Complementarity or independence of hemispheric specializations? A brief review.

The current review investigates the question of the relationship of different hemispheric specializations. Hemispheric specializations are the result of the seemingly distinctive ability of the left and right hemisphere to specialize in different cognitive functions. The review focuses on the concept of complementarity whereby the lateralization of one function predicts the asymmetric processing of another one. The complementarity of hemispheric specializations presents an interesting dilemma as the literature evidence is outwardly mixed. The causal and statistical hypotheses attempt to account for the observed findings, with support for both hypotheses. However, most of the evidence appears to align with the statistical pattern of complementarity. Converging lines of evidence suggest that there are multiple independent biases that play a role in how these functional cerebral asymmetries are organized in the human brain. Some of the functional and evolutionary implications of the existence of complementarity of hemispheric specializations are also briefly discussed.

Lateralized regular spatial patterns in oscillating drawing arm movements of right-handed young women.

There is a lacuna in literature with reference to the spatial lateral difference in fast rhythmical movements produced by the whole dominant and nondominant whole arm, where spinal regulation has a significant role. Based on a fast oscillating zigzag drawing task, this study focused on (a) creation of a specific model of the task based on the intermittencies of coupled vectors of the fast motion, (b) identification of the spatial patterns that triggered these vectors, and (c) identification of quantified lateral differences between the spatial rhythmical patterns. 12 strongly right-handed young women performed 9 to 11 trials drawing zigzag lines. Each participant was required to extend her arm and perform this task using the left and right arm selectively on a frontally positioned graphic design system. The spatial patterns produced on each trial were identified in terms of five constant combinations of horizontal (X) and vertical (Y) projections of each line on the zigzag drawings. The dominant arm differed from the nondominant arm in preferred patterns. Because the duration of each line in the zigzag was highly restricted in time, the appearance of the patterns with different block schemes of movement could be explained as being associated with lower levels of the central nervous system. Initiation of fast movement of the total upper arm is probably associated with selection of the block scheme of motor control appropriate to each arm. Each block scheme is grounded on the coupled vectors of motion organised with particular muscle groups. Some block schemes seemed linked specifically to the dominant arm.

Non-identical neural mechanisms for two types of mental transformation: event-related potentials during mental rotation and mental paper folding.

Reaction times, accuracy and 128-channel event-related potentials (ERPs) were measured from 14 normal, right-handed subjects while they performed two different parity-judgment tasks that require transformations of mental images: a relatively simple task requiring a single transformation (mental letter rotation), and a more complex task involving a coordinated sequence of transformations (mental paper folding). Reaction times increased monotonically with larger angular displacements from the upright (for mental rotation) and with number of squares carried (for mental paper folding). Both the tasks resulted in amplitude modulation of an approximately 420-700 ms latency ERP component at parietal electrodes. Scalp topographies indicated that right parietal cortex was activated during mental rotation, but bilateral parietal regions were activated during mental paper folding. Our results support the notion of a right hemispheric superiority for tasks involving simple, single mental rotations, but indicate greater involvement of the left hemisphere when a more complex sequence of transformations are required. This task-dependent lability of hemispheric function may account for some of the inconsistent results reported by previous neuroimaging and electrophysiological studies.

Turn that frown upside down: ERP effects of thatcherization of misorientated faces.

When inverted, thatcherized faces appear normal. This may be due to a decrease in configural and an increase in featural processing. It is not known whether this processing is continuous or reflects two distinct processing systems. Using event-related potentials (ERPs), we investigated the Thatcher effect on thatcherized and normal faces at varying orientations. The ERPs paralleled the perceptual illusion. The effect of thatcherization on upright faces was visible in P1 and N170 ERP components, possibly reflecting attentional engagement due to unpleasantness of thatcherized faces. Effects were also found over two later components, the P250 component, which has been related to configural recognition, and a late parietal component possibly reflecting featural processing. The effect of thatcherization on the two later components decreased gradually (for the P250 component) and abruptly (for the late parietal component) as the faces were rotated away from the upright.

Perceptual and motor mechanisms for mental rotation of human hands.

