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COMMENTARYAbsolutebrainsize:Didwethrowthebabyoutwiththebathwater?Lori Marino*Neuroscience and Behavioral Biology Program, 1462 Clifton Road, Suite 304, Emory University, Atlanta, GA 30322he recent study by Sherwood et species’ brain is devoted to cognitive dicted by the allometric scaling inherental. (1) in this issue of PNAS is processes. But could we have, at the in the enlargement of the human brain.a study in irony. It is thus so very least, missed something important In other words, Sherwood et al. (1) showTbecause the authors used some about absolute brain size in the process? that overall or absolute brain size con-of the most current and sophisticated Did we throw the baby out with the stitutes a key factor in the ratio of gliahistological and data-analytic tools to, in bathwater? The Sherwood et al. (1) to neurons. The authors suggest that thethe end, unearth...adinosaur. Now the study suggests that we might have. greater numbers of glia in the humanauthors did not do this in the literal Recent microarray studies have shown neocortex may be due to the increasedsense. Rather, they laid bare an ‘‘ex- that neuronal signaling and energy pro- energetic costs of larger dendritic arborstinct’’ measure of brain anatomy: that duction genes are up-regulated in the and longer fiber projections within theold fossil known as absolute brain size. human neocortex compared with the context of the large human brain. TheEven as far back as the 1800s, Alex- great ...
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Absolute brain size: Did we throw the baby out with the bathwater? Lori Marino* Neuroscience and Behavioral Biology Program, 1462 Clifton Road, Suite 304, Emory University, Atlanta, GA 30322 Thabaldsseomtnecdutseredoo.ySybrwheeufoissstnih1(i)inirtudyissPNASeossuhtsitI.ynosuorthauheetuscaeet?saetrbtboadreouoltoocsnegvtoitvlilpaerecieshabrtaidnisdevhSe,ewdhw,reovoahethtwarrreovsedceroeIsnsosteuht.Bulcohgtnfmoitteniehmneagartaolpnterestth,imnyleadsomissestcnaicetzeiisrnslelmcoorhpteaheseodabbyudtibcotaibrteluspeiltnumniasglho)sntwrehein( of the most current and sophisticated Did we throw the baby out with the stitutes a key factor in the ratio of glia histological and data-analytic tools to, in bathwater? The Sherwoodet al neurons. The authors suggest that the to. (1) the end, unearth . . . a dinosaur. Now the study suggests that we might have. greater numbers of glia in the human authors did not do this in the literal Recent microarray studies have shown neocortex may be due to the increased sense. Rather, they laid bare an ‘‘ex- that neuronal signaling and energy pro- lar er dendritic a tinctmeasureofbrainanatomy:thatductiongenesareup-regulatedintheenergeticcostsrofgctionswirbors oldfossilknownasabsolutebrainsize.humanneocortexcomparedwiththecaonndtleoxtngoefrtfhiebelarpgreojheumanbratihni.nTthhee Even as far back as the 1800s, Alex- great apes (6, 7). These findings suggest is that Sherwoodet1 anderBrandt(2)and,abitlater,Ottothattherewasselectionforhigherratessbhoottwotmhalitntehehumanbrainconfoarl).(ms Snell (3) demonstrated the importance of energy expenditure in human neocor- ammalian att ofscalingthebraintobodysize,signal-texcomparedwithinotherprimates(8).thoigthheerggleinaernaelurmonratioswipthlearrngeorf ing the impending demise of absolute One way to measure metabolic support brains. brain size as a valid measure of brain Furthermore S capacity. The final death knell wasAbsolute brain sizetehwtreherehrew,ehwroodterminedeetralg.i(e1)adloe-n struck in its most popular form by differen Harry Jerison, who reminded us once ces in glia–neuron ratios across again that brain– body allometry plays a humans and nonhuman primates in cor-major role in the size of any species’constitutes a keytical regions associated with specific hu-brain. He effectively argued that the man abilities, such as area 44, a key area brain, like any other organ, scales withfactor in the ratiofor language production, and area 32, body size, and the validity of the use of which is active during theory-of-mind brain size as a measure of intelligenceof glia to neurons.tasks in humans. Sherwoodet al. (1) orinformationprocessingcapacityrestsfionutnhdesneocrsiitgicniaflicaarnetasspaencdiessudgigfefsetrethnactes upon the size of the brain relative to the for neurons is by examining the ratio of sizeofthebody.Heintroducedtheen-gliatoneurons.Thedistributiondensi-tthheeseenreerggieotincss,hofavferobnetealnclaorrgteelxy,cevoenn-in cephalization quotient (EQ) as a proper ties of glia provide an indication of the measure of relative brain size across metabolic demand of neighboring neu- served over the past 25 million years of species (4). EQ is a number that essen- rons. Sherwoodet al..h.:goc-gmunadetagesti)inv.