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PSYCHOLOGY 



REVIEW ARTICLE 

published: 30 July 2014 
doi: 10. 3389/fpsyg. 2014. 00820 




The cortical microstructural basis of lateralized cognition: 
a review 

Steven A. Chance* 

Neuropathology, Nuffield Department of Clinical Neurosciences, Neuroanatomy and Cognition Group, University of Oxford, Oxford, UK 



Edited by: 

Christian Beste, Ruhr Universitat 
Bochum, Germany 

Reviewed by: 

Andrej A. Kibrik, Moscow State 
University, Russia 
Danieie Ortu, University of North 
Texas, USA 

*Correspondence: 

Steven A. Chance, Neuropathology, 
Nuffield Department of Clinical 
Neurosciences, Neuroanatomy and 
Cognition Group, University of Oxford, 
Level 1, West Wing, John Radcliffe 
Hospital, Oxford 0X3 9DU, UK 
e-mail: Steven. chance&ndcn. ox. ac. uk 



The presence of asymmetry in the human cerebral hemispheres is detectable at both the 
macroscopic and microscopic scales. The horizontal expansion of cortical surface during 
development (within individual brains), and across evolutionary time (between species), is 
largely due to the proliferation and spacing of the microscopic vertical columns of cells that 
form the cortex. In the asymmetric planum temporale (PT), minicolumn width asymmetry 
is associated with surface area asymmetry. Although the human minicolumn asymmetry 
is not large, it is estimated to account for a surface area asymmetry of approximately 9% 
of the region's size. Critically, this asymmetry of minicolumns is absent in the equivalent 
areas of the brains of other apes. The left-hemisphere dominance for processing speech 
is thought to depend, partly, on a bias for higher resolution processing across widely 
spaced minicolumns with less overlapping dendritic fields, whereas dense minicolumn 
spacing in the right hemisphere is associated with more overlapping, lower resolution, 
holistic processing. This concept refines the simple notion that a larger brain area is 
associated with dominance for a function and offers an alternative explanation associated 
with "processing type." This account is mechanistic in the sense that it offers a mechanism 
whereby asymmetrical components of structure are related to specific functional biases 
yielding testable predictions, rather than the generalization that "bigger is better" for any 
given function. Face processing provides a test case - it is the opposite of language, 
being dominant in the right hemisphere. Consistent with the bias for holistic, configural 
processing of faces, the minicolumns in the right-hemisphere fusiform gyrus are thinner 
than in the left hemisphere, which is associated with featural processing. Again, this 
asymmetry is not found in chimpanzees. The difference between hemispheres may also be 
seen in terms of processing speed, facilitated by asymmetric myelination of white matter 
tracts (Anderson etal., 1999 found that axons of the left posterior superior temporal lobe 
were more thickly myelinated). By cross-referencing the differences between the active 
fields of the two hemispheres, via tracts such as the corpus callosum, the relationship 
of local features to global features may be encoded. The emergent hierarchy of features 
within features is a recursive structure that may functionally contribute to generativity - 
the ability to perceive and express layers of structure and their relations to each other. 
The inference is that recursive generativity, an essential component of language, reflects 
an interaction between processing biases that may be traceable in the microstructure of 
the cerebral cortex. Minicolumn organization in the PT and the prefrontal cortex has been 
found to correlate with cognitive scores in humans. Altered minicolumn organization is also 
observed in neuropsychiatric disorders including autism and schizophrenia. Indeed, altered 
interhemispheric connections correlated with minicolumn asymmetry in schizophrenia 
may relate to language-processing anomalies that occur in the disorder. Schizophrenia 
is associated with over-interpretation of word meaning at the semantic level and over- 
interpretation of relevance at the level of pragmatic competence, whereas autism is 
associated with overly literal interpretation of word meaning and under-interpretation of 
social relevance at the pragmatic level. Both appear to emerge from a disruption of the 
ability to interpret layers of meaning and their relations to each other. This may be a 
consequence of disequilibrium in the processing of local and global features related to 
disorganization of minicolumnar units of processing. 



Keywords: minicolumn, cytoarciiitecture, lateralization, asymmetry, face-processing, language, schizophrenia, 
autism 



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The significance of human brain asymmetry depends broadly on 
two Unes of evidence: the presence of anatomical asymmetries at 
the large and small scale and the presence of functional lateral- 
ization of cognitive functions, most notably language. A major 
challenge is that the nature of the link between the two is not clear. 
For example, the simplest models tend to be based on the principle 
that a larger brain region on one side of the brain denotes domi- 
nance for a lateralized function (Galaburda, 1995). However, there 
are frequently exceptions to this rule. Asymmetries vary by degree 
between individuals. Furthermore, the correspondences between 
structures within the same individual and between structural 
asymmetry and functional lateralization are often inconsistent. 

