Brief communication How much larger is the relative volume of area 10 of the prefrontal cortex in humans.код для вставкиСкачать
AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 118:399 – 401 (2002) Brief Communication: How Much Larger Is the Relative Volume of Area 10 of the Prefrontal Cortex in Humans? Ralph L. Holloway* Department of Anthropology, Columbia University, New York, New York 10027 KEY WORDS brain; frontal lobe; prefrontal cortex; area 10; residuals; allometry ABSTRACT It has long been thought that the prefrontal cerebral cortex has been greatly expanded in the human brain. Semendeferi et al. ( Am. J. Phys. Anthropol. 114:224 –241) showed that Brodmann’s area 10 is relatively larger in the human compared to pongid brains. The question is: how much larger relatively is it? Using their data, it can be shown that the relative increase for human prefrontal area 10 is only 6% larger. Looking at the data base of neural structures provided by Stephan et al. ( Folia Primatol. (Basel) 35:1–29), it is apparent that 6% is a relatively low residual value from a predicted value based on allometric considerations between total brain weight and any given neural structure. When this small increase is combined with their earlier findings on area 13 of prefrontal cortex (Semendeferi et al.  J. Hum. Evol. 32:375–388), it appears that the prefrontal cortex in humans is not some 200% larger as claimed by some researchers (Deacon  Symbolic Species, New York: W.W. Norton; cf. Holloway  Am Sci 86:184 – 186), and that the findings of Semendeferi et al. ( Am. J. Phys. Anthropol. 114:224 –241) are in agreement with the earlier work (Semendeferi and Damasio  J. Hum. Evol. 38:317–332; Semendeferi et al.  J. Hum. Evol. 32:375–388), showing that the human frontal lobe volume is what would be expected for a primate of its brain size. While the prefrontal cortex may have increased relatively in Homo sapiens, the increase is likely to have been far less than currently believed. Am J Phys Anthropol 118:399 – 401, 2002. © 2002 Wiley-Liss, Inc. In their recent research paper on a comparative study of Brodmann’s area 10 of the prefrontal cortex, Semendeferi et al. (2001, p. 224) showed that the human value for area 10 is “. . . larger relative to the rest of the brain than it is in apes.” This observation, if true when replicated with larger sample sizes, is an important empirical finding, particularly since Semendeferi and Damasio (2000), von Bonin (1948), and Holloway (1964, 1968) suggested that the frontal lobe of humans is essentially the size one would expect for a primate of its brain size. Thus one of the long-standing myths regarding relatively larger frontal lobes in humans appears to have been replaced with excellent empirical studies showing that the situation is more complex. Still outstanding, however, is the possibility that the prefrontal cerebral cortex might be enlarged in Homo relative to the great apes, for which Deacon (1997) has strongly argued, mostly on the basis of earlier tables by Brodmann (1909), based on surface areas and his cytoarchitectonic maps which were then used by Blinkov and Glezer (1969, their Table 196) to arrive at the relative expansion for Homo. Not all observations suggest this to be the case. Uylings and van Eden (1990), using Pongo as their pongid example, showed that frontal lobe expansion in Homo was not statistically significantly enlarged, and that the prefrontal cortex of Homo was almost exactly on the regression line for the primates in their sample, and that allometric slopes were essentially 1.0 These figures contrast strongly with those of Deacon (1997) (cf. Holloway, 1998), which suggested that the human prefrontal cortex expanded ⫹200% from a primate ancestor during hominid evolution. The work of Brodmann (1909), and the compilations of Blinkov and Glezer (1968), did not use allometry to test whether or not the absolute increases in surface area/volume of prefrontal cortex are really significantly larger than expected for a primate with a human brain size. Given the increasing perceived importance of the prefrontal cortex in human complex cognitive behavioral patterns coming out of MRI, fMRI, and PET studies, it would be useful to have a more accurate assessment of the volumetric differences between humans and pongids, to which Semendeferi et al. (2001) have been adding newer information. © 2002 WILEY-LISS, INC. MATERIALS AND METHODS Using the data base of both Semendeferi et al. (2001) and Stephan et al. (1981), the amount of *Correspondence to: Ralph L. Holloway, Department of Anthropology, Columbia University, New York, NY 10027. E-mail: firstname.lastname@example.org Received 16 April 2001; accepted 28 December 2001. DOI 10.1002/ajpa.10090 Published online in Wiley InterScience (www.interscience.wiley. com). 