Hand preference and its flexibility according to the position of the object: a study in cercopithecines examining spontaneous behaviour and an experimental task (the Bishop QHP task)

The extant literature on manual laterality in non-human primates is inconclusive, plagued by inconsistent or contradictory findings and by disturbing methodological issues (e.g. uncontrolled influential factors, comparability issues). The present study examined hand preference and its flexibility in 15 red-capped mangabeys (C. t. torquatus) and 13 Campbell's monkeys (C. c. campbelli), two species that differ in their degree of arboreality. We investigated the influence of the spatial position of the object on hand preference for reaching. We considered spontaneous behaviour (reaching for food during daily feeding) and an experimental task: the QHP task. The QHP is a task that is used in humans. This is a simple reaching task that involves high spatial constraints on hand use. In our study, the subject had to reach for items that were placed on a semi-circle in front of it on five positions, including in the centre position, in the ipsilateral space and in the contralateral space. We assessed hand preference for reaching in front (baseline condition), and we examined how this preference changed when reaching in lateral positions. For reaching in front, about half of the subjects were lateralized and no group-level bias occurred, for both spontaneous and experimental conditions. When considering reaching in the lateral positions, we observed that the position of the object influenced hand use: individuals used the hand that was closest to the object. The results are discussed in relation to previous findings in humans and in non-human primates and regarding theories on handedness and flexibility of hand preference.     

Visual laterality responses to different emotive stimuli by red-capped mangabeys, Cercocebus torquatus torquatus

Hemispheric asymmetry in emotional perception has been put forward by different theories as the right hemisphere theory or the valence theory. But no consensus was found about the role played by both hemispheres. So, in order to test the different theories, we investigated preferential use of one eye in red-capped mangabeys, at the individual as well as at the group level. In this study we investigated the influence of the emotional value of stimuli on the direction and strength of visual preference of 14 red-capped mangabeys. Temporal stability of the bias of use of a given eye was evaluated by comparing our current results to those obtained 2.5 months previously. Two experimental devices, a tube and a box, tested five different stimuli: four food types varying in palatability and a neutral stimulus. The subjects’ food preferences were evaluated before testing the laterality. The mangabeys used their left eyes predominantly at the group level for the tube task. The majority of the subjects showed a visual preference at the individual level for the box task, but this bias was not present at the group level. As the palatability of the stimuli increased, the number of lateralized subjects and the number of subjects using preferentially their left eye increased. Similarly, the strength of laterality was related to food preference. Strength of laterality was significantly higher for subjects using their left eye than for subjects using their right eye. Preferential use of a given eye was stable over short periods 2.5 months later. Our data agree with reports on visual laterality for other species. Our results support the valence theory of a hemispheric sharing of control of emotions in relation to their emotional value.     

Sex differences in cerebral laterality of language and visuospatial processing

Sex differences on language and visuospatial tasks are of great interest, with differences in hemispheric laterality hypothesized to exist between males and females. Some functional imaging studies examining sex differences have shown that males are more left lateralized on language tasks and females are more right lateralized on visuospatial tasks; however, findings are inconsistent. Here we used functional magnetic resonance imaging to study thirty participants, matched on task performance, during phonological and visuospatial tasks. For each task, region-of-interest analyses were used to test differences in cerebral laterality. Results indicate that lateralization differences exist, with males more left lateralized during the phonological task and showing greater bilateral activity during the visuospatial task, whereas females showed greater bilateral activity during the phonological task and were more right lateralized during the visuospatial task. Our data provide clear evidence for differences in laterality between males and females when processing language versus visuospatial information.     

Hand preferences in unimanual and bimanual feeding by wild vervet monkeys (Cercopithecus aethiops)

Lateral preference was examined in spontaneous feeding actions in 2 troops of wild vervet monkeys (Cercopithecus aethiops). Processing of 4 foods (termites, leaf shoots, sugarcane, and fruit) was studied. Actions included unimanual reaching to moving objects, operating from an unstable posture, and coordinated bimanual processing. Between 19 and 31 subjects were available, according to the task. In 2 tasks, laterality of 2 independent stages was measured separately, giving 6 measures in all. On 4 of these measures, most monkeys were ambipreferent, and only a few showed significant hand preferences. Only for termite feeding and detaching material from fruits did the majority show significant lateralization; no tasks elicited exclusive use of 1 hand. Preference appeared labile, because in 2 tasks, population trends reversed with increasing age. No population trends to left or right were found; instead, these monkeys showed ambilaterality, with lateralization associated with task complexity.     