AUDITORY CORTEX, LANGUAGE, AND ASYMMETRY 

In humans, the superior temporal gyrus (STG) contains perhaps 
the most prominently asymmetrical brain area: the auditory asso- 
ciation cortex of the planum temporale (PT), lying posterior and 
lateral to Heschl's gyrus, contributing to the hemispheric asym- 
metry of the posterior Sylvian fissure. This region plays a key role 
in phonological processing and forms part of the receptive lan- 
guage region often identified as Wernicke's area. Geschwind and 
Levitsky (1968) found leftward asymmetry (greater size on the left 
than the right) of the PT in two-thirds of individuals. Around 
the same time in the late 1960s, Juhn Wada's test of alternately 
anesthetizing the cerebral hemispheres had also demonstrated the 
widespread left-hemisphere dominance for language processing. 
The implied association between leftward structural asymme- 
try and functional lateralization led some authors to suggest 
that cerebral asymmetry is a defining feature of the human 
brain (Corballis, 1991; Crow, 2000). In fact, there is uncer- 
tainty concerning the relationships between different measures 
of asymmetry and corresponding language lateralization. Indi- 
viduals with situs inversus (reversal of the bodily organs) who 
have reversed frontal petalia (asymmetric extension of the ante- 
rior Hmit of the fi-ontal lobe) stiU show normal asymmetry of the 
PT (Kennedy et al, 1999). This suggests dissociation between ele- 
ments of asymmetric structure. Other researchers have found that, 
although PT asymmetry and language laterality are significantly 
left-hemisphere biased, they may not be correlated (Eckert etal., 
2006). 

A more complex picture has emerged from psychological and 
neuroimaging studies which have clarified more precise associa- 
tions between structure and function. The PT may be subdivided 
into medial, lateral, and caudal parts, each associated with differ- 
ent aspects of speech processing (Tremblay etal., 2013). Anterior 
STG is sensitive to syntactic word category violation in a sentence 
(Friederici etal., 1993), while the posterior STG supports a left- 
hemisphere bias for phonological processing (e.g., Robson etal., 
2012). Meanwhile, the right-hemisphere auditory areas are domi- 
nant for music perception in untrained listeners (Ono et al, 20 1 1 ), 
although this functional asymmetry is modulated by degrees of 
expertise and ability. Therefore, the evidence for two aspects 
of lateralization, structural and functional, has become increas- 
ingly refined, suggesting that lateralized functions (e.g., language) 
often depend on multiple cognitive components (e.g., phonology, 
prosodic intonation etc. ) that may be modular in nature and struc- 
tural asymmetry (e.g.. Sylvian fissure length) depends on smaller 



structural components (e.g., anterior, posterior STG, sub-regions 
of PT). The relationship between structure and function appears 
to depend on the lateralization of these localized components. 

The search for the link between structure and function leads 
therefore to the small-scale modular components that constitute 
the functions of interest. Indeed, inconsistent matching between 
measures of asymmetry and lateralization may be due to attempts 
to match incompatible levels (e.g., attempting to match a small 
structural subregion asymmetry with the lateralization of a func- 
tion that emerges from the interaction of multiple regions). In 
terms of function, two underlying processing biases are apparent 
at a basic level that may contribute to language laterality. First, 
the left hemisphere is biased toward processing short temporal 
transitions in the sound signal which is especially suitable for rec- 
ognizing speech (Efron, 1963; Tallal etal., 1993; Shtyrov etal., 
2000; Zatorre etal., 2002). Conversely, the right hemisphere is 
biased for spectral sound processing (Zatorre and Belin, 2001) 
which may form the basis of the dominance of music perception 
in the right hemisphere in untrained listeners. Second, evidence 
supports the concept that in the generation of "meaning" the left 
parieto-occipito-temporal junction (Wernicke's area) is associated 
with the activation of more discrete, narrow, semantic associations, 
whereas the right hemisphere activates more distributed seman- 
tic fields appropriate to its greater sensitivity to context (Rodel 
etal., 1992). Event-related potentials (ERPs) in the STG are the 
first to diverge depending on the semantic categories of words 
(Dehaene, 1995) consistent with a role for this region early in 
category discrimination (although see Eckert etal., 2006 for con- 
sideration of an alternative - that this is a response to phonology 
secondary to meaning). Such ERPs are asymmetrical between the 
hemispheres, for example, a left temporo-parietal negativity for 
animal names and verbs and a left inferior temporal negativity for 
proper names. 

