Survival with an asymmetrical brain: advantages and disadvantages of cerebral lateralization

Recent evidence in natural and semi-natural settings has revealed a variety of left-right perceptual asymmetries among vertebrates. These include preferential use of the left or right visual hemifield during activities such as searching for food, agonistic responses, or escape from predators in animals as different as fish, amphibians, reptiles, birds, and mammals. There are obvious disadvantages in showing such directional asymmetries because relevant stimuli may be located to the animal's left or right at random; there is no a priori association between the meaning of a stimulus (e.g., its being a predator or a food item) and its being located to the animal's left or right. Moreover, other organisms (e.g., predators) could exploit the predictability of behavior that arises from population-level lateral biases. It might be argued that lateralization of function enhances cognitive capacity and efficiency of the brain, thus counteracting the ecological disadvantages of lateral biases in behavior. However, such an increase in brain efficiency could be obtained by each individual being lateralized without any need to align the direction of the asymmetry in the majority of the individuals of the population. Here we argue that the alignment of the direction of behavioral asymmetries at the population level arises as an "evolutionarily stable strategy" under "social" pressures occurring when individually asymmetrical organisms must coordinate their behavior with the behavior of other asymmetrical organisms of the same or different species.     

Lateralized interhemispheric transfer of color cues: evidence for dynamic coding principles of visual lateralization in pigeons

Visual feature discrimination tasks in pigeons reveal a right eye/left hemisphere dominance at the population level. Anatomical studies and lesion data show this visual lateralization to be related to asymmetries of the tectofugal system, which ascends from the tectum over the n. rotundus to the forebrain. Anatomically, this system is characterized by numerous morphological and connectional asymmetries which result in a bilateral visual representation in the dominant left hemisphere and a mostly contralateral representation in the subdominant right hemisphere. Ontogenetically, visual lateralization starts with an asymmetrical embryonic position within the egg, which leads to asymmetries of light stimulation. Differences in exposure to light stimulation between the eyes result in activity differences between the ascending tectofugal pathways of the left and the right hemisphere, which are transcribed during a critical time span into morphological asymmetries. The asymmetries established after this transient period finally start to determine the lateralized processes of the visual system for the entire life span of the individual. We now can show that these anatomical lateralizations are accompanied by asymmetries of interocular transfer, which enable a faster shift of learned color cues from the dominant right to the left eye than vice versa. In summary, our data provide evidence that cerebral asymmetries are based both on "static" anatomical and on "dynamic" process-dependent principles.     

Hemifield asymmetries differentiate VSTM for single- and multiple-feature objects

Visual short-term memory (VSTM) is a capacity-limited system for maintaining visual information across brief durations. Limits in the amount of information held in memory reflect processing constraints in the intraparietal sulcus (IPS), a region of the frontoparietal network also involved in visual attention. During VSTM and visual attention, areas of IPS demonstrate hemispheric asymmetries. Whereas the left hemisphere represents information in only the right hemifield, the right hemisphere represents information across the visual field. In visual attention, hemispheric asymmetries are associated with differences in behavioral performance across the visual field. In order to assess the degree of hemifield asymmetries in VSTM, we measured memory performance across the visual field for both single- and two-feature objects. Consistent with theories of right-hemisphere dominance, there was a memory benefit for single-feature items in the left visual hemifield. However, when the number of features increased, the behavioral bias reversed, demonstrating a benefit for remembering two-feature objects in the right hemifield. On an individual basis, the cost of remembering an additional feature in the hemifields was correlated, suggesting that the shift in hemifield biases reflected a redistribution of resources across the visual field. Furthermore, we demonstrate that these results cannot be explained by differences in perceptual or decision-making load. Our results are consistent with a flexible resource model of VSTM in which attention and/or working memory demands result in representation of items in the right hemifield by both the left and right hemispheres.     

Monocular asymmetries in recognition after an eye movement: Sighting dominance and dextrality

Although monocular recognition scores for targets presented immediately after an eye movement do not differ, the two eyes show marked recognition asymmetries when both eyes are receiving inputs but a specific target is only presented to one. In general, the right eye performs better than the left, although there are interactions with sighting dominance and the direction of eye movement.     

