. Both the total power of sodium pumps and brain temperature diverge for very small fiber diameters, indicating that too thin fibers are not beneficial for thermal balance. For very small brains blood flow is not a sufficient cooling mechanism deep in the brain. The theoretical lower bound on fiber diameter above which brain temperature is in the operational regime is strongly frequency dependent but finite due to synaptic depression. For normal neurophysiological conditions this bound is at least an order of magnitude smaller than average values of empirical fiber diameters, suggesting that mammalian brains operate in the thermodynamically safe regime. Analytical formulas presented can be used to estimate average firing rates in mammals, and relate their changes to changes in brain temperature, which can have important practical applications. In general, activity in larger brains is found to be slower than in smaller brains. References 1.Aiello

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Global and regional brain metabolic scaling and its functional consequences

Abstract: Background: Information processing in the brain requires large amounts of metabolic energy, the spatial distribution of which is highly heterogeneous, reflecting the complex activity patterns in the mammalian brain.

Cited by 137 publications

References 104 publications

Metabolic constraint imposes tradeoff between body size and number of brain neurons in human evolution

Metabolic constraint imposes tradeoff between body size and number of brain neurons in human evolution

The remarkable, yet not extraordinary, human brain as a scaled-up primate brain and its associated cost

Thermodynamic constraints on fiber diameter, neural activity, and brain temperature

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