What level of structural focus is appropriate to identify corre- 
sponding anatomical components underlying regional asymme- 
try? Not aU measures of the superior temporal plane identify 
hemispheric asymmetries. Since the original observations by 
Geschwind and Levitsky (1968), Zetzsche etal. (2001) have shown 
that the definition of PT borders influences the detection of cere- 
bral asymmetry. Pearlson et al. ( 1 997) suggested that measurement 
of surface area is more important than volume and Barta etal. 
(1997) detected asymmetries by surface area measurements that 
were not detected by volume measures. Both are consistent with 
the hypothesis of Harasty et al. (2003) that asymmetry of the PT 
is due to lengthening of the cortex on the left side relative to the 
right. These measures at the surface may therefore indirectly reveal 
differences in the underlying neural circuitry that is the basis for 
differences in processing bias between the hemispheres. 

The horizontal expansion of cortical surface during develop- 
ment (within individual brains), and across evolutionary time 
(between species), is largely due to the proliferation and spacing 
of radial minicolumns of cells that form the cortex (Rakic, 1995). 
These microscopic structures persist throughout the mature brain, 
where they span the 3-4 mm depth of the cortex with a hor- 
izontal width of approximately 50 |xm. Minicolumns emerge 
by radial migration of cells toward the brain's surface during 
embryonic formation of the cerebral cortex. Column-like radial 



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organization is found for cell bodies and their axonal and den- 
dritic connections. Auditory cortex in the STG develops a clear 
columnar cell distribution by the third trimester of fetal life, 
which is established in early childhood, although axonal matu- 
ration continues up to at least 12 years of age (Moore and Guan, 
2001) and probably later in more associative regions. Although 
the human minicolumn asymmetry is not large (Buxhoeveden 
etal., 2001; Hutsler, 2003), it is estimated to account for a sur- 
face area asymmetry of 8-9% of the region's size (Chance et al., 
2006). Notably, this asymmetry of minicolumn spacing is absent 
in the equivalent areas of the brains of other apes (Buxhoeve- 
den etal., 2001). The microscopic asymmetry in humans is also 
detected at the slightly larger scale of inter-connected "macrocol- 
umn" patches (approximately 500 |xm diameter) which are more 
widely spaced in the left than in the right auditory association cor- 
tex (Galuske etal., 2000). Recent single-unit electrophysiological 
recordings have demonstrated that cells within the same mini- 
column share greater similarity of stimulus sensitivity than with 
cells in neighboring columns (Opris etal., 2012). The combina- 
tion of stimulus-sensitive columns in a region presumably confers 
processing speciaUzation. 

Minicolumn organization in the PT has been found to corre- 
late with cognitive scores (tests such as the Mini Mental State Exam 
which covers a range of tasks including object naming and sim- 
ple sentence construction; Chance et al., 201 lb). The relationship 
with cognition was specific to minicolumn measures and was not 
found for neuron density, as also reported in monkeys (Cruz et al., 
2009). It has been suggested that greater spacing of minicolumns 
in human association cortex results in less-overlapping dendritic 
trees and allows more independent minicolumn function (Sel- 
don, 1981a,b). This is consistent with the association between 
the greater surface area and the wider spacing of evoked elec- 
trophysiological activity peaks in the superior temporal plane of 
the left hemisphere compared with the right (Yvert etal, 2001). 
Harasty et al. (2003) have developed the notion that widely spaced 
minicolumns function as discrete units facilitating computational 
processing of more independent components, whereas densely 
spaced minicolumns permit greater overlapping co-activation 
and therefore confer more holistic processing. In lung-Beeman's 
(2005) model, the basal dendrites of right-hemisphere pyramidal 
neurons have longer initial branches and more synapses further 
from the soma than left-hemisphere neurons where the more 
widely spaced minicolumns have more dendritic branching within 
their territory. Wider minicolumn spacing is therefore associ- 
ated with higher resolution processing across less-overlapping 
basal dendritic fields whereas dense minicolumn spacing is asso- 
ciated with lower resolution, holistic processing due to relatively 
greater distal sampling of more overlapping fields (Jung-Beeman, 
2005). 

