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Wed, Aug. 6th, 2008, 01:59 pm
Cerebral assymetry in an evolutionary perspective


When I started this blog, using it as a tool for criticism of popular psychological ideas was not the main motivation. However, since Hodos and Campbell released their first critique of comparative psychology [1], in 1969, a lot of comparative data on neuroanatomy and behavior appeared. This hasn't stopped psychologists and media types from championing theories that drank on evolutionary sources that were, in many senses, incorrect. That is why I wrote critiques of the triune brain hypothesis and of evolutionary psychology. Here, I continue the series on Yet Another Critiques (YACs), this time analysing theories of cerebral asymmetry.

 


Cerebral asymmetry is a crucial issue in modern neuroscience, and has acquired quite a status in popular accounts of brain function and behavior. A brain is considered to be asymmetrical (or lateralized) when one of its sides (either a cerebral hemisphere or subcortical regions) is structurally different from the other and/or performs a different set of functions [2]. In humans, language and speech production are functions controlled by the left hemisphere in right-handed individuals, while the right hemisphere seems to control spatial and emotional functions [3]. Data gathered from electroencephalography, functional imaging, behavioral studies, and lesion studies (reviewed in [2]) seemed to indicate a considerable hemispheric specialization in humans; in popular accounts, those differences were greatly amplified, and those data were used to create theories of “cognitive styles” and to explain sex differences in behavior and cognition. Thus, individual differences in behavior were explained as differences in “cognitive styles”, with “right-brained” individuals tending to be more synthetic, while “left-brained” individuals were more analytic. Those popular accounts failed to grasp the subtleties of the data set: in humans, for example, lateralization must be controlled for handedness and gender. Also, the observation that some functions appear to be lateralised does not entail that all functions are lateralised; popular psychology assumed that more holistic functions were differentially controlled by the cerebral hemispheres, while all data gathered concerning cerebral asymmetries so far point to mild differences in punctual functions.


Cerebral asymmetry was once viewed as a “unique” trait of humans. As in most cases of our “unique” traits (cf reference [4]), it was soon discovered that brain lateralization is widespread among both mammals and birds [5]. The first theories of brain lateralization, capitalizing on the presence of this trait in anthropoid primates, associated it with language, tool use, and handedness [5], but cerebral asymmetry seems to be present in species in which those behavioral characters are largely absent, or are not prominent, as well. Thus, other authors suggested that lateralization evolved to prevent conflict of response emission arising from visual input of two laterally placed eyes; this is particularly evident in birds, which lack the large corpus callosum found in mammalian brains that connects the left and right hemispheres [6]. In the avian brain, the main commissural system is found in mesencephalic structures – i.e. the tectal and posterior commissures –, and is thought to suppress lateralization [7].


In most species of birds, eyes are placed laterally, which creates a comparatively small degree of binocular vision in the frontal field. Each eye is able to examine different portions of the visual environment; information from each of the two visual fields, then, is processed primarily separately.


In this condition, the presence of hemispheric specialization may habe the important function of preventing conflicting responses elicited by stimuli perceived simultaneously in two monocular visual fields, each demanding a different response. If one hemisphere is dominant in the control of a certain behaviour, then conflict of response emission would be avoided by having a lateralized brain [...]. Birds, therefore, may have had quite specific reasons to develop brain asymmetry [8].


In contrast, mammals have a well-developed corpus callosum, and perceptual information can be conveyed easily to both hemispheres. Some mammals also present both ipsilateral and contralateral projections from each eye to the brain, while in birds there is complete decussation at the optic chiasma [8]. Even in mammals with frontally placed eyes (carnivores and primates), there are differences in the inputs from one eye to each of the hemispheres (which allowed behavioral research on lateralization in the first place). Being larger, the fibers that cross to the contralateral hemisphere in those mammals relay signals faster than the fibers that go to the ipsilateral hemisphere, being dominant during binocular stimulation [9].


It seems, thus, that even in mammals – with their enlarged corpus callosum and, in some cases, frontally placed eyes – the selective pressures for brain asymmetries appear to be similar to those postulated for birds; that is, cerebral lateralization seems to have appeared to avoid the elicitation of conflicting responses to stimuli that arrive at different regions of the visual field. It seems unlikely, given the phylogenetic relations between birds and mammals, that lateralization arose de novo in both Mamalia and Aves [8]. However, a truly comparative framework for lateralization is needed to understand whether brain asymmetry is homologous or homoplasical in birds and mammals. Keep in mind that outgroup analysis is very useful to judge the historical homology of any given trait (this is described in one of the first posts in this blog); if it can be estimated whether brain lateralization was present in the common reptilian ancestor shared by birds and mammals, then it can be said that this trait is historically homologous in these species. Also, data from the other vertebrate radiations – fishes, reptiles and amphibians – can help us judge the evolutionary history of cerebral asymmetries, which, in turn, can help us make judgments about its conservativeness and adaptive significance.