Where a person with a squint is actually looking: Gaze-cued orienting in crossed eyes

In this study, we investigated gaze-cued attention orienting when the perceived eyes are not looking in the same direction. This condition occurs in strabismus (squint). Participants were asked to detect laterally presented reaction signals preceded by schematic faces in which the direction (left, straight, or right) of the left and right eye was independently manipulated. Consistent with earlier studies, the results showed a reliable cuing effect by two eyes with parallel gaze direction. Gaze-cued orienting was also shown in a situation when one eye was averted and the other eye was looking straight ahead. The gaze cuing was not significantly stronger in the former than in the latter situation. When both eyes were either nasally or temporally averted, no shifts of visual attention were observed. The results suggest that, if both eyes are visible, the direction of both eyes is computed and integrated for the gaze-cued orienting.     

Early visual experience influences behavioral lateralization in the guppy

Individual differences in lateralization of cognitive functions characterize both humans and non-human species. Genetic factors can account for only a fraction of the variance observed and the source of individual variation in laterality remains in large part elusive. Various environmental factors have been suggested to modulate the development of lateralization, including asymmetrical stimulation of the sensory system during ontogeny. In this study, we raised newborn guppies in an asymmetric environment to test the hypothesis that early left–right asymmetries in visual input may affect the development of cerebral asymmetries. Each fish was raised in an impoverished environment but could voluntarily observe a complex scene in a nearby compartment containing a group of conspecifics. Using asymmetric structures, we allowed some subjects to observe the complex scene with the right eye, others with the left eye, and control fish with both eyes. Among asymmetrically stimulated fish, the mirror test revealed eye dominance congruent with the direction of asymmetric stimulation, while controls showed no left–right laterality bias. Interestingly, asymmetric exposure to social stimuli also affected another aspect of visual lateralization—eye preference for scrutinizing a potential predator—but did not influence a measure of motor asymmetry. As the natural environment of guppies is fundamentally asymmetrical, we suggest that unequal left–right stimulation is a common occurrence in developing guppies and may represent a primary source of individual variation in lateralization as well as an efficient mechanism for producing laterality phenotypes that are adapted to local environmental conditions.     

Don’t look! don’t touch! inhibitory control of eye and hand movements

Inhibitory control of eye and hand movements was compared in the stop-signal task. Subjects moved their eyes to the right or left or pressed keys on the right or left in response to visual stimuli. The stimuli were either central (angle brackets pointing left or right) or peripheral (plus signs turning into Xs left or right of fixation), and the task was either pro (respond on the same side as the stimulus) or anti (respond on the opposite side). Occasionally, a stop signal was presented, which instructed subjects to inhibit their responses to the go stimulus. Stop-signal reaction times (SSRTs) were faster overall for eye movements than for hand movements, and they were affected differently by stimulus conditions (central vs. peripheral) and task (pro vs. anti), suggesting that the eyes and hands are inhibited by different processes operating under similar principles (i.e., a race between stop and go processes).     

Can theories of visual representation help to explain asymmetries in amygdala function?

Emotional processing differs between the left and right hemispheres of the brain, and functional differences have been reported more specifically between the left and right amygdalae, subcortical structures heavily implicated in emotional processing. However, the empirical pattern of amygdalar asymmetries is inconsistent with extant theories of emotional asymmetries. Here we review this discrepancy, and we hypothesize that hemispheric differences in visual object processing help to explain the previously reported functional differences between the left and right amygdalae. The implication that perceptual factors play a large role in determining amygdalar asymmetries may help to explain amygdalar dysfunction in the development and maintenance of posttraumatic stress disorder.     

Perception of geometrical arrays tachistoscopically exposed in right and left visual fields.

Geometrical stimuli (48 6-item arrays of familiar forms, e.g., circle), tachistoscopically presented in the right or left visual field, were more accurately perceived in the right than left visual field by 15 college students. Targets about half the length of the displays exposed here were perceived with equal facility in both visual fields (Bryden, 1960). Results suggest that length of array might affect the difference in perceptual accuracy of forms shown in the right and left visual fields. Figures in the right visual field were predominantly processed from left to right, and forms in the left visual field from right to left. Since more symbols were identified in the right than left visual field, the left to right encoding sequence may be more efficient than a right to left movement. Limited experience of most Ss in reading symbols from left to right is probably only one factor. Extensive experience reading alphabetical material from left to right might have developed the physiological mechanism underpinning this sequence more than the one serving the opposite movement.     

Lateralization of a food search task in the domestic chick

Monocularly occluded Warren sex-linked domestic chicks (Gallus domesticus) were presented with a search test which required the differentiation of familiar food grains from unfamiliar pebbles bearing a strong resemblance to food. Male and female chicks using their left eye performed this discrimination significantly more poorly than did chicks using their right eye, both during learning and after asymptotic performance was reached. This left/right difference was superimposed upon a difference between the sexes, with females pecking fewer pebbles than males. Because of the complexity of the search test utilized, it is difficult to determine whether the left/right difference found is attributable to lateralization of visual discrimination ability or to other factors, such as lateralized differences in food search pattern or investigatory responses to novel pebbles. Nevertheless, asymmetric responses of this type provide additional evidence that lateralization of function in the brain, long thought to be a uniquely human phenomenon, is widespread among vertebrates.     