EVOLUTIONARY COMPARISON OF AUDITORY AND 
FACE-PROCESSING ASYMMETRIES 

It has been suggested by some (Annett, 1985; McManus, 1985) 
that hemispheric asymmetries are human specific and offer a neu- 
ral correlate of uniquely lateralized function, including language, 
in humans. A challenge to this thesis is found in compara- 
tive neuroanatomical studies that have reported the presence of 



asymmetries in other primate species (LeMay and Geschwind, 
1975; HoUoway and De La Coste-Lareymondie, 1982; Gan- 
non etal., 1998). However, in contrast with the macroscopic 
picture based on surface landmarks, current evidence indi- 
cates evolutionary discontinuity for microscopic, cytoarchitectural 
asymmetry. Region size estimates based on cytoarchitecturaUy 
defined boundaries have found that asymmetries are weaker in 
chimpanzees compared to humans (Spocter etal., 2010), indi- 
cating that species differences in asymmetry are more readily 
identified when cytoarchitectural features are used. Hemispheric 
asymmetries at the neuronal level show yet more consistent differ- 
ences between humans and other primates (Chance and Crow, 
2007). Asymmetry in the spacing of minicolumnar units of 
neurons in the human PT is absent in the brains of other pri- 
mates (Buxhoeveden etal., 2001), and there is a preponderance 
of large layer III pyramidal neurons (Hutsler, 2003) with wider 
dendritic arbors (Seldon, 1981a,b) filling the space in the left 
hemisphere compared with the right in humans. Both Broca's 
area and Wernicke's area in humans have hemispheric asym- 
metries of neuropil (Amunts etal, 1999; Anderson etal., 1999). 
Chimpanzees lack neuropil asymmetry in the equivalent areas 
(Sherwood et al., 2007). Neuron density in the posterior STG (area 
Tpt) in chimpanzees is not asymmetrical (Schenker etal., 2005). 
It is worth acknowledging, however, that symmetry of cytoar- 
chitectural organization may not always be detected - Spocter 
etal. (2012) did not detect a significant asymmetry of neu- 
ropil fraction in the PT or Heschl's gyrus in chimpanzees or 
humans. 

Face processing is another highly evolved ability in primates 
that provides an interesting comparison in two respects - it is 
asymmetrically dominant in the opposite direction to language, 
i.e., face processing is dominant in the right hemisphere in humans 
(Kanwisher etal, 1997), and it is also a function successfully per- 
formed by our closest primate relative, the chimpanzee (Parr et al., 

2009) . Although both species perceive faces in a predominantly 
holistic manner (see Taubert and Parr, 2010), this process is clearly 
lateralized in humans in whom holistic analysis is biased to the 
right hemisphere (while individual facial features are detected in 
the left hemisphere; Rossion et al., 2000). The face processing area 
in the ventral temporal cortex is part of the brain network support- 
ing social cognition in humans and other primates and is found 
in the mid-fusiform region (roughly equivalent to Brodmann area 
37 in human brain). This area falls within a larger surrounding 
region that processes visual objects in general. This local special- 
ization and the high heritability of face processing (Zhu etal., 

2010) make it plausible that there is a detectable neuroanatomical 
correlate in this region, although the extent to which the neural 
structure depends on genetic contribution or early social learning 
is unresolved. 

In humans, cells have become large and less densely packed 
in the evolution of mid-fusiform cortex compared to the chim- 
panzee and this is accentuated in the left hemisphere with the 
result that there is an inter-hemispheric asymmetry that is not 
found in chimpanzees (Chance etal., 2013). Consequently, in 
humans, the wider minicolumns and larger neurons are found 
in the hemisphere opposite to the one that is dominant for face 
perception. Therefore, unlike auditory language processing, it 