 

Structural and behavioral asymmetries in fishes, amphibians and reptiles
Bisazza and colleagues [8] reviewed structural and behavioral asymmetries in fishes, amphibians, and reptiles, and concluded that there is variation in population and individual levels in many instances of lateralization in all those clades, which is consistent with the data presented for birds and mammals. For example, the
habenular nuclei, located bilaterally in the anterior dorsal diencephalon (under the epiphysis), is asymmetrical in size in cyclostomes (lampreys and hagfishes), sharks, some teleost fishes, and amphibians [10]. In the frogs Rana esculenta and Rana temporaria, the left habenula consists of two distinct nuclei, whereas the right habenula has a single nucleus [11, 12]. In Rana esculenta, asymmetry in spontaneous and evoked activity in the habenulae was also observed [13], with the density and amplitude of spikes obtained from the left habenula being smaller than the density and amplitude of spikes obtained from the right habenula. This asymettry appears to have appeared quite early in the evolution of vertebrates; the lamprey Petromyzon sp. presents a right habenulo-peduncolar tract [14], and the cyclostome Myxine glutinosa has a right habenula that is bigger than the left one [15].

The bulk of data reviewed by Bisazza and his colleagues [8] is behavioral. In fishes, for example, there is population-wise lateralization in the escape behavior of Girardinus falcatus, Coregonus nasus and Coregonus clupeaformis; in rotational swimming, T-maze choice, courtship and copulatory behavior, and detour behavior of Gambusia holbrooki; stridulation sound production in Ictalurus punctatus; and in eye use in Danio rerio. In toads, “pawedness” (i.e., preference for use of one paw) was observed in the toads Bufo bufo, Bufo marinus and Bufo viridis, while the frog Rana pipiens is lateralised in terms of the neural control of its vocalizations, the frog Hyla regilla is lateralised in its escape responses, and the newt Triturus vulgaris is lateralised in its sexual behavior – all asymmetries observed at population level. There is considerable difference between populations in terms of lateralised aggressive responses in chameleons from the Anolis genus, as well. Evidence for behavioral asymmetry is found in the fossil record, as well. Cambrian trilobites have a higher incidence of scars on the right posterior region of their bodies [16], which could either indicate a bias for left turning while escaping predators in trilobites, or an asymmetry in the direction of attack by their predators [8].


It seems, then, that functional and structural asymmetries are present, at the population level, in all vertebrate radiations – indeed, it is possible that it was also present in Cambrian invertebrates as well. The data so far is not sufficient to fully resolve the question of whether this represents a case of convergent evolution, with laterality appearing in many species independently, or of a conservative trait. However, the amount of species that have behavioral and cerebral asymmetries, and the widespread distribution of this trait, seems to be indicative of homology.



The functional significance of asymmetry

In all cases studied so far, structural and functional asymmetries are widespread among populations, but the trait has not reached fixation in the species – that is, some populations, but not all, within a given species present lateralization of functions. Lateralization was also observed at the individual level in many traits in different species – for example, eye use in the fighting fish Betta splendens, or escape behavior in Jenynsia lineata. However, gross morphological asymmetries (eg, number of rays in the pectoral fins of fishes) do not correlate with behavioral asymmetries at the individual level, which could be indicative of the adaptiveness of behavioral asymmetries.

What, then, should be the adaptive value of lateralization of behavior? In fishes, amphibians, and reptiles, many behavioral traits seem to present a turning bias at the population level – that is, at least 50% of the individuals in a population tend to turn to the same direction in escape behavior, for example. Rogers [17] proposed that the presence of a population bias in lateralization may have some influence on social interactions and group structure: chicks who have been manipulated to remove lateralized input in ovo do not present behavioral asymmetries when adults, and this manipulation affects the coherence and consistency of social structure. Male fiddler crabs (genus Uca) possess an enlarged claw used in courtship and agonistic displays, as well as smaller claw used for object manipulation; there is some evidence that some forms of agonistic interaction are less frequent in heteroclawed than in homoclawed fights in Uca pugilator and Uca pugnax.


It should be remembered that correlation does not imply causation. A third variable could be the cause of both variables in a correlation; if chicks present a “behavioral syndrome” that correlates some behavioral lateralization and group structure at the population level, it is possible that a third variable – probably brain asymmetry – is the cause of this correlation. As such, the correlation per se is a by-product of the morphological adaptation.