(1kinissrtoiinlcsulconeralirov.Thenoituloveniarbetmarip tially quantifies how much larger or whether glial cell densities are rela-smaller the average brain size of a given tively higher in human frontal cortex nitive and linguistic specializations have speciesisrelativetotheexpectedbraincomparedwithotherprimates.Theyemergteivdebfyunelcatiboonrsatoifngthoenphriegfrhoern-toarlder size based on body size. Likewise, the reasoned that significantly higher glia– execu regressionacrossasampleofspeciesplifythekindofuniquetraitthatwouldSmhaerewoodet al. (1) provide support provides similar information. And, al- provide a basis for human intelligence. though different authors have different However, the Sherwoodet al. (1) study for the idea that the human brain is theoreticaljustificationsfortheparame-ismuchmorethanastudyincelldensi-cmaonrebeorunledsesrsatolaordgeinhtohmatincooindtberxat.inHaonwd-ters of the brain– body size relationship ties, metabolism, and allometry. What across species [see Deaneret al ever, these findings also engender many makes this article so compelling is that. (5) for review],allmeasuresofrelativebrainithasprofoundimplicationsforthetqwueesetniobnrsaianbosiuztetahnedrecloagtinoitnisohni.pIbfeh-u-size are based on the common assump- question of neurobiological continuity tion that it is only meaningful to con- across species, particularly across hu- man brains fall in line with generally sider brain size if body size, or some mans and our closest nonhuman rela- expected patterns of relationship among relative measure, is taken into account. tives, the great apes. It addresses the overall size, neuron density, and glia– Therefore, nowadays, absolute brain size general question of whether human neuron ratios and yet possess a number as a measure of cognitive capacity is brains should best be thought of as large of striking cognitive features, how considered obsolete. hominoid brains, or, alternatively, as a should the absolute size of brains be However, in the rush to abandon ab- singularly endowed product of evolution interpreted? What happens to brains solute brain size in favor of measures of somewhat apart from the rest of primate when they enlarge over time? How can relative brain size, have we been alto- brain evolution. gether too hasty? Well, no, not entirely. Sherwoodet al. (1), did indeed find There are valid reasons for taking into that the human frontal cortex displaysThe author declares no conflict of interest. account the allometric relationship a higher ratio of glia to neurons than inSee companion article on page 13606. between brain and body size when at- other primates. However, and impor-*E-mail: tempting to infer how much of any tantly, this relative difference is pre-© 2006 by The National Academy of Sciences of the USA
PNASSeptember 12, 2006vol. 103no. 3713563–13564
these changes provide a substrate for changes in cognitive abilities? When More Is More than Just More When brains enlarge, they can do so in a couple of different ways. They may add more neurons or make existing neu-rons larger, or some combination of both. However, both of these changes pose design problems that need to be solved because larger neurons have longer axons and dendrite conduction times will be slower. When the number of neurons increases, it becomes more difficult for each individual neuron to maintain connectivity. Therefore, brains cannot enlarge (either by adding neu-rons or by making them bigger) without the organization of the brain changing. The main way most mammal brains have enlarged is by increasing modular-ity to accommodate increases in the number of neurons. Increased modular-ity increases the number of processing areas. Indeed, there is substantial evi-dence that mammals with more neocor-tex possess more cortical areas and more units of parcellation (e.g., col-umns, etc.) than smaller-brained mammals (9).
