Behavioral asymmetries of psychomotor performance in rhesus monkeys (Macaca mulatta): a dissociation between hand preference and skill.

Hand preferences were recorded for 35 rhesus monkeys (Macaca mulatta) as they manipulated a joystick in response to 2 computerized tasks. These preferences were then used to contrast 8 left- and 10 right-handed subjects on performance measures of hand skill. Individual hand preferences were found, but no significant population asymmetry was observed across the sample. However, the performance data reveal substantial benefits of right-handedness for joystick manipulation, as this group of monkeys mastered the 2 psychomotor tasks significantly faster than did their left-handed counterparts. The data support earlier reports of a right-hand advantage for joystick manipulation and also support the importance of distinguishing between hand preference and manual performance in research on functional asymmetries.     

Visuospatial reaching preferences of common marmosets (Callithrix jacchus): an assessment of individual biases across a variety of tasks

Using multiple measures of hand preference, the authors investigated lateralization at an individual level in 21 common marmosets. Despite showing group biases for sensory and communication functions, these same marmosets did not show a group bias in direction of lateralized hand use. Hand preferences were recorded on four novel reaching tasks requiring different levels of visual guidance and postural control. As found for simple food holding (with the same subjects), they displayed strong individual hand preferences but no group bias indicative of handedness. The strength of hand preference was influenced by task demands: stronger preferences were expressed when subjects adopted a suspended posture, and when "successful" versus "unsuccessful" foraging strategies were compared. Comparisons between visuospatial reaching and simple food holding preferences also revealed that half of the subjects displayed a division of function between the hands/hemispheres; subjects displayed opposing preferences in simple and visuospatial reaching, which would be beneficial for the performance of coordinated bimanual tasks. Given the apparent absence of a selective advantage for handedness, the authors suggest that hand preferences may reflect hemispheric dominance of other cognitive domains (i.e., temperament).     

Note on hand use in the manipulation of joysticks by rhesus monkeys (Macaca mulatta) and chimpanzees (Pan troglodytes)

In a recent article MacNeilage, Studdert-Kennedy, and Lindblom (1987) proposed that nonhuman primate handedness may be contingent on the specific task requirements with visual-spatial tasks yielding left-hand preferences and fine motor tasks producing right-hand preferences. This study reports hand preferences in the manipulation of joysticks by 2 rhesus monkeys (Macaca mulatta) and 3 chimpanzees (Pan troglodytes). Reach data were also collected on these same subjects and served as a basis for comparison with preference data for manipulation of the joystick. The data indicated that all 5 subjects demonstrated significant right-hand preferences in manipulating the joystick. In contrast, no significant hand preferences were found for the reach data. Reaction time data also indicated that the right hand could perform a perceptual-motor task better than the left hand in all 5 subjects. Overall, the data indicate that reach tasks may not be sensitive enough measures to produce reliable hand preferences, whereas tasks that assess fine motor control produce significant hand preferences.     

Development of hand preferences in marmosets (Callithrix jacchus) and effects of aging

The authors investigated the development of unimanual hand use and hand preferences during feeding in 15 marmosets (Callithrix jacchus), ages birth to 51-70 months. Bimanual hand use was common at 1-2 months, but by 5-8 months unimanual holding had developed and so had significant hand preferences. Half of the marmosets preferred to pick up and take food to the mouth with the left hand, and half preferred the right hand. Individuals maintained the same hand preference at all ages examined. Significant relationships were also found between the postures adopted during feeding and the direction of hand preferences displayed by juvenile marmosets. There was a positive correlation between increased suspension and increased left-hand preference, and a negative correlation between increased feeding in a tripedal posture and increased left-hand preference. These results are discussed in terms of motor development and hemispheric specialization.     

Asymmetrical hand use in rhesus monkeys (Macaca mulatta) in tactually and visually regulated tasks

Asymmetrical hand use by rhesus monkeys (Macaca mulatta) was investigated in a series of tactually and visually guided tasks. The 1st experiment recorded manual preferences of 29 monkeys for solving a haptic discrimination task in a hanging posture. There was a left-hand population bias: 21 monkeys had a left-hand bias, 4 a right-hand bias, and 4 no bias. The 2nd experiment, 4 tasks with 23 to 51 monkeys, investigated the critical components of the 1st experiment by varying the posture (hanging, sitting, or tripedal) and the sensory requirements (tactile or visual). Posture influenced hand bias, with a population-level left-hand bias in hanging and sitting postures, but an almost symmetrical distribution in the tripedal posture. A left-hand bias was found for both sensory modalities, but the bias was stronger in the tactual tasks. Results suggest a possible right-hemisphere specialization in the rhesus for tactile, visual, or spatial processing.     

