The elaborate structure of the brain as the core unit of the nervous system in groups as diverse as cephalopods, insects and vertebrates implies that the brain's evolutionary history is of at least equal complexity.
Studies targeted at elucidating aspects of brain evolution involve a variety of approaches, with comparative and evolutionary perspectives complementing neuroscientific ones. From these, a set of general properties of brains have emerged, which shall be outlined here.
Vertebrate brain evolution
The classical view of telencephalic evolution proposes that the fish palaeostriatum is the antecedent of the human globus pallidus, the amphibian archistriatum is the antecedent of the human amygdala and the reptile neostriatum is the antecedent of the human caudate and putamen. Birds are thought to have unique additional basal ganglia, the hyperstriatum. Accordingly, the fish palaeocortex was thought to be the antecedent of the human olfactory cortex, the reptile archicortex to be the antecedent of the human hippocampus, while birds were proposed to have no further pallial regions. The neocortex was regarded as the unique and latest achievement of mammals. Since the 1960s and 1970s however, the classical view of brain evolution has been increasingly challenged. It is known that evolution is not linear, and thus one cannot assume that more recently evolved species are more advanced. According to the Avian Brain Nomenclature Consortium, the avian palaeostriatum augmentatum is homologous to the mammalian neostriatum, the avian palaeostriatum primitivum is homologous to the mammalian globus pallidus, and the avian hyperstriatum, neostriatum and archistriatum may be homologous to mammalian pallial regions. Moreover, recent findings suggest that mammals did not arise from reptiles, indicating that the reptilian nuclear pallial organisation cannot represent the ancestral conditions for mammals as was previously assumed. It is also known that telencephala of fish do not only contribute to olfactory functions and that fish have a hippocampus whose main function is not olfaction, but memory and spatial mapping. Overall, evidence indicates that there are pallial, striatal and pallidal structures in most or all vertebrates. It is apparent that the organisation of the basal ganglia amongst vertebrates is conserved, whereas the organisation of the pallial domains is more varied.
Evolution and Intelligence: What is different about the human brain?
A good measure of intelligence is mental or behavioural flexibility resulting in the appearance of novel solutions that are not part of the animal's normal repertoire. Among the many functions of the brain organ is the one of providing sensory imput for differentiating the set of mental contents, or mind. Thus brains differ among species, as required to survive in species-specific ecological circumstances, or niches. The species-specific minds, built upon the sensory imput from the respective brain, operate under general psychological conditions and upon neural correlates, whose change results in the highest-level regulated behavior; but brain architectures also generate complex reflexes and kinesias (behavioral patterns, often involved in courtship and prey capture) without or before psychological involvement. It is unclear if the refinement of these abilities should be included in the global concept of a species' intelligence. Of all the proposed neural correlates of intelligence, general properties such as brain size, relative brain size, encephalization and prefrontal cortex are not the optimal predictors for intelligence. It is the number of cortical neurons combined with a high conduction velocity that correlates best with intelligence. Humans do not have the largest brain or cortex (either in absolute or relative terms) but have the largest number of neurons and perhaps the greatest information processing capacity. In addition, highly specialized structures in the human prefrontal cortex may also play an important role.
As intelligence has evolved in different classes, orders and families of vertebrates, it does not seem to have evolved in an orthogenetic way (i.e. that a single line culminates in Homo sapiens for example) but in a parallel way. Amongst vertebrates, humans are more intelligent than great apes, cetaceans and elephants, while these species are probably more intelligent than monkeys, and monkeys more intelligent than prosimians and the remaining animals. On the other hand, it is not clear whether humans have unique properties. Aspects of the most discussed properties of human uniqueness (tool use, tool-making, grammatical language, consciousness, self-awareness, imitation, deception and theory of mind) are also recognized in other non- human primates and large-brained animals. Concerning the primate's ability to learn languages, the existence of precursors to Wernicke's area and Broca's area in non-human primates is currently being discussed.
Overall, the outstanding intelligence of humans seems not to have resulted from qualitative differences, but rather from a combination and subsequent improvement of characteristics, including the theory of mind, language and consciousness.
Evolution at genetic and molecular level
Considering the great similarity between the chimpanzee and human genome, evolutionary changes in anatomy are more likely based on changes in control mechanisms of gene expression rather than sequence changes in proteins.
Apparently, mutations with greater pleiotropic effects are a less common source of variation due to their deleterious effects. Several genetic features (gene duplication, regulatory sequence expansion and diversification, and alternative protein isoform expression) increase variation and minimize pleiotropy associated with evolutionary mutations by contributing to compartmentation and redundancy. These mechanisms arise in coding sequences, whereas variation in promotor use or choice of splicing site arises in regulatory sequences. Several studies indicate that evolutionary mutations of regulatory sequences take place at loci encoding transcription factors or cis-regulatory elements. These evolutionary mutations are responsible for gain, loss or modification of morphological traits and provide a mechanism to change one trait while preserving the role of pleiotropic genes in other processes. There are some examples of evolutionary changes in anatomy due to gene duplication and mutation in coding sequences (for example changes in HOX-proteins being associated with shifts in form or development mechanisms). However, these events are relatively rare and may have accompanying deleterious pleiotropic effects, thereby limiting their contribution to evolution under natural selection.
Overall, both regulatory sequences and coding regions contribute to the evolution of anatomy, but it can be concluded that morphological evolution occurs primarily through changes in regulatory sequences.