We measured brain potentials from human subjects performing a mental rotation task requiring right-left judgments of misoriented hands, and a control task requiring palm-back judgments of the same stimuli. High-density, 128-channel event-related potentials (ERPs) were recorded from 16 normal, right-handed subjects. There was a main effect of task at five different latencies: 148 ms (occipital), 180 ms (parietal), 388 ms (vertex), 556 ms (central-parietal), and 900 ms (vertex). Source estimations derived from topographic data indicate that frontal brain regions were strongly activated after 300 ms in the control task, but not until about 900 ms in the rotation task. We conclude that the neural computations underlying mental hand rotation may be recruited from relatively early stages of visuo-perceptual analysis; these early computations influence subsequent processing within a parietal-prefrontal system for the integration of perception with action.

Animal behaviour: Laterality in tool manufacture by crows.

New Caledonian crows (Fig. 1) fashion tapered tools from either the left or the right edge of the long narrow leaves of pandanus trees or screw pines, which they use to extract invertebrates in rainforest vegetation. Although right-handedness is thought to be uniquely human, we show here that crows from different localities display a widespread laterality in making their tools, indicating that this behaviour is unlikely to be attributable to local social traditions or ecological factors. To our knowledge, this is the first demonstration of species-level laterality in manipulatory skills outside humans.

Is the handedness gene on the X chromosome? Comment on Jones and Martin (2000).

G. V. Jones and M. Martin (2000) argued, contrary to M. C. Corballis (1997), that a gene for handedness might plausibly be located in homologous, noncombining regions of the X and Y chromosomes. The specific model they proposed is unlikely to be correct, but a case can be made for an X-linked gene that has no homologue on the Y chromosome and that is subjected to X-inactivation in females. An X-linked gene predicts no overall sex difference in the incidence of left-handedness; the slight preponderance of left-handers among males might then be attributed to a higher incidence of pathologically induced left-handedness.

Interhemispheric visual matching in the split brain.

Three split-brained subjects, one (N.G.) with full forebrain commissurotomy and two (V.P. and J.W.) with callosotomy, made same-different judgments about pairs of visual stimuli that were flashed either unilaterally or bilaterally. In separate blocks of trials, the stimuli could differ in luminance, size, or color. In the bilateral condition, only J.W. scored above chance, and only minimally, on the luminance and size tasks, and none of the subjects scored above chance on the color task. Accuracy was generally much higher, especially for V.P. and J.W., when the stimuli were unilateral. These results confirm that there is little or no interhemispheric transfer of the visual attributes of luminance, size or color in the split brain.

Interhemispheric comparisons in a man with complete forebrain commissurotomy.

J. Sergent (1991) claimed that split-brained people are highly accurate in judging which is the larger of 2 circles in opposite visual hemifields but are relatively poor at judging whether circles in the 2 hemifields are of the same size. The discrepancy could be due, at least in part, to an artifact. A split-brained man, L.B., was markedly worse than normals at judging which was the larger of 2 circles or the longer of 2 horizontal lines in opposite hemifields, and his performance could be largely accounted for without assuming any interhemispheric transfer. L.B. also judged whether a single flashed line extended further into the left or right hemifield and, as in a previous study (M. C. Corballis, 1995), was strongly biased to respond "right longer." This bias was not observed in the judgments about the circles or the separated lines, suggesting that it is not due to a compression of perceived space in the left hemifield.

Much ado about mirrors.

Takano (1998) has suggested four different kinds of reversal to explain why mirrors reverse left and right and not up and down or back and front. In fact, mirrors perform only one kind of reversal: They simply reverse about their own planes, and reflection about one plane is equivalent to reflection about any other, plus a translocation and rotation. The reflection of an object is termed its enantiomorph. Perception of the enantiomorphic relation normally requires an act, either physical or mental, of alignment. In deciding whether two objects are enantiomorphs, there is a tendency to align them so that the reversal is about the axis of least asymmetry. But in deciding whether a single object is one of two possible enantiomorphic forms, people generally rotate it to some canonical orientation. In the case of objects with defined top-bottom, back-front, and left-right axes, the canonical orientation is determined by the top-bottom and back-front axes, leaving the left-right axis to carry the reversal. The main reason for this, I suggest, is that the top-bottom and back-front axes have functional priority, and the left-right axis cannot be defined until top-bottom and back-front are established. This means that the latter two axes have priority in establishing the canonical orientation. The left-right axis is usually, but not always, the axis of least asymmetry.