Contrast of hand preferences between communicative gestures and non-communicative actions in baboons: Implications for the origins of hemispheric specialization for language

Gestural communication is a modality considered in the literature as a candidate for determining the ancestral prerequisites of the emergence of human language. As reported in captive chimpanzees and human children, a study in captive baboons revealed that a communicative gesture elicits stronger degree of right-hand bias than non-communicative actions. It remains unclear if it is the communicative nature of this manual behavior which induces such patterns of handedness. In the present study, we have measured hand use for two uninvestigated behaviors in a group of captive olive baboons: (1) a non-communicative self-touching behavior (“muzzle wipe” serving as a control behavior), (2) another communicative gesture (a ritualized “food beg”) different from the one previously studied in the literature (a species-specific threat gesture, namely “hand slap”) in the same population of baboons. The hand preferences for the “food beg” gestures revealed a trend toward right-handedness and significantly correlated with the hand preferences previously reported in the hand slap gesture within the same baboons. By contrast, the hand preferences for the self-touching behaviors did not reveal any trend of manual bias at a group-level nor correlation with the hand preferences of any communicative gestures. These findings provide additional support to the hypothesized existence in baboons of a specific communicative system involved in the production of communicative gestures that may tend to a left-hemispheric dominance and that may differ from the system involved in purely motor functions. The hypothetical implications of these collective results are discussed within the theoretical framework about the origins of hemispheric specialization for human language.     

Motor inhibition associated with the affordance of briefly displayed objects

Research has demonstrated that left- and right-hand responses are facilitated when they are performed with the hand compatible with the orientation of a viewed object. This suggests that graspable objects automatically activate the motor representations that correspond to their orientation. It has recently been proposed that similar positive stimulus–response compatibility effects (PCE) may turn into negative compatibility effects (NCE) when a prime object is displayed very briefly. These NCEs are suggested to reflect motor inhibition mechanisms—motor activation triggered by briefly viewed objects may be treated by the motor system as unwanted, and thus it is rapidly inhibited. We examined whether the motor activation triggered by the orientation of a task-irrelevant object is similarly inhibited when the object is displayed briefly. In Experiment 1, a NCE was observed between the orientation of an object and the responding hand when the object was displayed for 30 or 70 ms. The effect turned into a PCE when the object was displayed for 370 ms. Experiment 2 confirmed that this motor inhibition effect was produced by the handle affordance of the object rather than some abstract visual properties of the object.     

An action sequence withheld in memory can delay execution of visually guided actions: the generalization of response compatibility interference

Withholding an action plan in memory for later execution can delay execution of another action, if the actions share a similar (compatible) action feature (i.e., response hand). This phenomenon, termed compatibility interference (CI), was found for identity-based actions that do not require visual guidance. The authors examined whether CI can generalize to both identity-based and location-based actions that require visual guidance. Participants withheld a planned action based on the identity of a stimulus and then immediately executed a visually guided action (touch response) to a 2nd stimulus based on its color identity (Experiment 1), its spatial location (Experiment 2), or an intrinsic spatial location within an object (Experiment 3). Results showed CI for both left- and right-hand responses in Experiment 1. However, CI occurred for left- but not right-hand responses in Experiment 2 and 3. This suggests that CI can generalize to visually guided actions under cognitive control but not to actions that invoke automatic visual-control mechanisms where the left hemisphere may play a special role (C. Gonzalez, T. Ganel, & M. Goodale, 2006). The code occupation account for CI (G. Stoet & B. Hommel, 2002) is also discussed.     

