From monkeys to humans: what do we now know about brain homologies?IntroductionWhy a comparative approach remains importantThe pervasive effects of body sizeThe difficult cross-species morphing problemDefining visual areas by retinotopic mappingDelays and inhibitionVisual maps with non-retinotopic coordinatesSomatotopy and tonotopyDevelopment and evolutionAreas surrounding MT/V5Posterior superior occipital cortexParietal visual areasInferior areas anterior to VP/V3vFrontal visuomotor cortexConclusionsAcknowledgementsReferences and recommended readingFrom monkeys to humans: what do we now know aboutbrain homologies?Martin I Sereno and Roger BH TootellDifferent primate species, including humans, have evolved by arepeated branching of lineages, some of which have becomeextinct. The problem of determining the relationships amongcortical areas within the brains of the surviving branches (e.g.humans, macaque monkeys, owl monkeys) is difficult forseveral reasons. First, evolutionary intermediates are missing,second, measurement techniques are different in differentprimate species, third, species differ in body size, and fourth,brain areas can duplicate, fuse, or reorganize between andwithin lineages.AddressesDepartment of Cognitive Sciences, University of California,San Diego, La Jolla, CA 92093-0515, USACorresponding author: Sereno, MI ([email protected])Current Opinion in Neurobiology 2005, 15:135–144This review comes from a themed issue onCognitive neuroscienceEdited by Angela D Friederici and Leslie G UngerleiderAvailable online 18th March 20050959-4388/$ – see front matter# 2005 Elsevier Ltd. All rights reserved.DOI 10.1016/j.conb.2005.03.014IntroductionThe detailed homology of brain regions among monkeys,apes and humans is intrinsically interesting to evolution-ary biologists. But as humans, we also have a particularinterest in brain regions that are similar enough amongthese groups that studies of their non-human counterpartsmight be directly relevant to human cognition. Brainregions in humans that have changed substantially fromthose in other primates are also intriguing. Here, we beginby reviewing methodological issues and then considercurrent ideas about the homologies of cortical areas inprimates with a focus on vision.Why a comparative approach remainsimportantInvasive anatomical and physiological experiments can becarried out routinely only in a small number of species ofnon-human, non-ape primates. In practice, these experi-ments have been limited to one loris (Galago), severalNew World monkeys (Cebus, Aotus, Saimiri, Callithrix) andone Old World monkey (Macaca). Apart from lesser apesand great apes, macaque monkeys come from the groupmost closely related to humans; thus, they are the naturalmodel system for humans. However, the last commonancestor of humans and macaques dates back to morethan 30 million years ago [1]. Since that time, New andOld World monkey brains have evolved independentlyfrom the brains of apes and humans, resulting in a com-plex mix of shared and unique features of the brain ineach group [2].Evolutionary biologists are often interested in sharedderived characters — i.e. specializations that havediverged from a basal condition that are peculiar to aspecies or grouping of species. Such divergent featuresare important for classification (e.g. a brain area that isunique to macaque-like monkeys, but not found in anyother primate group). Evolutionary biologists also distin-guish similarities caused by inheritance (homology), fromsimilarities caused by parallel or convergent evolution(homoplasy — a similar feature that evolved in parallel intwo lineages, but that was not present in their lastcommon ancestor). An example of homoplasy comes fromlayer 4A of primary visual cortex, which stains densely forcytochrome oxidase in virtually all New and Old Worldmonkeys, indicating that the common ancestor of thisgroup probably had this feature. Layer 4A in apes andhumans, by contrast, stains lightly for cytochrome oxi-dase. But one New World monkey, the owl monkey, alsohas a lightly stained layer 4A. Given the distribution ofthis feature, it is likely that owl monkeys evolved thisfeature in parallel with apes and humans [3].By contrast with taxonomists, neuroscientists are usuallyinterested in trying to determine which features areconserved across species (whether by inheritance or par-allel evolution), indicating that those features might havea basic functional and/or developmental role. The onlyway to obtain either of these kinds of information is toexamine data from multiple species.The power of the comparative approach was re-empha-sized in the study of ocular dominance columns in areaV1. Originally thought to be related to stereo vision, suchcolumns were visualized and experimentally manipulatedin macaque monkeys by monocular deprivation, and wereshown to be absent in ‘lower’ mammals such as the rat.Then it was revealed that some New World monkeys (e.g.squirrel monkeys) have poorly organized ocular domi-nance columns. This initially made sense because of animplicit ‘Great Chain of Being’ assumption: macaques arethe next ‘level up’ from squirrel monkeys, and should,therefore, be less well organized, in similar way to ‘lower’www.sciencedirect.com Current Opinion in Neurobiology 2005, 15:135–144mammals. However, squirrel monkeys appear to havegood stereo vision [4]. Recent studies have shown thatV1 exhibits either well-defined ocular dominance col-umns or well-defined angioscotomas (cortical images ofthe retinal blood vessel pattern unique to each eye), butnot both, even within a species [5]. It is thus possible thatrather than being involved in stereo vision, the presenceor absence of ocular dominance columns reflects twodifferent possible stable outcomes — both equally useful— of the competitive growth of two sets of activity-dependent axon terminals (contralateral and ipsilateral)in the context of both of them having to maintain a highresolution retinotopic map [6]. There might even be anadvantage to not having well-defined ocular dominancecolumns, because their absence reduces the lateral dis-placement on the V1 retinotopic map of the two copies ofinformation from the left and right eyes [7]. Consistentwith this idea, the visuotopic map in squirrel monkey 4Cwas found to be so precise that retinal blood vesselpatterns generating shadows only 3 cones wide wereresolved [5].The fact that some primate species do not