In contrast, there is ample evidence that changes arising in coding sequences play a crucial role in several important physiological differences between species. Regarding the synapse proteome, a great expansion of protein types due to gene family duplication and diversification has been revealed. Data suggests that most functional synaptic proteins were present in metazoans. This proto-synapse, with its signalling pathways responding to environmental cues and performing simple cell-cell communication, has been elaborated on during the evolution of invertebrates and vertebrates. It is very likely that the increase in complexity in molecular signalling of vertebrates, along with neuron number and connectivity, contributes to their great behavioural capacity. Even small changes in components of synaptic signalling have a great multiplicative effect on neuronal function. Moreover, comparisons of synapse- signalling complexes between Drosophila and mice indicate that additional species-specific adaptations of common synaptic subcomponents have diverged by duplication, recruitment and replacement of genes. Regional specialization with differential signal processing in mouse brains was also discovered. Different brain regions express a similar set of postsynaptic proteins, but in different combinations of expression levels. Recently-evolved genes encoding upstream molecules and structural components of signalling pathways seem to contribute most to diversity.
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- Jarvis, E.D.; Güntürkün, O.; Bruce, L.; Csillag, A.; Karten, H.; Kuenzel, W.; Medina, L.; Paxinos, G.; Perkel, D.J.; Shimizu, T.; Others, (2005). "Avian brains and a new understanding of vertebrate brain evolution". Nature Reviews Neuroscience 6: 151-159. DOI:10.1038/nrn1606. Abstract | Full Text
- Roth, G.; Dicke, U. (2005). "Evolution of the brain and intelligence". Trends in Cognitive Sciences 9 (5): 250-257. Full Text
- Abstract: Intelligence has evolved many times independently among vertebrates. Primates, elephants and cetaceans are assumed to be more intelligent than ‘lower’ mammals, the great apes and humans more than monkeys, and humans more than the great apes. Brain properties assumed to be relevant for intelligence are the (absolute or relative) size of the brain, cortex, prefrontal cortex and degree of encephalization. However, factors that correlate better with intelligence are the number of cortical neurons and conduction velocity, as the basis for information-processing capacity. Humans have more cortical neurons than other mammals, although only marginally more than whales and elephants. The outstanding intelligence of humans appears to result from a combination and enhancement of properties found in non-human primates, such as theory of mind, imitation and language, rather than from ‘unique’ properties.
- Sherwood, C.C.; Subiaul, F.; Zawidzki, T. (2008). "A natural history of the human mind: tracing evolutionary changes in brain and cognition". Journal of Anatomy 212 (4): 426-454. DOI:10.1111/j.1469-7580.2008.00868.x. Full Text
- Abstract: Since the last common ancestor shared by modern humans, chimpanzees and bonobos, the lineage leading to Homo sapiens has undergone a substantial change in brain size and organization. As a result, modern humans display striking differences from the living apes in the realm of cognition and linguistic expression. In this article, we review the evolutionary changes that occurred in the descent of Homo sapiens by reconstructing the neural and cognitive traits that would have characterized the last common ancestor and comparing these with the modern human condition. The last common ancestor can be reconstructed to have had a brain of approximately 300–400 g that displayed several unique phylogenetic specializations of development, anatomical organization, and biochemical function. These neuroanatomical substrates contributed to the enhancement of behavioral flexibility and social cognition. With this evolutionary history as precursor, the modern human mind may be conceived as a mosaic of traits inherited from a common ancestry with our close relatives, along with the addition of evolutionary specializations within particular domains. These modern human-specific cognitive and linguistic adaptations appear to be correlated with enlargement of the neocortex and related structures. Accompanying this general neocortical expansion, certain higher-order unimodal and multimodal cortical areas have grown disproportionately relative to primary cortical areas. Anatomical and molecular changes have also been identified that might relate to the greater metabolic demand and enhanced synaptic plasticity of modern human brain's. Finally, the unique brain growth trajectory of modern humans has made a significant contribution to our species' cognitive and linguistic abilities.
- Carroll, S.B. (2005). "Evolution at two levels: on genes and form". PLoS Biol 3 (7): e245. DOI:10.1371/journal.pbio.0030245. Free Full Text | Download PDF
- Emes, R.D.; Pocklington, A.J.; Anderson, C.N.G.; Bayes, A.; Collins, M.O.; Vickers, C.A.; Croning, M.D.R.; Malik, B.R.; Choudhary, J.S.; Armstrong, J.D.; Others, (2008). "Evolutionary expansion and anatomical specialization of synapse proteome complexity". Nature Neuroscience (6): pages to be defined. DOI:10.1038/nn.2135. Full Text
- Abstract: Understanding the origins and evolution of synapses may provide insight into species diversity and the organization of the brain. Using comparative proteomics and genomics, we examined the evolution of the postsynaptic density (PSD) and membrane-associated guanylate kinase (MAGUK)-associated signaling complexes (MASCs) that underlie learning and memory. PSD and MASC orthologs found in yeast carry out basic cellular functions to regulate protein synthesis and structural plasticity. We observed marked changes in signaling complexity at the yeast-metazoan and invertebrate-vertebrate boundaries, with an expansion of key synaptic components, notably receptors, adhesion/cytoskeletal proteins and scaffold proteins. A proteomic comparison of Drosophila and mouse MASCs revealed species-specific adaptation with greater signaling complexity in mouse. Although synaptic components were conserved amongst diverse vertebrate species, mapping mRNA and protein expression in the mouse brain showed that vertebrate-specific components preferentially contributed to differences between brain regions. We propose that the evolution of synapse complexity around a core proto-synapse has contributed to invertebrate-vertebrate differences and to brain specialization.