The developmental origins of bimanual coordination: A dynamic perspective.

Patterns of interlimb coordination associated with infant reaching fluctuate frequently over developmental time. This study investigated whether these fluctuations are related to coordination tendencies. Interlimb patterns were studied in reaching and nonreaching movements in 4 infants, which were followed through their 1st year. Each week, reaching and nonreaching endpoint kinematics were recorded in both arms during multiple 14-s trials. It was found that patterns of interlimb coordination in reaching matched coordination tendencies in nonreaching. Reaching fluctuated between uni- and bimanual periods. During the bimanual periods, nonreaching interlimb activity tended to be synchronous. During the unimanual periods, nonreaching activity revealed no predominant form of interlimb coordination. It is argued that changing coordination tendencies may influence the organization of specific goal-oriented behaviors from early in life. (PsycINFO Database Record (c) 2011 APA, all rights reserved)     

Distinguishing between the effects of frequency and amplitude on interlimb coupling in tapping a 2:3 polyrhythm

Rhythmic interlimb coordination is characterized by attraction to stable phase and frequency relations. Sudden, unintended transitions between such coordination patterns have been observed in iso- and multifrequency tasks when movement frequency was gradually increased. These transitions have been accounted for by modeling the two limbs as nonlinearly coupled oscillators. The prevailing form of the coupling function is based on time derivatives, but an alternative formulation can be derived by incorporating time delays. These time delays may be related to the neurophysiological delays associated with the use of kinesthetic afferences. The two ways of deriving coupling functions for interlimb coordination allow for different predictions with respect to the effects of movement frequency and amplitude on the strength of interaction between the limbs. In the current experiment, the effects of amplitude and frequency were dissociated experimentally, so as to arrive at an empirically motivated choice between the two ways of formalizing interlimb coupling. Subjects tapped the polyrhythm 2:3 at five different frequencies under three amplitude conditions. Whereas no effects of amplitude were observed, the strength of interaction between the hands decreased with increasing movement frequency. These results support the time-delay version of the model, in which differential (loss of) stability of coordination modes results from differential dependence on movement amplitude, but overall coupling strength is related reciprocally to movement frequency squared. This version of the model was related tentatively to three proposed aspects of interlimb coordination: (1) neurophysiological delays associated with the use of kinesthetic afferences; (2) rate-dependent decrease in pattern stability; and (3) differential entrainment influences of kinesthetic signals.     

Acquiring bimanual skills: Contrasting forms of information feedback for interlimb decoupling.

Addressed the learner's capability to perform different upper-limb actions simultaneously with the help of various sources of information feedback. An elbow flexion movement was made in the left limb together with a flexion-extension-flexion movement in the right limb. Interlimb interactions were assessed at the structural as well as the metrical level of movement specification during acquisition and retention. Despite a strong initial tendency for the limbs to be synchronized, findings revealed that Ss became gradually more successful in interlimb decoupling as a result of practice with augmented feedback. However, detailed knowledge of movement kinematics was no more effective than global outcome information for interlimb decoupling, indicating that knowledge of results may have more potential for acquiring multiple degree-of-freedom tasks than previously believed. Finally, the data support the general notion that learning new coordination tasks involves the suppression of preexisting preferred coordination tendencies, which is often a prerequisite for building new coordination modes. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Sensorimotor state of the contralateral leg affects ipsilateral muscle coordination of pedaling

The objective of this study was to determine if independent central pattern generating elements controlling the legs in bipedal and unipedal locomotion is a viable theory for locomotor propulsion in humans. Coordinative coupling of the limbs could then be accomplished through mechanical interactions and ipsilateral feedback control rather than through central interlimb neural pathways. Pedaling was chosen as the locomotor task to study because interlimb mechanics can be significantly altered, as pedaling can be executed with the use of either one leg or two legs (cf. walking) and because the load on the limb can be well-controlled. Subjects pedaled a modified bicycle ergometer in a two-legged (bilateral) and a one-legged (unilateral) pedaling condition. The loading on the leg during unilateral pedaling was designed to be identical to the loading experienced by the leg during bilateral pedaling. This loading was achieved by having a trained human "motor" pedal along with the subject and exert on the opposite crank the torque that the subject's contralateral leg generated in bilateral pedaling. The human "motor" was successful at reproducing each subject's one-leg crank torque. The shape of the motor's torque trajectory was similar to that of subjects, and the amount of work done during extension and flexion was not significantly different. Thus the same muscle coordination pattern would allow subjects to pedal successfully in both the bilateral and unilateral conditions, and the afferent signals from the pedaling leg could be the same for both conditions. Although the overall work done by each leg did not change, an 86% decrease in retarding (negative) crank torque during limb flexion was measured in all 11 subjects during the unilateral condition. This corresponded to an increase in integrated electromyography of tibialis anterior (70%), rectus femoris (43%), and biceps femoris (59%) during flexion. Even given visual torque feedback in the unilateral condition, subjects still showed a 33% decrease in negative torque during flexion. These results are consistent with the existence of an inhibitory pathway from elements controlling extension onto contralateral flexion elements, with the pathway operating during two-legged pedaling but not during one-legged pedaling, in which case flexor activity increases. However, this centrally mediated coupling can be overcome with practice, as the human "motor" was able to effectively match the bilateral crank torque after a longer practice regimen. We conclude that the sensorimotor control of a unipedal task is affected by interlimb neural pathways. Thus a task performed unilaterally is not performed with the same muscle coordination utilized in a bipedal condition, even if such coordination would be equally effective in the execution of the unilateral task.     