Motor inhibition associated with the affordance of briefly displayed objects

Research has demonstrated that left- and right-hand responses are facilitated when they are performed with the hand compatible with the orientation of a viewed object. This suggests that graspable objects automatically activate the motor representations that correspond to their orientation. It has recently been proposed that similar positive stimulus-response compatibility effects (PCE) may turn into negative compatibility effects (NCE) when a prime object is displayed very briefly. These NCEs are suggested to reflect motor inhibition mechanisms--motor activation triggered by briefly viewed objects may be treated by the motor system as unwanted, and thus it is rapidly inhibited. We examined whether the motor activation triggered by the orientation of a task-irrelevant object is similarly inhibited when the object is displayed briefly. In Experiment 1, a NCE was observed between the orientation of an object and the responding hand when the object was displayed for 30 or 70 ms. The effect turned into a PCE when the object was displayed for 370 ms. Experiment 2 confirmed that this motor inhibition effect was produced by the handle affordance of the object rather than some abstract visual properties of the object.     

Haptic tracking permits bimanual independence

This study shows that in a novel task-bimanual haptic tracking-neurologically normal human adults can move their 2 hands independently for extended periods of time with little or no training. Participants lightly touched buttons whose positions were moved either quasi-randomly in the horizontal plane by 1 or 2 human drivers (Experiment 1), in circle and square patterns in the vertical plane by 2 human drivers (Experiment 2), or at different frequencies in the horizontal plane by 2 human drivers (Experiment 3). Bimanual contact was maintained equally well in all conditions even though in Experiment 1 the left- and right-hand motions were uncorrelated (in the 2-driver condition), in Experiment 2 the left- and right-hand motions were spatially incongruous when circles and squares were tracked at the same time, and in Experiment 3 the left- and right-hand motions maintained different frequency ratios. Because haptic tracking has revealed that humans can in fact move their 2 hands independently, it may have potential as a new behavioral tool for revealing other perceptual-motor capabilities.     

Reciprocal recognition of sifaka (<Emphasis Type="Italic">Propithecus verreauxi verreauxi</Emphasis>) and redfronted lemur (<Emphasis Type="Italic">Eulemur fulvus rufus</Emphasis>) alarm calls

Redfronted lemurs (Eulemur fulvus rufus) and Verreaux's sifakas (Propithecus verreauxi verreauxi) occur sympatrically in western Madagascar. Both species exhibit a so-called mixed alarm call system with functionally referential alarm calls for raptors and general alarm calls for carnivores and raptors. General alarm calls also occur in other contexts associated with high arousal, such as inter-group encounters. Field playback experiments were conducted to investigate whether interspecific recognition of alarm calls occurs in both species, even though the two species rarely interact. In a crossed design, redfronted lemur and sifaka alarm calls were broadcast to individuals of both species, using the alarm call of chacma baboons (Papio cynocephalus) as a control. Both species responded with appropriate escape strategies and alarm calls after playbacks of heterospecific aerial alarm calls. Similarly, they reacted appropriately to playbacks of heterospecific general alarm calls. Playbacks of baboon alarm calls elicited no specific responses in either lemur species, indicating that an understanding of interspecific alarm calls caused the responses and not alarm calls in general. Thus, the two lemur species have an understanding of each other's aerial as well as general alarm calls, suggesting that even in species that do not form mutualistic associations and rarely interact, common predator pressure has been sufficient for the development of heterospecific call recognition.     

Lateral preference profiles and right shift attempt histories of consistent and inconsistent left-handers

Differences in abilities and preferences exist between left-handers who both write and throw with their left hands (consistent left-handers) and those who write with their left hand but prefer to throw with their right (inconsistent left-handers). It is also known that many left-handers are pressured to switch to right-hand writing, and that these pressures can lead to a right shift attempt. The present study is the first to explore the joint effects of the consistent/inconsistent left-handedness dichotomy, right shift attempt history, and lateral preference profiles. Testing 379 Canadian adults between the ages of 18 and 94 indicated that, while both types of left-handers were equally likely to experience a right shift attempt, the inconsistent left-handers were more likely to successfully switch to right-hand writing. Further analyses revealed that throwing hand was more associated than writing hand with the direction of sidedness for a lateral preference index based upon eye, foot, and ear preferences. More specifically, right-hand throwers were much more likely to have a rightward lateral preference score than were left-hand throwers, regardless of current preferred writing hand. Overall, the results support an hypothesis that the left-handers who are least likely to submit to rightward switch pressures are those with the strongest, most consistent left-sided lateral preference profile.     