400 R.L. HOLLOWAY TABLE 1. Residuals for Homo sapiens of various neural nuclei, based on Stephan et al. (1981) (volumes in mm3) Structure Correlation Predicted Observed Difference % Difference Striatum Septum Thalamus Hippocampus Cerebellum Neocortex Medulla Mesencephalon Meninges Ventricles 0.994 0.983 0.995 0.954 0.992 0.998 0.988 0.994 0.946 0.956 48,394 2,095 25,288 10,863 131,226 1,126,181 16,745 9,214 14,688 8,934 28,689 2,610 18,222 10,287 137,421 1,006,530 9,622 8,087 13,205 18,732 ⫺19,705 515 ⫺7,066 ⫺576 6,195 ⫺119,651 ⫺7,123 ⫺1,127 ⫺1,483 9,798 ⫺68.7 19.7 ⫺38.78 ⫺5.6 4.51 ⫺11.89 ⫺74.03 ⫺13.94 ⫺11.23 52.31 relative increase of neural structures is calculated. Using the data of Semendeferi et al. (2001) on area 10 without the human data points, one can calculate the regression equation for available primate area 10. This equation allows one to calculate the expected human value based on the size of the brain. Subtracting the actual volume of area 10 from the expected volume provides a measure of the residual value, which can be compared with other known residuals from the large data base provided by Stephan et al. (1981) for other neural structures. In this case, the neural structures, e.g., the neocortex and cerebellum, had the log (base 10) values regressed against the log (base 10) of brain volume. Total brain volumes were not corrected, and included the volume of the particular structure, which in the case of the neocortex, varies from about 60 – 76% of total brain volume. The other structures are relatively small, and correcting them does not appreciably alter the residuals. RESULTS Table 2 of Semendeferi et al. (2001, p. 234) shows that in absolute terms, the human volume of area 10 is approximately seven times as large as the chimpanzee’s volume of area 10, and their Figure 7 (Semendeferi et al., 2001, p. 235) shows graphically the large absolute increment of human over other great ape volumes, being ca. 1.2% of brain volume in Homo, but only ca. 0.6 – 0.7% in the chimpanzee. However, their Figure 8, a log-log plot of volume of area 10 upon total brain volume, shows that the human point is almost exactly on the regression line they calculated. If one asks what the residual value is for the human value, using only the ape values and predicting what the expected human value of area 10 should be, the amount is 903.03 mm3. The equation for predicting the human volume is Y ⫽ ⫺ 5.808 ⫹ 1.639 共X兲 Where X is log base 10 volume, using only the five ape values for area 10 and their respective brain volumes, the predicted volume for Homo of area 10 would be 13,314.96 mm3, and the actual volume would be 14,218 mm3. Thus 共14,218 ⫺ 13315兲/14218 ⫽ .0635, or 6.35% This amount is certainly not dramatic, and we await more sampling before knowing whether 6% is indeed a significant relative increase. Put in the perspective of residuals known for other structures of the human brain, Table 1, based on the data set of Stephan et al. (1981), gives some examples of human residuals, expressed in percent difference between observed and predicted values. The human cerebellum comes closest, being 6.20% larger if all 44 species of primate are used, but ⫺9.5% if only anthropoids are used. The human neocortex is ⫺11.33% less than expected, and yet it is universally accepted that the human value of the neocortex lies directly on the total primate regression line of volume of the neocortex against total brain volume. There is no claim in the literature that these residuals are truly significant in a statistical way. More dramatic residuals are ⫺121% for the primary visual cortex (area 17) and ⫺144% for the lateral geniculate nucleus (for more examples, see Holloway, 1997), and these suggest that the residuals are significant. The 95% confidence intervals curve sharply away from the regression lines at the ends of the distributions when using log-log plots, making it difficult to assess significant departures. DISCUSSION The work being done by Semendeferi et al. (1997, 2001) is important and represents long-overdue and valuable additions to our understanding of comparative primate neurology and human brain evolution. As the residuals in Table 1 suggest, it is very likely that while brain size has important relationships with the conservation of various neural structures (e.g., see Finlay et al., 2001), there have been important shifts of other neural nuclei and fiber systems in the human brain during its evolutionary course, representing reorganization of the brain. It is quite likely that the human cerebral cortex has also undergone mosaic evolutionary changes, but it remains to be demonstrated exactly which regions have changed the most in terms of volumes, and cytoarchitectonic organization of layers and cell types. For the time being, however, I see these data as more strongly suggesting that it will be connectivity patterns rather than volumes of neural tissues that make the human brain distinct from those of our VOLUME OF AREA 10 OF HUMAN PREFRONTAL CORTEX pongid cousins. In any event, it is important to use allometric tests for residual values between observed and predicted volumes if we are to assess the relative increase or decreases of neural structures in both the comparative and evolutionary senses. ACKNOWLEDGMENTS I thank Chet Sherwood, Francys Subiaul, Michael Yuan, Doug Broadfield, and the anonymous reviewers for useful comments and suggestions. The views expressed here are solely those of the author. LITERATURE CITED Blinkov SM, Glezer II. 1968. The human brain in figures and tables. A quantitative handbook. New York: Plenum Press, Basic Books, Inc. Bonin G von. 1948. The frontal lobe of primates: cytoarchitectural studies. Frontal lobes. Res Bibl Ass Nerv Ment Dis 27:67– 83. Brodmann K. 1909. Vergleichende Lokalisationslehre der Grossrindhirne. Leipzig: Barth. Deacon T. 1997. The symbolic species: the co-evolution of language and the brain. New York: W.W. Norton & Co. Finlay BL, Darlington RB, Nicastro N. 2001. 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