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appears that the arrangement of minicolumns that confers dom- 
inance for face processing is the thinner, denser spacing that is 
found in the right hemisphere (Chance etal., 2013). Meanwhile, 
the absence of asymmetry in chimpanzees may relate to better per- 
formance than humans in tasks such as inverted face recognition 
that have ecological validity for chimpanzees (Matsuzawa, 2007). 
The human asymmetry is relatively confined to the mid-posterior 
fusiform region, as a previous study that included the more ante- 
rior fusiform (area 20) reported that minicolumn width in human 
subjects did not show a statistically significant asymmetry (Di Rosa 
etal, 2009). A further indication that this functional specializa- 
tion is associated with minicolumn structure - face discrimination 
ability is reduced in old age (an effect described as "dedifferenti- 
ation"; Goh etal., 2010) and marked minicolumn alteration is 
also found in fusiform cortex in old age (Di Rosa et al., 2009). As 
with auditory language processing, there is also left-hemisphere 
dominance for written language and disordered reading is asso- 
ciated with damage to the left temporo-parietal area (the angular 
gyrus), first noted by the 19* -century neurologist Dejerine. How- 
ever, inability to read ("pure alexia") is associated with damage 
to the left mid-fusiform gyrus (Leff etal, 2006). It has been sug- 
gested that the wider minicolumn spacing in this region of the 
left hemisphere may relate to its role in visual word recognition 
in humans in addition to its role in face processing (Chance etal., 
2013). 

MECHANISTIC MODELS 

If the point of convergence between functional and anatomi- 
cal lines of evidence implicates these small, modular units, a 
mechanistic model is desirable to explain this across different 
domains of processing. In the visual domain, it is possible that 
wider minicolumn spacing may be associated with detailed fea- 
ture processing, whereas thin minicolumns may facilitate holistic, 
configural processing of the type usually associated with face pro- 
cessing. In such a scheme, face processing is similar to music 
processing. Holistic, configural processing for face recognition 
(or music) benefits from the computational overlap generated by 
densely spaced minicolumns in the fusiform gyrus. This mecha- 
nistic interpretation is consistent with a correspondence between 
the rightward lateralization of holistic face processing and the 
thin minicolumns found in the right hemisphere in humans 
and replicates the structure-function correspondence found in 
the auditory domain although the processing demands of the 
function lead to different hemispheric dominance. This suggests 
that minicolumn width is dissociated from "dominance," per se, 
and instead relates to the type of processing: featural or holis- 
tic. The wider minicolumn spacing in the left STG facilitates 
fine temporal discrimination because minicolumns function as 
more discrete computational elements, whereas dense minicol- 
umn spacing in the right STG supports broad spectral processing, 
due to the minicolumns' greater computational overlap. The hemi- 
spheric processing bias for a given task is likely to depend on the 
degree to which task success emphasizes local or global process- 
ing and the hemispheric asymmetry of minicolumnar units in the 
brain region associated with that functional domain. This concept 
refines the simple notion that a larger brain area is associated with 
dominance for a function and offers an alternative, mechanistic 



explanation associated with "processing type" (Van Veluw et al., 
2012). 

The processing-type hypothesis has the advantage of acknowl- 
edging the active role of the "non-dominant" hemisphere. It is 
recognized increasingly that many tasks combine elements of both 
holistic and featural processing (Rossion etal, 2000). Thus, two 
streams of processing occur in parallel - global processing in 
broad-activation fields of the right hemisphere and local process- 
ing in focused fields of the left hemisphere. In isolation, these 
streams simply encode two separate levels of detail, but by cross- 
referencing the differences between the active fields of the two 
hemispheres via the corpus caUosum the relationship of local fea- 
tures to global features may be encoded. The emergent hierarchy 
of features within features is a recursive structure that may func- 
tionally contribute to generativity - the ability to perceive and 
express layers of structure and their relations to each other. It has 
been argued that recursive generativity is an essential, or even, 
the key component of human language behavior (Crow, 2005). 
The description here is consistent with such a scenario although 
it cannot be concluded that the presence of recursion necessar- 
ily entails this form of structural asymmetry. Cytoarchitectural 
asymmetries have been found in normal auditory cortex that cor- 
relate with the number of axons passing through the connecting 
regions of the corpus callosum (Chance etal., 2006). A greater 
number of minicolumnar units in the hemispheric region that is 
typically functionally dominant was associated with more inter- 
hemispheric connections through the area of the corpus callosum 
connected to that region. 

This mechanistic, processing-type hypothesis potentially con- 
tributes to a coherent, descriptive account of cerebral asymmetries 
of structure and function. However, it is also necessary to identify 
an evolutionary advantage conferred by this organization, partic- 
ularly if it is different in humans from other apes. Although not 
originally associated with asymmetry, Gabora (2002) has proposed 
a model of the evolutionary enhancement of cognitive process- 
ing capacity in humans through the cross-referencing of different 
levels of conceptual organization. Similar to the recursive pro- 
cess described above, Gabora (2002) describes the interpolation 
between concepts at "varying levels of abstraction (i.e., cup, con- 
tainer, thing)" as providing stepping stones in a recursive process 
of "variable focus," She speculates that a pre-palaeolithic mind 
"activated regions of conceptual space of fixed size with lim- 
ited ability to focus," but the capacity for variable focus evolved 
enabling alternately widening and narrowing the "activation func- 
tion." Although Gabora (2002) describes this as a process of focus 
fluctuating over time, at least part of this requirement may be 
met concurrently by the asymmetry between hemispheres as they 
process different levels of abstraction. Furthermore, although 
Gabora's (2002) "activation function" was not clearly defined, it 
seems reasonable to interpret it not just in the abstract but as a field 
of activated units such as the overlapping minicolumns described 
above. 