Incomplete gustatory lateralization as shown by analysis of taste discrimination after callosotomy.

The lateral organization of the gustatory pathway in man is incompletely understood. Majority of the studies support an uncrossed projection from each side of the tongue to the cortex, but reports of an opposite crossed organization continue to appear in the neurological literature. We studied the lateral organization of the gustatory pathway in normal controls, a man with a complete callosal agenesis, and a man with a complete section of the corpus callosum, a right anterior-frontal lesion, and language in the left hemisphere. Sapid solutions were applied to one or the other side of the tongue, and subjects reported the taste of the stimulus either verbally or by manually pointing to the name of the taste. There were no differences in accuracy and reaction time between the right and left hemitongues of the controls and the genetically acallosal observer. By contrast, the callosotomy subject showed a constant marked advantage of the left hemitongue over the right for both accuracy and speed of response, though performance with right stimuli was clearly above chance. The left advantage can be attributed to the left hemisphere being favored by the essentially verbal nature of the task, or to the presence of a lesion in cortical gustatory areas in the right hemisphere, or to both factors. Whichever of these hypotheses turns out to be correct, the results unequivocally reject the notion of an exclusively crossed organization of the gustatory pathway from the tongue to the cortex, and favor the notion of a bilaterally distributed organization of this pathway with a marked predominance of the uncrossed over the crossed component.

Interhemispheric visual integration in three cases of familial callosal agenesis.

Three cases of callosal agenesis (a 39-year-old woman and her 11- and 12-year-old daughters) were tested on their ability to integrate visual information between the visual hemifields. They were all able to name colors and digits in either hemifield with high accuracy and were able to decide whether letters or digits in opposite hemifields were the same or different. They had greater difficulty deciding whether colors in opposite hemifields were the same or different. When shown 6-letter words made up of pairs of 3-letter words that straddled the midline (e.g., MANAGE, ROTATE), they responded to them as whole words and never as 3-letter words, suggesting perceptual continuity across the midline, at least for verbal material. The most likely interpretation is that the integration of form, but not color, is achieved through the intact anterior commissure in these participants.

Effect of luminance on successiveness discrimination in the absence of the corpus callosum.

Three split-brained subjects, one with full forebrain commissurotomy and two with callosotomy, were impaired at judging whether pairs of lights in opposite visual fields were successive or simultaneous. This impairment did not vary with luminance when the lights were grey against a dark background, but was more pronounced when the lights were equiluminant with a yellow background. All three subjects were also better able to discriminate succession from simultaneity when the lights were both in the left visual field than when they were both in the right. A fourth subject with callosal agenesis was only slightly impaired relative to normal subjects, who were virtually errorless.

Interhemispheric transfer of colour and shape information in the presence and absence of the corpus callosum.

Two split-brained subjects, one (L.B.) with full forebrain commissurotomy and one (R.B.) with callosal agenesis, and a group of twenty neurologically intact subjects were tested in three discrimination tasks: a go-no go task, a two-choice task, and a three-choice task. The discriminations were based on colour in Experiment 1, and on shape in Experiment 2. The stimuli were presented in one or other visual field, and the subjects responded with the fingers of one or other hand, allowing the differences in reaction time between crossed and uncrossed responses (CUD) to be calculated. For the normal subjects the CUD tended to diminish with the complexity of the tasks, suggesting that both hemispheres were increasingly involved. Unlike R.B. and the normal controls, who made virtually no errors, L.B. had increasing difficulty as task complexity increased. He was better able to transfer information from the right to the left hemisphere than vice versa, but an analysis of his accuracy under the crossed conditions showed that the amount transferred was always well under one bit. This confirms previous evidence that L.B. has very limited subcortical transfer of either colour or shape.

Sperry and the Age of Aquarius: science, values and the split brain.