Is social interaction the main cause of behavioral lateralization in those vertebrates, then? What of cerebral asymmetries – are they correlated to those behavioral traits? Are they caused by social interaction? There is very little evidence for that. In birds and mammals, for example, it seems that the lateralization of cerebral structures happened because of differential inputs from visual (and possibly other sensory as well) spaces; there is little evidence that those differential inputs correlate – or are indeed caused – by social demands. In fishes, amphibians and reptiles, lateral placement of the eyes and a reduced corpus callosum is the rule rather than the exception; as such, it is much more parsimonious to postulate that cerebral asymmetries and behavioral lateralization were caused by the specific demands imposed by differential conduction velocities of efferents originated in spatially segregated sensory fields.


There is considerable species differences, however, in the behavioral traits which are lateralised; those homoplasies must be explained as well. For example, in some species, social interaction is lateralised – that is, social stimuli presented monocularly to one eye tend to elicit responses more readily and in higher frequency than when presented to another eye. In other species, presentation of noxious stimuli (eg, predator models) to one eye elicit escape responses, while those responses are more rarely elicited when the same stimulus is presented to the other eye. In humans, there is lateralization in the processing of positive vs. negative valence of emotional stimuli [18]. Clearly, social behavior, emotional appraisal and antipredator responses are functionally different domains; the selective pressures that act on one are not the same pressures acting on the other. It is possible, though, that those species-specific asymmetries constitute exaptations of more primitive functions of cerebral lateralization – that is, even though the primary adaptive value of lateralization was the augmented accuracy in the processing of spatially segregated stimuli, the same adaptation was later “co-opted” for other functions.


 


In the blogosphere

Asymmetrical brains help fish (and us) to multi-task, in Not Exactly Rocket Science

Asymetric architecture in the left and right hemispheres, in Developing Intelligence


Cellular "tug-of-war" breaks brain symmetry, in Neurophilosophy 


References


[1] Hodos W, Campbell CBG (1969). Scala Naturae: Why there is no theory in comparative psychology., Psychological Review 76: 337-350.


 


[2] Bradshaw JL (1989). Hemispheric Specialization and Psychological Function. Chichester: John Wiley and Sons.


 


[3] Bradshaw JL, Nettleton NC (1981). The nature of hemispheric specialization in man. Behavioral and Brain Sciences 4: 51-91.


 


[4] Preuss TM (2000). What's human about the human brain? In: Gazzaniga MS (ed.), The New Cognitive Neurosciences, 2nd edition, pp. 1219-1234. Cambridge: MIT Press.


 


[5] Bradshaw JL, Rogers LJ (1993). The Evolution of Lateral Asymmetries, Language, Tool Use, and Intellect. New York: Academic Press.


 


[6] Rogers LJ (1996). Behavioral, structural and neurochemical asymmetries in the avian brain: A model system for studying visual development and processing. Neuroscience and Biobehavioral Reviews 20: 487-503.


 


[7] Parsons CH, Rogers LJ (1993). Role of the tectal and posterior commissures in lateralization of the avian brain. Behavioral Brain Research 54: 153-164.


 


[8] Bisazza A, Rogers LJ, Vallortigara G (1998). The origins of cerebral asymmetry: A review of evidence of behavioural and brain lateralization in fishes, reptiles and amphibians. Neuroscience and Biobehavioral Reviews 22: 411-426.


 


[9] Proudfoot RE (1983). Hemiretinal differences in face recognition: Accuracy versus reaction time. Brain and Cognition 2: 25-31.


 


[10] Walker SF (1980). Lateralization of functions in the vertebrate brain: A review. British Journal of Psychology 71: 329-367.


 


[11] Brainterberg V, Kemali M (1970). Exceptions to bilateral symmetry in the epithalamus of lower vertebrates. Journal of Comparative Neurology 138: 137-146.


 


[12] Morgan MJ, O'Donell JM, Oliver RF (1973). Development of left-right asymmetry in the habenular nuclei of Rana temporaria. Journal of Comparative Neurology 149: 203-214.


 


[13] Vota-Pinardi U, Kemali M (1990). Neuroelectrophysiology of the morphologically asymmetric habenulae of the frog. Comparative Biochemistry and Physiology A 96: 421-424.


 


[14] Jansen J (1930) The brain of Mixine glutinosa. Journal of Comparative Neurology 49: 359-507.


 


[15] Frontera JG (1952). A study of the anuran diencephalon. Journal of Comparative Neurology 96: 1-69.


 


[16] Babcock LE, Robinson RA (1989). Preferences of Paleozoic predators. Nature 337: 695-696.


 


[17] Rogers LJ (1989). Laterality in animals. International Journal of Comparative Psychology 3: 5-25.


 


[18] Cacioppo JT, Berntson GG, Larsen JT, Pehlmann KM, Ito TA (2000). The psychophysiology of emotion. In: Lewis M, Haviland-Jones JM (eds.), Handbook of Emotions, 2nd edition, pp. 173-191. New York: Guilford Press.

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