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Global and regional brain metabolic scaling and its functional consequences.

Karbowski J - BMC Biol. (2007)

Bottom Line: 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.The exception is white matter, the metabolism of which seems to scale with a standard specific exponent of -1/4.The neurophysiological factors that might account for the regional uniformity of the exponents and for the excessive scaling of the total brain metabolism are discussed, along with the relationship between brain metabolic scaling and computation.

View Article: PubMed Central - HTML - PubMed

Affiliation: Sloan-Swartz Center for Theoretical Neurobiology, Division of Biology 216-76, California Institute of Technology, Pasadena, CA 91125, USA. jkarb@its.caltech.edu

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.

Results: In this study, it was found, based on empirical data, that despite this heterogeneity, the volume-specific cerebral glucose metabolic rate of many different brain structures scales with brain volume with almost the same exponent: around -0.15. The exception is white matter, the metabolism of which seems to scale with a standard specific exponent of -1/4. The scaling exponents for the total oxygen and glucose consumptions in the brain in relation to its volume are identical, at 0.86 +/- 0.03, which is significantly larger than the exponents 3/4 and 2/3 that have been suggested for whole body basal metabolism on body mass.

Conclusion: These findings show explicitly that in mammals: (i) volume-specific scaling exponents of the cerebral energy expenditure in different brain parts are approximately constant (except brain stem structures), and (ii) the total cerebral metabolic exponent against brain volume is greater than the much-cited Kleiber's 3/4 exponent. The neurophysiological factors that might account for the regional uniformity of the exponents and for the excessive scaling of the total brain metabolism are discussed, along with the relationship between brain metabolic scaling and computation.

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Scaling of the volume-specific glucose utilization rate in subcortical gray matter with brain volume. The specific metabolic scaling exponent had the following values: (A) -0.15 for thalamus (y = -0.15x + 0.03); (B) -0.14 for hippocampus (y = -0.14x - 0.13), which represents limbic structures; (C) -0.15 for caudate (y = -0.15x + 0.02), which represents basal ganglia; (D) -0.15 for cerebellum (y = -0.15x - 0.09).
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Figure 3: Scaling of the volume-specific glucose utilization rate in subcortical gray matter with brain volume. The specific metabolic scaling exponent had the following values: (A) -0.15 for thalamus (y = -0.15x + 0.03); (B) -0.14 for hippocampus (y = -0.14x - 0.13), which represents limbic structures; (C) -0.15 for caudate (y = -0.15x + 0.02), which represents basal ganglia; (D) -0.15 for cerebellum (y = -0.15x - 0.09).

Mentions: Some subcortical structures of gray matter use half of the energy used in the cortex (e.g., limbic structures in cat and monkey; see Clarke and Sokoloff [5] and Additional file 1), yet almost all of them exhibit a similar scaling homogeneity, with metabolic specific exponents also around -0.15 (Figure 3, Table 1). The volume-specific metabolisms of two brain stem structures (the superior colliculus, involved in visual coordination, and the inferior colliculus, involved in auditory processing) seem to be exceptions, as they scale with brain size with the exponent of approximately 0 (Table 1). This might be caused by their highly variable activities (see Additional file 1), and we do not know how other brain stem structures behave. The high degree of allometric uniformity for the most of the subcortical system is even more striking than that for the cortex, as subcortical regions are much more diverse in function and biophysical properties than cortical areas. For example, the thalamus and hippocampus play very different roles in the brain, the former mediating sensory input to the cortex, whereas the latter is implicated in memory processes, yet their scaling exponents and corresponding confidence intervals are almost identical (Figure 3A,B and Table 1).


Global and regional brain metabolic scaling and its functional consequences.

Karbowski J - BMC Biol. (2007)

Scaling of the volume-specific glucose utilization rate in subcortical gray matter with brain volume. The specific metabolic scaling exponent had the following values: (A) -0.15 for thalamus (y = -0.15x + 0.03); (B) -0.14 for hippocampus (y = -0.14x - 0.13), which represents limbic structures; (C) -0.15 for caudate (y = -0.15x + 0.02), which represents basal ganglia; (D) -0.15 for cerebellum (y = -0.15x - 0.09).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC1884139&req=5

Figure 3: Scaling of the volume-specific glucose utilization rate in subcortical gray matter with brain volume. The specific metabolic scaling exponent had the following values: (A) -0.15 for thalamus (y = -0.15x + 0.03); (B) -0.14 for hippocampus (y = -0.14x - 0.13), which represents limbic structures; (C) -0.15 for caudate (y = -0.15x + 0.02), which represents basal ganglia; (D) -0.15 for cerebellum (y = -0.15x - 0.09).
Mentions: Some subcortical structures of gray matter use half of the energy used in the cortex (e.g., limbic structures in cat and monkey; see Clarke and Sokoloff [5] and Additional file 1), yet almost all of them exhibit a similar scaling homogeneity, with metabolic specific exponents also around -0.15 (Figure 3, Table 1). The volume-specific metabolisms of two brain stem structures (the superior colliculus, involved in visual coordination, and the inferior colliculus, involved in auditory processing) seem to be exceptions, as they scale with brain size with the exponent of approximately 0 (Table 1). This might be caused by their highly variable activities (see Additional file 1), and we do not know how other brain stem structures behave. The high degree of allometric uniformity for the most of the subcortical system is even more striking than that for the cortex, as subcortical regions are much more diverse in function and biophysical properties than cortical areas. For example, the thalamus and hippocampus play very different roles in the brain, the former mediating sensory input to the cortex, whereas the latter is implicated in memory processes, yet their scaling exponents and corresponding confidence intervals are almost identical (Figure 3A,B and Table 1).

Bottom Line: 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.The exception is white matter, the metabolism of which seems to scale with a standard specific exponent of -1/4.The neurophysiological factors that might account for the regional uniformity of the exponents and for the excessive scaling of the total brain metabolism are discussed, along with the relationship between brain metabolic scaling and computation.

View Article: PubMed Central - HTML - PubMed

Affiliation: Sloan-Swartz Center for Theoretical Neurobiology, Division of Biology 216-76, California Institute of Technology, Pasadena, CA 91125, USA. jkarb@its.caltech.edu

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.

Results: In this study, it was found, based on empirical data, that despite this heterogeneity, the volume-specific cerebral glucose metabolic rate of many different brain structures scales with brain volume with almost the same exponent: around -0.15. The exception is white matter, the metabolism of which seems to scale with a standard specific exponent of -1/4. The scaling exponents for the total oxygen and glucose consumptions in the brain in relation to its volume are identical, at 0.86 +/- 0.03, which is significantly larger than the exponents 3/4 and 2/3 that have been suggested for whole body basal metabolism on body mass.

Conclusion: These findings show explicitly that in mammals: (i) volume-specific scaling exponents of the cerebral energy expenditure in different brain parts are approximately constant (except brain stem structures), and (ii) the total cerebral metabolic exponent against brain volume is greater than the much-cited Kleiber's 3/4 exponent. The neurophysiological factors that might account for the regional uniformity of the exponents and for the excessive scaling of the total brain metabolism are discussed, along with the relationship between brain metabolic scaling and computation.

Show MeSH
Related in: MedlinePlus