Verbal asymmetries and levels of processing in an interactive dual-task paradigm

This study examined how the dual-task laterality paradigm produces patterns of cerebral asymmetry different from those obtained in studies of comparable single-laterality tasks. We systematically examined at what level of processing a concurrent verbal memory-load influences accuracy of recognition of laterally presented nouns relative to that in a control condition. Four groups of 20 subjects each were tested in an interactive dual-task paradigm requiring them to compare lateralized nouns directly with one of three nouns concurrently held in memory prior to accuracy of recognition. The groups differed according to the types of comparisons being made: physical identity, phonetic orthographic similarity, phonetic similarity using non-orthographic words, and category membership. Subjects in each group carried out three tasks. They were required to determine if a specified match had occurred between a memory-load word and the lateralized word, identify the lateralized word, and report the memory-load words. Another 20 subjects were assigned to a control laterality condition in which no concurrent memory-load was used. Control subjects were required to respond to a laterally presented word by pressing a reaction-time key to indicate recognition of the word and then to report the word. No significant visual-field differences occurred in accuracy of recognition for either the control or matching-task groups. However, reaction-time latencies and errors increased as a function of the level of processing. The accuracy of recognition did not support the predictions of Kinsbourne's attentional model but the reaction times provided some support for the concept of selective left-hemisphere interference proposed by Hellige. A limited-capacity approach was suggested as a possible alternative explanation of laterality effects.     

Hemispheric specialization for reading

Behavioral laterality tasks with linguistic stimuli were used to assess the differential processing efficiencies of the cerebral hemispheres in right- and left-handed adults. Findings from a lateralized lexical decision task with concrete nouns supported Zaidel's (1983) "direct access" model of hemispheric functioning. A dual task consisting of oral and silent reading indicated that the right hand was significantly more disrupted than the left during unimanual finger tapping; however, some bilateral interference was observed. Taken together the findings suggest that although the left hemisphere was relatively more efficient, the right hemisphere was dynamically involved in the reading process.     

Multitask investigation of individual differences in hemispheric asymmetry

Right-handed subjects (N = 120) participated in four different laterality tasks designed to measure aspects of cerebral hemisphere asymmetry: identification of dichotically presented consonant-vowel syllables (CVs), examination of the effects of concurrent repetition of CVs and concurrent anagram solution on finger-tapping by the right and left hands, lateralized identification of CVs presented tachistoscopically to the left and right visual fields, and left/right biases on a free-vision face task involving judgments of emotion. Ear differences in the dichotic listening task were related to the pattern of lateralized interference in the dual-task finger-tapping paradigm. There were no other significant relations between pairs of tasks, but when the present results are considered in the light of other recent experiments, there appears to be a relation between lateral bias on the free-vision face task and visual field differences in tachistoscopic identification. The pattern of results has implications for hypothesized individual differences among right-handers in cerebral dominance for verbal processes, input pathway dominance, and asymmetric arousal of the two cerebral hemispheres.     

Hemispheric involvement in shadowing vs. interpretation: a time-sharing study of simultaneous interpreters with matched bilingual and monolingual controls

A time-sharing study used shadowing and interpretation/paraphrasing tasks to evaluate lateralization in professional interpreters individually matched to bilingual and monolingual controls. A two-step multivariate general linear model procedure was used to determine lateralized effects and extent of disruption produced by the tasks. Results revealed the monolingual group to be left lateralized for both tasks, but the two bilingual groups were lateralized in the LH only for shadowing. The monolingual group was significantly different from the bilingual groups in the pattern of hand asymmetry for interpretation/paraphrasing. The findings replicate outcomes of prior repeated measures analysis of variance procedures on percentage of change scores. However, new information is added by the more refined analysis. The findings are also discussed in terms of previous laterality studies using similar tasks and subject samples.     