Asynchrony of lateral onset as a factor in difference in visual field.

An experiment in matching judgments was designed to examine a role of perceptual process in apparent asymmetry. Recognition of Hirakana letters (Japanese letters) was required. The experimental condition in which stimuli were presented to the left visual field first and to the right visual field second produced more errors for all stimulus intervals (0 to 60 msec.) than experimental conditions where stimuli were presented to the right visual field first and to the left one second. Especially, superiority of the latter condition was marked with the longest stimulus interval employed. These results indicate superiority of the left hemisphere function for recognizing Hirakana letters and suggest that not only memory but also perceptual process contributes to this laterality effect.     

Evoked potential and visual half-field evidence for task-dependent cerebral asymmetries in congenitally deaf adults

Evoked potentials to laterally presented stimuli were collected from left and right tempero-parietal sites during performance of two visual half-field tasks, lexical decision, and line orientation discrimination. Reaction time and accuracy data were simultaneously collected. The behavioral data indicated the development of a right field advantage for the lexical decision task as a function of practice. A principal components analysis revealed three independent evoked potential components which displayed task-dependent hemispheric asymmetries. Multiple regression analyses revealed that visual half-field asymmetries in response accuracy were closely related to hemispheric asymmetries on several independent evoked response components. Subject's scores on independent tests of verbal reasoning and spatial relations were also found to be closely related to hemispheric asymmetry on several independent evoked response components. These data support a multidimensional concept of cerebral specialization. They also suggest that visual field asymmetries reflect the confluence of several underlying processes which have independent lateralization distributions across the population. In general, the results underscore the need for further research on the nature of the relationship between cerebral and perceptual asymmetries.     

Verifying visual properties in sentence verification facilitates picture recognition memory

According to the perceptual symbols theory (Barsalou, 1999), sensorimotor simulations underlie the representation of concepts. We investigated whether recognition memory for pictures of concepts was facilitated by earlier representation of visual properties of those concepts. During study, concept names (e.g., apple) were presented in a property verification task with a visual property (e.g., shiny) or with a nonvisual property (e.g., tart). Delayed picture recognition memory was better if the concept name had been presented with a visual property than if it had been presented with a nonvisual property. These results indicate that modality-specific simulations are used for concept representation.     

Visual implicit memory in the left hemisphere: evidence from patients with callosotomies and right occipital lobe lesions

Identification of visually presented objects and words is facilitated by implicit memory for past visual experiences with those items. Several behavioral and neuroimaging studies suggest that this form of memory is dependent on perceptual processes localized in the right occipital lobe. We tested this claim by examining implicit memory in patients with extensive right occipital lobe lesions, using lexical-decision, mirror-reading, picture-fragment, and word-fragment-completion tests, and found that these patients exhibited normal levels of priming. We also examined implicit memory in patients with complete callosotomies, using standard and divided-visual-field word-fragment-completion procedures, and found that the isolated left hemisphere exhibited normal priming effects. The results indicate that the right occipital lobe does not play a necessary role in visual implicit memory, and that the isolated left hemisphere can support normal levels of visual priming in a variety of tasks.     

Support for lateralization of the Whorf effect beyond the realm of color discrimination

Recent work has shown that Whorf effects of language on color discrimination are stronger in the right visual field than in the left. Here we show that this phenomenon is not limited to color: The perception of animal figures (cats and dogs) was more strongly affected by linguistic categories for stimuli presented to the right visual field than those presented to the left. Moreover, the magnitude of the visual field asymmetry was reduced when demands on verbal working memory were increased by a secondary task. This reduction did not occur when the secondary task imposed demands on spatial working memory. Taken together, these results demonstrate that the lateralized Whorf effect may be quite general, reflecting an interaction of linguistic and perceptual codes primarily in the left hemisphere.     