The use of bouts and frequencies in the evaluation of hand preferences for a coordinated bimanual task in chimpanzees (Pan troglodytes): an empirical study comparing two different indices of laterality

Hand preferences for a coordinated bimanual task were assessed in 109 chimpanzees (Pan troglodytes). Hand preference was evaluated for 4 test sessions using bouts and frequencies of hand use to compare the sensitivity of each level of analysis in evaluating individual variation in handedness. Overall, significant population-level right-handedness was found using several different measures of hand use. Handedness indices based on bouts and frequencies were highly and significantly correlated. Moreover, hand preferences were consistent across tests despite efforts to situationally bias preference during each test. Taken together, these data do not support the view that bouts are a better level of analysis for evaluating hand preference. The results further suggest that hand preferences for coordinated bimanual actions are not influenced by situational factors and may reflect an inherent specialization of the left hemisphere for motor skill.     

The ecology of spatial memory in four lemur species

Evolutionary theories suggest that ecology is a major factor shaping cognition in primates. However, there have been few systematic tests of spatial memory abilities involving multiple primate species. Here, we examine spatial memory skills in four strepsirrhine primates that vary in level of frugivory: ruffed lemurs (Varecia sp.), ring-tailed lemurs (Lemur catta), mongoose lemurs (Eulemur mongoz), and Coquerel’s sifakas (Propithecus coquereli). We compare these species across three studies targeting different aspects of spatial memory: recall after a long-delay, learning mechanisms supporting memory and recall of multiple locations in a complex environment. We find that ruffed lemurs, the most frugivorous species, consistently showed more robust spatial memory than the other species across tasks—especially in comparison with sifakas, the most folivorous species. We discuss these results in terms of the importance of considering both ecological and social factors as complementary explanations for the evolution of primate cognitive skills.     

Target animacy influences chimpanzee handedness

We employed a bottom-up, quantitative method to investigate great ape handedness. Our previous investigation of gorillas (Gorilla gorilla gorilla) demonstrated that contextual information influenced an individual’s handedness toward target objects. Specifically, we found a significant right-hand bias for unimanual actions directed toward inanimate target objects but not for actions directed to animate target objects (Forrester et al. in Anim Cogn 14(6):903–907, 2011). Using the identical methodological technique, we investigated the spontaneous hand actions of nine captive chimpanzees (Pan troglodytes) during naturalistic, spontaneous behavior. We assessed both the frequencies and proportions of lateralized hand actions directed toward animate and inanimate targets employing focal follow video sampling. Like the gorillas, the chimpanzees demonstrated a right-handed bias for actions directed toward inanimate targets, but not toward animate targets. This pattern was evident at the group level and for the majority of subjects at the individual level. We postulate that a right-hand bias for only inanimate targets reflects the left hemisphere’s dominant neural processing capabilities for objects that have functional properties (inanimate objects). We further speculate that a population-level right-hand bias is not a human-unique characteristic, but one that was inherited from a common human-ape ancestor.     

Doing two things at once: The role of temporal compatibility

Performance in a periodically repeating keypress response was measured as a function of the relation between the response patterns required of the two hands. Compared to identical left- and right-hand responses, performance was degraded when the temporal periods of the left- and right-hand responses were not harmonically related. By contrast, performance was not degraded compared to the identical task control when the left- and right-hand responses had the same or harmonically related periods. These findings suggest a limitation in parallel generation of multiple time frames that is assumed to be associated with a late stage of central processing in which response commands are generated.     

Maternal cradling bias in baboons: The first environmental factor affecting early infant handedness development?

The most emblematic behavioral manifestation of human brain asymmetries is handedness. While the precise mechanisms behind the development of handedness are still widely debated, empirical evidences highlight that besides genetic factors, environmental factors may play a crucial role. As one of these factors, maternal cradling behavior may play a key role in the emergence of early handedness in the offspring. In the present study we followed 41 Papio anubis infants living in social groups with their mother for which direction (e.g., left- or right-arm) and degree of maternal cradling-side bias were available from a previous published study. We assessed hand preferences for an unimanual grasping task at three developmental stages: (A) 0–4, (B) 4—6, and (C) 9–10 months of age. We found that individual hand preferences for grasping exist as soon as the first months of age, with a population-level left-handedness predominance, being stable until 6 months; to wit the period during which juveniles are mainly carried by their mothers. More importantly, this early postnatal handedness is positively correlated with maternal cradling lateralization. Interestingly, hand preferences assessed later in the development, once juveniles are no longer carried (i.e., from 9 to 10 months of age), are less dependent from the maternal cradling bias and less consistent with the earlier developmental stages, especially in infants initially cradled on the right maternal side. Our findings suggest that the ontogenetic dynamics of the infant's hand preference and its changes might ultimately rely on the degree of infant dependence from the mother across development.     