Lateralized Increases in Cerebral Blood Flow during Performance of Verbal and Spatial Tasks: Relationship with Performance Level

Physiologic neuroimaging studies have shown lateralized regional increase in brain activity during cognitive tasks, but the hypothesis that such changes are correlated with task performance has not been tested directly. We examined cerebral blood flow (CBF) changes induced by cognitive tasks in relation to performance. CBF was measured with the ¹³³Xenon clearance method in 34 normal right-handed young (age < 30) volunteers during resting baseline and during the performance of a verbal analogies and a spatial line orientation test. Performance measures included "speed" and "power" estimates of both activation tasks. Resting CBF was moderately correlated with performance. The correlations were slightly higher with activated CBF for verbal but not spatial performance. The degree of increase (task-baseline) did not correlate with performance for either task. The highest and topographically specific correlations were obtained between laterality of CBF and verbal performance. Higher left hemispheric activation was correlated with verbal performance, and this correlation was significantly higher in the angular gyrus region. For the spatial task the correlations were with relatively higher right hemispheric activation but without regional specificity. The results underscore the importance of integrating behavioral performance data with physiologic measures in neuroimaging activation studies.     

Paw preference is not affected by postural demand in a nonprimate mammal (Felis silvestris catus)

Previously, it has been thought that handedness is unique to humans. Recently, it has been found that hand or paw preferences are common among a variety of vertebrate species. Different models have been put forth to describe the evolution of primate handedness. In this study we aimed to explore whether these models can also be used to predict manual laterality in nonprimate mammalian groups. The cat (Felis silvestris catus) is a good nonprimate model for manual laterality, as cats frequently use paws to catch and hold prey. Cats were exposed to two standardized manual laterality tasks, differing in postural demand. Subjects (N = 28) were forced to use either a stable or unstable body posture (i.e., sitting or standing vs. vertical clinging) to extract food items from a plastic box attached at two different heights. We revealed that cats exhibited paw preferences at an individual level with about 40% left, 30% right, 30% nonlateralized subjects. Postural demand was linked to task difficulty: the unstable body posture was found to be significantly more difficult than the stable body posture. However, these differences in postural demand and task difficulty did not lead to differences in direction or strength of paw preference. Findings suggested that nonprimate mammals differ from primates in their sensitivity to task related factors, such as postural demand. Results coincide with those of some prosimians, providing support for the hypothesis that postural demand and the associated task complexity became influencing factors on manual laterality in the course of primate evolution.     

Temporal dynamics of interference in Simon and Eriksen tasks considered within the context of a dual-process model

Behavioral and brain potential measures were employed to compare interference in Eriksen and Simon tasks. Assuming a dual-process model of interference elicited in speeded response tasks, we hypothesized that only lateralized stimuli in the Simon task induce fast S–R priming via direct unconditional processes, while Eriksen interference effects are induced later via indirect conditional processes. Delays to responses for incongruent trials were indeed larger in the Eriksen than in the Simon task. Only lateralized stimuli in the Simon task elicited early S–R priming, maximal at parietal areas. Incongruent flankers in the Eriksen task elicited interference later, visible as a lateralized N2. Eriksen interference also elicited an additional component (N350), which accounted for the larger behavioral interference effects in the Eriksen task. The findings suggest that interference and its resolution involve different processes for Simon and Eriksen tasks.     

Motivation, affect, and hemispheric asymmetry: power versus affiliation

In 4 experiments, the authors examined to what extent information related to different social needs (i.e., power vs. affiliation) is associated with hemispheric laterality. Response latencies to a lateralized dot-probe task following lateralized pictures or verbal labels that were associated with positive or negative episodes related to power, affiliation, or achievement revealed clear-cut laterality effects. These effects were a function of need content rather than of valence: Power-related stimuli were associated with right visual field (left hemisphere) superiority, whereas affiliation-related stimuli were associated with left visual field (right hemisphere) superiority. Additional results demonstrated that in contrast to power, affiliation primes were associated with better discrimination between coherent word triads (e.g., goat, pass, and green, all related to mountain) and noncoherent triads, a remote associate task known to activate areas of the right hemisphere.     

Lateralized Changes in Regional Cerebral Blood Flow during Performance of Verbal and Facial Recognition Tasks: Correlations with Performance and “Effort”