PSYCHOLOGICAL SPACE AND LATERALIZED PROCESSING 

The Gabora's (2002) model suggests an evolutionary benefit that 
may be provided by different levels of processing, compatible with 
existing lateralized processing biases. The proposed advantage of 



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variable focus is to expand the capacity of conceptual space by 
interpolation between concepts. In statistical terms, it is equiva- 
lent to the generation of continuous data rather than categorical 
data. In psychological terms, it may be described as the con- 
trast between dimensional and categorical processing. Therefore, 
if the mechanistic interpretation of microstructural asymmetries 
is related to this interpolation between concepts and therefore to 
the generation of continuous dimensions that define a continu- 
ous conceptual space, one would expect some association with 
the organization of the dimensions of conceptual space in the two 
cerebral hemispheres. 

It is often challenging to obtain data for the separate hemi- 
spheres, however, in the language domain some investigations 
have provided data on the organization of semantic space in each 
hemisphere. Taylor etal. (1999) found that the right hemisphere 
uses more dimensions than the left hemisphere to represent the 
semantic map in typical subjects. It is unclear if more dimensions 
constitutes less efficient coding (i.e., in the right hemisphere each 
dimension may contribute less to the representation of different 
concepts, whereas in the left hemisphere the dimensions are more 
discriminatory and so fewer are needed) or more complex rep- 
resentation (i.e., the right hemisphere may take account of more 
aspects of a given concept). However, more diffuse activation of 
the network in response to a linguistic stimulus, consistent with 
the model of holistic, overlapping activation described above, has 
been proposed to explain the lesser discrimination between pri- 
mary and secondary word meanings that is also typically found in 
the right hemisphere (Weisbrod et al, 1998). This lower resolution 
discriminative capacity in the right hemisphere is found for face 
processing even as the right hemisphere is also dominant for mak- 
ing categorical (face vs non-face) distinctions (Meng et al., 2012). 
This is consistent with the notion that the holistic processing of 
the densely spaced minicolumns in the right hemisphere facilitates 
broad categorical processing, whereas the left hemisphere differ- 
entiates components within dimensional psychological space. The 
combination of an increased number of dimensions and more 
diffuse activation in the right-hemisphere network suggests that 
the dimensions are partly correlated and less separable than truly 
orthogonal dimensions. 

The phenomenon of key dimensions along which concepts can 
be organized provides a structure for mentally sorting concepts. 
This is desirable so that semantic information may be efficiently 
processed at different levels of elaboration (Craik and Lockhart, 
1972). Similar to Gabora's (2002) variable focus, a benefit may 
be conferred by complementary forms of elaboration with one 
hemisphere emphasizing the clear separation of concepts and the 
other allowing more overlap. Different metrics underlying the 
conceptual space are possible (Gardenfors, 2000), which suggest 
differences in conceptual organization corresponding to hemi- 
sphere differences. Just as with the revolution in understanding 
of the physical universe in the early 20th century, which indicated 
that physical space is curved, there have been suggestions that the 
underlying structure of conceptual space is also not what we may 
first assume. For example, various psychological spaces are better 
represented by the "city-block" metric (Arable, 1991) rather than 
the familiar Euclidean metric that has been typically assumed (e.g., 
in multi-dimensional scaling analysis such as Paulsen et al., 1996). 



The metric is so-called because the distance between concepts is 
measured as if restricted to a grid-like system of roads (hence "city- 
block" or "Manhattan" metric) rather than "as the crow flies" in 
Euclidean space. In the city-block metric, points equidistant from 
a central point lie on a square around it rather than a Euclidean 
circle. It has been argued that the sharp-cornered form of the non- 
Euclidean city-block metric better models the natural tendency to 
perceive discontinuities between concepts with the corners of a 
square creating a discontinuity between the concepts on either 
side of them (Arable, 1991; Gardenfors, 2000). The orthogonal 
edges of the square mimic the way conceptual dimensions (such 
as "size" and "domesticity") are not arbitrary and interchangeable. 
The difference between hemispheres in the separation and corre- 
lation between dimensions suggests a hemispheric difference in 
the metric of the conceptual space. 