Face processing is enhanced in the left and upper visual hemi-fields

We tested whether two known hemi-field asymmetries would affect visual search with face stimuli. Holistic processing of spatial configurations is better in the left hemi-field, reflecting a right hemisphere specialization, and object recognition is better in the upper visual field, reflecting stronger projections into the ventral stream. Faces tap into holistic processing and object recognition at the same time, which predicts better performance in the left and upper hemi-field, respectively. In the first experiment, participants had to detect a face with a gaze direction different from the remaining faces. Participants were faster to respond when targets were presented in the left and upper hemi-field. The same pattern of results was observed when only the eye region was presented. In the second experiment, we turned the faces upside-down, which eliminated the typical spatial configuration of faces. The left hemi-field advantage disappeared, showing that it is related to holistic processing of faces, whereas the upper hemi-field advantage related to object recognition persisted. Finally, we made the search task easier by asking observers to search for a face with open among closed eyes or vice versa. The easy search task eliminated the need for complex object recognition and, accordingly, the advantage of the upper visual field disappeared. Similarly, the left hemi-field advantage was attenuated. In sum, our findings show that both horizontal and vertical asymmetries affect the search for faces and can be selectively suppressed by changing characteristics of the stimuli.     

Attentional factors in visual field asymmetries.

Over the past 30 years, numerous studies have reported left/right asymmetries in visual field performance, with performance generally superior in the right visual field for verbal tasks and in the left visual field for spatial tasks. These asymmetries parallel those found in neurological studies of hemispheric specialization. Consequently, many investigators have concluded that visual hemifield differences are primarily a reflection of the functional differences between the two cerebral hemispheres. However, alternative explanations proposing that visual field effects are dependent on other factors such as inadequate fixation, eye movements during presentation, postexposural scanning, and attentional biases have been offered. The potential impact of each of these factors on visual field differences are reviewed and discussed. Evidence is provided suggesting that attention and hemispheric functional differences interact to produce the magnitude and direction of visual field differences.     

Similarity-based asymmetries in perceptual matching

Asymmetries, where response times differ depending on the order of two stimuli, have been widely used to explore fundamental aspects of perceptual processing. Given how much is made of asymmetries in the study of perception there has been surprisingly little research into the cognitive mechanisms that may underlie why comparing two objects in isolation depends on the order of presentation. In visual search, for example, asymmetries are typically attributed to fundamental processing characteristics as opposed to the inherent relation between two stimuli. However, one possible explanation for asymmetries found in perceptual processing is that similarity is important in the task and it is similarity itself that is asymmetric. In the current paper, we use a stimulus set for which the transformational account of similarity predicts asymmetries based on differences in transformational complexity. Using the fine-grained measure of reaction time we show that directional differences in transformation distance successfully predict asymmetries in the speed of matching two stimuli in sequence. The results are discussed in relation to the role of transformations in perceptual identification more generally, and how transformations could be revealing about how objects are compared in other experimental contexts where objects are compared directionally (e.g., visual search).     

Ratings of emotion in faces are influenced by the visual field to which stimuli are presented

This experiment was designed to assess the differential impact of initially presenting affective information to the left versus right hemisphere on both the perception of and response to the input. Nineteen right-handed subjects were presented with faces expressing happiness and sadness. Each face was presented twice to each visual field for an 8-sec duration. The electro-oculogram (EOG) was monitored and fed back to subjects to train them to keep their eyes focused on the central fixation point as well as to eliminate trials confounded by eye movement artifact. Following each slide presentation, subjects rated the intensity of the emotional expression depicted in the face and their emotional reaction to the face on a series of 7-point rating scales. Subjects reported perceiving more happiness in response to stimuli initially presented to the left hemisphere (right visual field) compared to presentations of the identical faces to the right hemisphere (left visual field). This effect was predominantly a function of ratings on sad faces. A similar, albeit less robust, effect was found on self-ratings of happiness (the degree to which the face elicited the emotion in the viewer). These data challenge the view that the right hemisphere is uniquely involved in all emotional behavior. The implications of these findings for theories concerning the lateralization of emotional behavior are discussed.     

Deployment of spatial attention to words in central and peripheral vision

Four perceptual identification experiments examined the influence of spatial cues on the recognition of words presented in central vision (with fixation on either the first or last letter of the target word) and in peripheral vision (displaced left or right of a central fixation point). Stimulus location had a strong effect on word identification accuracy in both central and peripheral vision, showing a strong right visual field superiority that did not depend on eccentricity. Valid spatial cues improved word identification for peripherally presented targets but were largely ineffective for centrally presented targets. Effects of spatial cuing interacted with visual field effects in Experiment 1, with valid cues reducing the right visual field superiority for peripherally located targets, but this interaction was shown to depend on the type of neutral cue. These results provide further support for the role of attentional factors in visual field asymmetries obtained with targets in peripheral vision but not with centrally presented targets.