The effect of unilateral hand contractions on psychophysiological activity during motor performance: Evidence of verbal-analytical engagement

ObjectivesConscious engagement in movement control can influence motor performance. In most cases, the left hemisphere of the brain plays an important role in verbal-analytical processing and reasoning, so changes in the balance of hemispheric activation may influence conscious engagement in movement. Evidence suggests that unilateral hand contractions influence hemispheric activation, but no study has investigated whether there is an associated effect of hand contractions on verbal-analytical processing during motor performance. This study utilized psychophysiological (and behavioural) measures to examine whether pre-performance unilateral hand contraction protocols change verbal-analytical engagement during motor performance.DesignA repeated measures crossover design was employed.MethodsTwenty-eight participants completed three hand contraction protocols in a randomised order: left-, right- and no-hand contractions. Electroencephalography (EEG) measures of hemispheric asymmetry were computed during hand contractions. A golf putting task was conducted after each protocol. EEG connectivity between sites overlying the left verbal-analytical temporal region (T7) and the motor planning region (Fz) was computed for the 3 sec prior to movement initiation. Additionally, electrocardiography (ECG) and electromyography (EMG) signals were analysed 6 sec prior to movement initiation until 6 sec after. Golf putting performance (distance from the target) and putter swing kinematics were measured.ResultsContralateral hemisphere activity was revealed for the left-hand and right-hand contraction conditions. During motor planning, the left-hand contraction protocol led to significantly lower T7-Fz connectivity, and the right-hand contraction protocol led to significantly higher T7-Fz connectivity than the other conditions. EMG, ECG and kinematic measures did not differ as a function of condition. Importantly, T7-Fz connectivity mediated the relationship between hand squeezing and motor performance (distance from the target).ConclusionThe EEG results suggest that pre-performance unilateral hand contractions influence the extent of verbal-analytical engagement during motor planning, which in turn influences motor performance. However, the hand contractions did not influence cardiac activity, muscle activity or kinematics.     

Do Children Perceive Postural Constraints When Estimating Reach or Action Planning?

Estimation of whether an object is reachable from a specific body position constitutes an important aspect in effective motor planning. Researchers who estimate reachability by way of motor imagery with adults consistently report the tendency to overestimate, with some evidence of a postural effect (postural stability hypothesis). This idea suggests that perceived reaching limits depend on an individual's perceived postural constraints. Based on previous work with adults, the authors expected a significant postural effect with the Reach 2 condition, as evidenced by reduced overestimation. Furthermore, the authors hypothesized that the postural effect would be greater in younger children. They then tested these propositions among children aged 7, 9, and 11 years by asking them to estimate reach while seated (Reach 1) and in the more demanding posture of standing on 1 foot and leaning forward (Reach 2). Results indicated no age or condition difference, therefore providing no support for a postural effect. When the authors compared these data to a published report of adults, a developmental difference emerged. That is, adults recognize the perceived postural constraint of the standing position resulting in under- rather than overestimation, as displayed in the seated condition. Although preliminary, these observations suggest that estimates of reach (action planning) continue to be refined between late childhood and young adulthood.     

Chimpanzee (Pan troglodytes) handedness: variability across multiple measures of hand use

This study examined intertask consistency in handedness across multiple measures of hand use in a sample of 187 chimpanzees (Pan troglodytes). Hand preferences for 2 to 6 measures were collected from the sample, and hand preference scores were derived on the basis of the individual hand preferences for each measure. Seven of 15 possible intratask correlations were significant, with some degree of clustering depending on the motor demands of the tasks. Two overall measures of handedness revealed population-level right-handedness in the chimpanzees, although the degree of bias was reduced for chimpanzees tested on more than 3 measures of hand use. The results are interpreted in the context of several recent studies that proposed theoretical models of handedness in nonhuman primates.