So enlarged brains can support in-creases in cognitive ability because they may be more highly segmented and dif-ferentiated, thereby possessing more complexity than their smaller counter-parts. This is a case of more being more than just more. Enlarged brains not only have more neurons, they also have greater complexity, which is more than just more. Therefore, brain enlargement, and the increases in complexity that necessarily accompany it, may provide the substrate for enhanced cognitive abilities or even the emergence of new cognitive abilities. In this context, abso-lute brain size regains its value as a brain metric because it becomes a proxy for increased organizational complexity. So maybe it should be retrieved from the bathwater! Implications for Neurobiological Continuity The deep fundamental insight supported by Sherwoodet al. (1) is that the human brain is not unique or anomalous. Rather, the human brain is a product of changes in brain anatomy that are well predicted by scaling expectations for any nonhuman anthropoid primate. The
study by Sherwoodet al. (1) is a particu-larly elegant example of a growing body of evidence for this conclusion. For in-stance, several studies have shown that the human frontal cortex occupies the same proportion of total cortex in hu-mans as it does in great apes (10, 11). Therefore, humans are typical primates with regard to the portion of their cor-tex devoted to frontal cortex. Similarly, the human brain possesses the degree of cortical gyrification expected for a pri-mate of our brain size (12). These find-ings show that there are ways to obtain new or enhanced cognitive abilities in human brains that are perfectly consis-tent with the way brain evolution oc-curred in other primates. [To be fair, there is also evidence that the human brain might depart from certain allomet-ric expectations (13).] Regardless of which features of the human brain are typical of other pri-mate brains, the more general point is that a consideration of absolute brain size provides insight into which features of the human brain are predictable and which are not. Therefore, absolute brain size has turned out to be an important variable in its own right for understand-ing mammalian brain evolution.
1. Sherwood CC, Stimpson CD, Raghanti MA, Wild-Brain Behav Evol55:44-52. Goodman M (2004)Trends Genet20:578-585. man DE, Uddin M, Grossman LI, Goodman M, 6. Uddin M, Wildman DE, Liu G, Xu W, Johnson 9. Kaas JH (1993)Perspect Dev Neurobiol1:101-107. Redmond JC, Bonar CJ, Erwin JM, Hof PR RM, Hof PR, Kapatos G, Grossman LI, Good- 10. Semendeferi K, Lu A, Damasio H (2002)Nat (2006)Proc Natl Acad Sci USA103:13606-13611. man M (2004)Proc Natl Acad Sci USA101:2957-Neurosci5:272-276. 2. Brandt A (1867)Bull Soc Imp Nat Moscou40:525-543. 2962. 11. Bush EC, Allman JM (2004)Proc Natl Acad Sci 3. Snell O (1891)Sitz Ges Morph Physiol (Munchen) M, Lachuer J, Zapala MA, Redmond JC,7. CaceresUSA101:3962-3966. 7:90-94. Kudo L, Geschwind DH, Lockhart DJ, Preuss T, 12. Zilles K, Armstrong E, Moser KH, Schleicher A, 4. Jerison HJ (1973)The Evolution of the Brain andBarlow C (2003)Proc Natl Acad Sci USAStephan H (1989)Brain Behav Evol34:143-150. Intelligence(Academic, New York). Rilling JK, Insel TR (1999) 100:13030-13035. 13.J Hum Evol37: 5. Deaner RO, Nunn CL, van Schaik CP (2000) 8. Grossman LI, Wildman DE, Schmidt TR, 191-223.
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