Functional neuroimaging has been used to investigate neural substrates of mnemonic processes, and cerebral blood flow (CBF) measures have been sensitive to activation with memory tasks. Studies of memory with two-dimensional¹³³Xenon clearance techniques found that word and face recognition tasks produced contralateral CBF changes in mid-temporal cortical regions. This study replicated the activation paradigm, expanding to the three-dimensional resolution of positron emission tomography (PET). Word and face recognition, and a control baseline task were administered to 19 healthy right-handed volunteers (11 men, 8 women) during successive 10 min PET¹⁵O-water measures of CBF. Quantitative CBF rates were calculated with the arterial input function and the equilibrium model. Redistributions of blood flow were compared across tasks using both absolute and relative (region/whole brain) CBF.Replicating the¹³³Xenon clearance findings, CBF was “appropriately” lateralized during task performance (left–right for words > left–right for faces) in the mid-temporal region. Contrary to predictions, the recognition tasks did not activate expected mesolimbic or prefrontal areas. The task-induced CBF changes also correlated with performance. Bilateral CBF in mid-temporal and parahippocampal gyrus regions of interest correlated with the ability to correctly identify word targets (sensitivity). Left-lateralized CBF in the amygdala and hippocampus correlated with better word sensitivity as well as specificity (ability to correctly reject foils). Complementally, right-lateralized CBF in the parahippocampal gyrus correlated with better face specificity performance. In addition, left-lateralized CBF in the amygdala and right-lateralized CBF in the parahippocampal gyrus and hippocampus correlated with “mental effort” indices (task performance relative to basal ability) for word and face memory tasks, respectively. Thus, whereas this recognition task showed the expected lateralized increase in the mid-temporal region and not in frontal and limbic areas, lateralized activation in some of these areas was associated with better performance. Exploratory analyses on other regions showed lateralized changes in one additional temporal region, the occipital-temporal, and several limbic regions.     

An investigation of immune system disorder as a "marker" for anomalous dominance

Geschwind and Galaburda (1987) proposed that immune disorder (ID) susceptibility, along with left handedness and familial sinistrality (FS), is a "marker" for anomalous dominance. The theory predicts lesser left lateralization for language processes, lessened left hemisphere abilities, and enhanced right hemisphere abilities. We assessed language laterality (dichotic consonant vowel task) and performances on spatial and verbal tasks. Subjects were 128 college students. The factors of handedness, sex, FS, and immune disorder history (negative or positive) were perfectly counterbalanced. Left-handers were significantly less lateralized for language and scored lower than right-handers on the spatial tasks. Females scored lower on mental rotation than males, but performed comparably to males on the spatial relations task. The only effect of ID was by way of interaction with FS on both spatial tasks--subjects who were either negative or positive on both FS and ID status factors scored significantly higher than subjects negative for one but positive for the other factor. A speculative explanatory model for this interaction was proposed. The model incorporates the notion that FS and ID factors are comparably correlated, but in opposite directions, with hormonal factors implicated by other research as relevant for spatial ability differences. Finally, no support for the "anomalous dominance" hypothesis predictions was found.     

Absence of exposure time influence on lateralized face recognition and object naming latency tasks

J. Sergent (1982, Perception & Psychophysics, 31, 451-461; 1983, Psychological Bulletin, 93, 481-512) postulates that the left cerebral hemisphere preferentially extracts higher spatial frequency information, while the right hemisphere preferentially extracts lower frequency spatial information, from the visual scene. According to this view, shorter exposure times favor better right than left hemisphere performance, while longer exposure times favor better left than right hemisphere performance on tachistoscopic laterality tasks. We studied the effects of a threefold variation (40 msec versus 120 msec) in exposure duration, with constant 3-mL luminance, on face recognition and on object naming latency task performances. These are the same stimulus parameters employed by J. Sergent (1983, Psychological Bulletin, 93, 481-512) to demonstrate exposure duration effects in a task requiring the judgment of the sex of models from face photographs. We found the expected LVF superiority on the face recognition task and RVF superiority on the object naming task. There was, however, no influence of exposure duration on the performances. It is concluded that these tasks, which tap established lateralized processing asymmetries, are quite robust in their resistance to exposure time influence.     

Working Memory for Temporal and Nontemporal Events in Monkeys

This is the first report that introduces appropriate behavioral tasks for monkeys for investigations of working memory for temporal and nontemporal events. Using several behavioral tests, the study also shows how temporal information is coded during retention intervals in the tasks. Each of three monkeys was trained with two working memory tasks: delayed matching-to-sample of stimulus duration (DMS-D) and delayed matching-to-sample of stimulus color (DMS-C). The two tasks employed an identical apparatus and responses and differed only in the temporal and nontemporal attribute of the stimuli to be retained for correct performance. When a retention interval between the sample and comparison stimuli was prolonged, the monkeys made more incorrect responses to short samples in the DMS-C task, suggesting “trace decay” of memory for short stimuli. However, the same monkeys showed no such increase in incorrect responses to short samples in the DMS-D task, suggesting active coding of temporal information, that is, the length of stimulus duration, during the retention interval. When variable lengths of samples were presented with a fixed retention interval, the monkeys made more incorrect responses when length differences between short and long samples were small in the DMS-D task, but not in the DMS-C task. This suggests that the codes of working memory retained in the DMS-D task were not absolute (analogical) but rather were relative (categorical) and related to differences in the duration of the samples.     