The separation of conceptual dimensions also changes during 
development. Normally, a developmental shift occurs: whereas 
older children and adults perceive dimensions such as high and 
tall, or big and bright, to be separable, young children tend to 
confuse these concepts (Carey, 1978). Goldstone and Barsalou 
( 1998) have described the development of reasoning about dimen- 
sions: "dimensions that are easily separated by adults, such as the 
brightness and size of a square, are treated as fused together for 
children. . . [they] have difficulty identifying whether two objects 
differ on their brightness or size even though they can easily see 
that they differ in some way. Both differentiation and dimen- 
sionalization occur throughout one's lifetime." This has been 
described as a developmental shift from a more Euclidean cog- 
nitive metric to the more separable dimensions of the city-block 
metric (Gardenfors, 2000). The development of more orthogonal 
dimensions therefore is associated with more sophisticated cogni- 
tive discriminative ability. Aspects of brain structural maturation 
and plasticity presumably relate to this process of cognitive matu- 
ration. The increase in discrimination associated with orthogonal 
dimensions is similar to the acquisition of expertise, which is often 
associated with left-hemisphere specialization for fine-grained dif- 
ference judgements, e.g., for faces, word meaning and music. The 
process, extended over childhood, is also likely to be influenced by 
the social and cultural environment, including the requirements 
of social integration and communicative pressure for shared con- 
ceptual frameworks. Appropriately, it is the same hemisphere (the 
left) that is associated with the acquisition of expert discrimina- 
tion and dominance for the communicative faculty of language 
that reinforces it. 

SCHIZOPHRENIA AND AUTISM 

Testing the mechanistic role of cytoarchitectural asymmetry on 
these aspects of cognitive function is challenging as the later- 
alized functions of interest appear to be confined to humans 
and, debatably, few other animals. However, disruptions of both 
minicolumnar structural organization and lateralized function are 
found in human neuropsychiatric disorders which provide further 
insight. 

Altered cerebral asymmetry has been found in schizophrenia 
(Bilder etal., 1994; DeLisi etal, 1997; Chance etal., 2005) and the 
prominent role of language anomalies in schizophrenia also impli- 
cates lateralization (Crow, 1990). The auditory region offers one 



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of the dearest associations between psychotic symptoms and brain 
structure, as it is activated during auditory hallucinations (Shergill 
etal, 2000; Ropohl etal, 2004). The loss of left-hemisphere ERP 
mismatch responses to anomalous words at the end of a sentence, 
based on incongruous word meaning (Spironelli et al., 2008), pro- 
vides a link between the sensory, phonological abnormalities and 
linguistic meaning. Reduced gray matter in this area, including the 
PT, is one of the most replicated structural changes in the disor- 
der. Minicolumn asymmetry of this region is also altered in male 
patients (in whom iUness is usually more severe) in such a way 
that both hemispheres are configured more like the typical right 
hemisphere (Chance etal., 2008). 

Word generation (semantic fluency) tests the integrity of the 
semantic network that encodes basic knowledge about the mean- 
ings of words. Patients with schizophrenia have been shown to 
have networks that are less organized than those of control sub- 
jects (Paulsen etal., 1996; Rossell et al, 1999). If increased number 
of dimensions is taken to be indicative of more diffuse activation 
in the right-hemisphere network in normal subjects (as described 
above; Taylor etal., 1999), then the hypothesis that patients have 
unusually diffuse semantic associations in the left hemisphere 
as well as the right hemisphere (Weisbrod etal, 1998) predicts 
that patients use more, poorly discriminative dimensions overaD. 
This is supported by several studies which reported less effective 
mapping of semantic space in low dimensions for schizophrenia, 
indicating the requirement for more dimensions (Paulsen etal., 
1996; Rossell etal., 1999). The evidence that semantic category 
boundaries are less clear in schizophrenia (Paulsen etal, 1996) 
raises the prospect that the city-block metric may not provide a 
better fit for patients. In adolescent onset schizophrenia it has been 
found that the city-block metric provided a less beneficial data fit 
than in controls (Chance etal., 2011a). Therefore, alterations in 
the dimensions of conceptual space, consistent with disruption 
of lateralized cognitive processing biases, accompany abnormal 
anatomical structure of the cortex, including altered asymmetrical 
cytoarchitecture in schizophrenia. 