Although Sperry's empirical science reinforced a materialist view of the relation between mind and brain, his concept of an emergent consciousness that could causally influence neural function is reminiscent of Cartesian dualism, purportedly allowing for free will, individual responsibility for action and a synthesis of science with moral and religious values. Yet Sperry insisted that his view was entirely materialistic and that the critical distinction was not between a non-material mind and a material brain, but rather between holism and reductionism. A similar distinction is attributed to right- vs left-brain modes of thought as revealed by the split-brain studies, and Sperry's hope for the unification of holistic and reductionist approaches may also relate to his conviction that these two modes are fundamentally unified in the normal brain.

Role of the commissures in interhemispheric temporal judgments.

A man who had undergone forebrain commissurotomy (L.B.) and a man with agenesis of the corpus callosum (R.B.) judged whether pairs of spatially separated lights were successive or simultaneous. Stimulus onset asynchronies (SOAs) were 0, 17, 33, 50, 67, 83, 117, and 150 ms. When the lights were in opposite visual fields, the SOA at which the discrimination first reached a level significantly above chance was 150 ms for L.B., 67 ms for R.B., and 33 ms for "normal" participants. Results parallel evidence from reaction time studies in which estimates of interhemispheric transfer time for callosal agenesis patients lie between those of normal controls and those with surgical section of the forebrain commissures. L.B. also showed a left-visual-field deficit in the discrimination, though it was less marked than his deficit with bilateral presentations.

Interhemispheric neural summation in the absence of the corpus callosum.

One subject with full forebrain commissurotomy (L.B.), two with callosotomy (J.W. and M.E.), one with callosal agenesis (R.B.) and 10 normal subjects performed a simple reaction time task in which visual stimuli were either presented singly in one or other visual field, or in both visual fields simultaneously. Reaction times were faster to double stimuli than to single ones, but in the normal subjects this 'redundancy gain' did not exceed that predicted by probability summation (the horse-race model). In the four subjects lacking the corpus callosum, the gain did exceed that predicted by probability summation when the stimuli were brighter than the background, implying subcortical neural summation. In the three surgical cases (L.B., J.W. and M.E.) the gain was greatly diminished when the stimuli were equiluminant with the background, suggesting that neural summation occurred at the collicular level. In normal subjects, callosal transfer may ensure that at least some degree of interhemispheric neural summation occurs, even with unilateral input. The acallosal subject (R.B.) was anomalous in that neural summation was not diminished by equiluminance.

Interhemispheric transmission times in the presence and absence of the forebrain commissures: effects of luminance and equiluminance.

One subject (L.B.) with full forebrain commissurotomy, one (R.B.) with callosal agenesis and 20 normal controls were tested for simple reaction time (RT) with each hand, to visual stimuli in one or the other visual field. RTs for uncrossed conditions (hand ipsilateral to the visual field) were subtracted from RT to crossed conditions (hand contralateral to the visual field) to yield the crossed-uncrossed difference (CUD), taken to be a measure of interhemispheric transfer time. CUDs increased from an average of 4.9 ms among the control subjects, to 23.3 ms for R.B., to 53.1 ms for L.B. Although overall RTs in all subjects increased with decreasing luminance of the stimuli, the CUD was not systematically affected and remained largely unaffected even under equiluminance. The results support previous evidence that interhemispheric transfer, even in the split brain, depends on visually insensitive pathways.

Cerebral asymmetry: motoring on.

I argue that the phylogenetic and neurobiological bases for cerebral asymmetry in humans are likely to be found in motor systems rather than in perceptual systems. Current genetic models of human laterality suggest that a `dextral' allele might be responsible for right-handedness and left-cerebral dominance for speech in the majority of humans. The linking of handedness with language lateralization might reflect the early evolution of language as predominantly a system of manual gestures, perhaps switching to a mainly vocal system only with the emergence of Homo sapiens. So-called `mirror neurons' in the prefrontal cortex of the monkey, which fire both when the animal makes a grasping response and when it sees the same response performed by others, might be part of a circuit that is the precursor to language circuits in the brain. This circuit appears to be bilateral in monkeys, but left-hemispheric in humans.