Valence specific laterality effects in free viewing conditions: the role of expectancy and gender of image

Recent research has looked at whether the expectancy of an emotion can account for subsequent valence specific laterality effects of prosodic emotion, though no research has examined this effect for facial emotion. In the study here (n=58), we investigated this issue using two tasks; an emotional face perception task and a novel word task that involved categorising positive and negative words. In the face perception task a valence specific laterality effect was found for surprise (positive) and anger (negative) faces in the control but not expectancy condition. Interestingly, lateralisation differed for face gender, revealing a left hemisphere advantage for male faces and a right hemisphere advantage for female faces. In the word task, an affective priming effect was found, with higher accuracy when valence of picture prime and word target were congruent. Target words were also responded to faster when presented to the LVF versus RVF in the expectancy but not control condition. These findings suggest that expecting an emotion influences laterality processing but that this differs in terms of the perceptual/experience dimension of the task. Further, that hemispheric processing of emotional expressions appear to differ in the gender of the image.     

The effects of control and lack of control on active and passive avoidance in rhesus monkeys

Most studies which have examined the effects of lack of control have utilized test tasks in which active responding is required, and generally they have found impaired learning. Those few studies which have required passive responding in the test task generally have found facilitation of learning. The present two experiments examined the effects of lack of control in both active and passive avoidance tasks in a primate species (Macaco mulatta) not previously used in this research area. In Experiment 1, although the group without control (IE) tended to be inferior at active and superior at passive avoidance in comparison to the group with control (E), there were no significant differences. In Experiment 2, utilizing a difficult discrimination task in which subjects were required to learn when and when not to respond actively to avoid aversive stimulation, greater group differences were found. Two monkeys from Group IE failed to escape in active avoidance acquisition and, as a whole. Group IE was somewhat slower to respond than Group E. At passive avoidance, however. Group IE was superior to Group E and, as a consequence, more efficiently solved the discrimination problem. Implications of the present results for interpretation of the effects of lack of control as deficits are discussed.     

Hemispatial neglect and serial order in verbal working memory

Working memory refers to our ability to actively maintain and process a limited amount of information during a brief period of time. Often, not only the information itself but also its serial order is crucial for good task performance. It was recently proposed that serial order is grounded in spatial cognition. Here, we compared performance of a group of right hemisphere-damaged patients with hemispatial neglect to healthy controls in verbal working memory tasks. Participants memorized sequences of consonants at span level and had to judge whether a target consonant belonged to the memorized sequence (item task) or whether a pair of consonants were presented in the same order as in the memorized sequence (order task). In line with this idea that serial order is grounded in spatial cognition, we found that neglect patients made significantly more errors in the order task than in the item task compared to healthy controls. Furthermore, this deficit seemed functionally related to neglect severity and was more frequently observed following right posterior brain damage. Interestingly, this specific impairment for serial order in verbal working memory was not lateralized. We advance the hypotheses of a potential contribution to the deficit of serial order in neglect patients of either or both (1) reduced spatial working memory capacity that enables to keep track of the spatial codes that provide memorized items with a positional context, (2) a spatial compression of these codes in the intact representational space.     

Ontogenetic dissociation between habit learning and recognition memory in capuchin monkeys (Cebus apella)

The performance of young and adult capuchin monkeys (Cebus apella) on a Concurrent Discrimination Learning (CDL) test and a Delayed Non-Matching to Sample (DNMS) task were investigated. Results indicate that all subjects were able to learn the CDL test with 20-pairs simultaneously and retain this stimulus/reward association within 24-h interval. In contrast, young subjects did not perform the DNMS task with the same proficiency as adults. While adults' scores were above chance across all memory test delays, the young capuchin monkeys performed the test by chance level. These results support the hypothesis that these two tasks require different cognitive processes mediated by two independent neural systems with a differentiated ontogenetic development. Moreover, they provide evidence that this dissociation occurs not only in humans and Old World monkeys but also in the New World capuchin monkeys indicating that this species can be a valuable alternative model for investigations of the neurobiological basis of memory.