The developmental shift from the Euclidean cognitive metric to 
the more separable dimensions of the city-block metric proposed 
by Gardenfors (2000) may be relevant in the neurodevelopmental 
context of schizophrenia. Although there is a clear genetic com- 
ponent in the etiology of schizophrenia, onset of illness is not 
identified untU adolescence or early adulthood. It has been pro- 
posed that, structurally, this may be linked to the time course of 
myelination (Crow etal, 2007; Chance etal., 2008). Functionally, 
it may be linked to the shift in cognitive metric and as dimen- 
sionalization matures the anomalies associated with psychosis are 
exposed, leading to the recognition of "onset" and diagnosis. 

Schizophrenia patients sometimes have difficulty in recogniz- 
ing their own face (Kircher etal., 2003) and minicolumns have 
also been shown to be altered in the fusiform gyrus in patients (Di 
Rosa etal., 2009). In another neuropsychiatric condition, people 
with autism have a selective deficit in perceiving facial expressions 
categorically (Teunisse and de Gelder, 2001) which affects acti- 
vation of the fusiform gyrus (Pierce etal, 2004). One of the few 
neuropathological features of the disorder is altered minicolumn 
organization (Casanova et al, 2006) accompanied by altered neu- 
ron density in layer III of the fusiform gyrus (Van Kooten et al.. 



2008). Although it is not, so far, apparent that the effect in autism 
is asymmetrical between the hemispheres, it is clear that these 
alterations present a risk of disruption to the very structures that 
support lateralized face processing and are consistent with atypical 
processing in that functional domain. Indeed, attempts to char- 
acterize the deficits in ASD at a broader level led to the "weak 
central coherence" hypothesis (Frith, 1989) which proposes that 
the core difference in ASD involves poor integration of "featural" 
information into a coherent whole. 

In terms of language and theory of mind, autism is associ- 
ated with excessively literal interpretation of word meaning and 
under-interpretation of social relevance at the pragmatic level. 
Both appear to emerge from a disruption of the ability to inter- 
pret layers of meaning and their relations to each other. Altered 
processing of semantic categories has been implicated in autism 
(Gastgeb et al., 2006; although further studies have suggested that 
the effects are often subtle). More broadly, in visual categoriza- 
tion tasks, deficits in prototype formation have been indicated 
(Gastgeb etal., 2012) and altered influence of categorical knowl- 
edge in autism has been interpreted as a reduction of top-down 
influence on perceptual discrimination (Soulieres etal., 2007). In 
the context of altered minicolumn structure, these effects are con- 
sistent with the mechanistic model of minicolumn asymmetry 
influencing different levels of processing that are lateralized for 
some functions. 

In contrast to autism, schizophrenia is associated with over- 
interpretation of word meaning at the semantic level and over- 
interpretation of relevance at the level of pragmatic competence. 
Altered interhemispheric connections have been found to be cor- 
related with minicolumn asymmetry in auditory language cortex 
in schizophrenia suggesting a link to language-processing anoma- 
lies that occur in the disorder (Chance etal., 2008; Simper etal, 
2011). Therefore, both disorders may involve a contribution from 
disequilibrium in the processing of local and global features related 
to the disorganization of minicolumnar units of processing. 

ACKNOWLEDGMENTS 

Dr. Steven A. Chance was supported by a project grant (#6026) 
from Autism Speaks, USA, and is supported by a grant from the 
Shirley Foundation, UK. 

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Conflict of Interest Statement: The author declares that the research was conducted 
in the absence of any commercial or financial relationships that could be construed 
as a potential conflict of interest. 

Received: 24 January 2014; accepted: 10 July 2014; published online: 30 July 2014. 
Citation: Chance SA (2014) The cortical microstructural basis oflateralized cognition: 
a review. Front. Psychol 5:820. doi: 10.3389/Jpsyg.2014.00820 
This article was submitted to Cognition, a section of the journal Frontiers in Psychology. 
Copyright © 2014 Chance. This is an open-access article distributed under the terms 
of the Creative Commons Attribution License (CC BY). The use, distribution or repro- 
duction in other forums is permitted, provided the original author(s) or licensor are 
credited and that the original publication in this journal is cited, in accordance with 
accepted academic practice. No use, distribution or reproduction is permitted which 
does not comply with these terms. 



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