A comparison of intra- and interpersonal interlimb coordination: coordination breakdowns and coupling strength

Intra- and interpersonal interlimb coordination of pendulums swung from the wrist was investigated. For both kinds of coordination, the steady state and breakdown of bimanual rhythmic coordination as indexed by the time series of the relative phase angle phi were studied under the manipulation of coordination mode, frequency of oscillation, and the difference in the eigenfrequencies (preferred tempos) of the individual oscillating limbs. The properties observed for both intra- and interpersonal coordination were those predicted by a dynamical model of rhythmic coordination that considers the coordinated limbs coupled to be nonlinear oscillators. Using a regression method, the coupling strengths of the coupled system were recovered. As predicted by the dynamical model, the strength of the dynamic was generally greater for the in-phase than the anti-phase mode and decreased with increasing frequency. Further, the strength of the interpersonal interlimb coupling was weaker than that of intrapersonal interlimb coupling.     

The MHC class I genes of the rhesus monkey. Different evolutionary histories of MHC class I and II genes in primates

Homologues of the human HLA-A and -B MHC class I loci have been found in great apes and Old World primates suggesting that these two loci have existed for at least 30 million years. The C locus, however, shows some sequence similarity to the B locus and has been found only in gorillas, chimpanzees, and humans. To determine the age of the MHC class I C locus and to examine the evolution of the A and B loci we have cloned, sequenced, and in vitro translated 16 MHC class I cDNAs from two unrelated rhesus monkeys (Macaca mulatta) using both cDNA library screening and PCR amplification. Analyses of these sequences suggest that the C locus is not present in the rhesus monkey, indicating that this locus may be of recent origin in gorillas, chimpanzees, and humans. The rhesus monkey's complement of MHC class I genes includes the products of at least one expressed A locus and at least two expressed B loci, indicating that a duplication of the B locus has taken place in the lineage leading to these Old World primates. Comparison of rhesus monkey MHC class I cDNAs to their primate counterparts reveals fundamental differences between MHC class I and class II evolution in primates. Although MHC class II allelic lineages are shared between humans and Old World primates, no such trans-species sharing of allelic lineages is seen at the MHC class I loci.     

Dissociation of muscular and spatial constraints on patterns of interlimb coordination.

Interlimb coordination is subject to constraints. One major constraint has been described as a tendency for homologous muscle groups to be activated simultaneously. Another has been described as a biasing of limb segments to movement in the same direction. In 2 experiments, the 2 constraints were placed in opposition: In-phase or antiphase contraction of homologous muscles of contralateral limbs produced movement that was spatially antiphase or in-phase, respectively. Probability distributions of relative phase were obtained under manipulations of phase detuning and movement speed. They revealed that the equilibrium and stability of coordination were related, respectively, to spatial relative phase and muscular relative phase. Previously observed spatial and muscular constraints reflect a (possibly very general) factorization of attractor location and attractor strength in the dynamics of interlimb coordination. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Spinal cord coordination of hindlimb movements in the turtle: intralimb temporal relationships during scratching and swimming

Hindlimb interlimb coordination was examined in turtles during symmetrical "same-form" behaviors in which both hindlimbs utilized the same movement strategy ("form") and during asymmetric "mixed-form" behaviors in which the form exhibited by one hindlimb differed from that of its contralateral partner. In spinal turtles, three forms of scratching were examined: rostral, pocket, and caudal. Bilateral symmetrical same-form scratching was studied for each of the forms. Asymmetric mixed-form scratching (rostral scratching of a hindlimb and pocket scratching of the other hindlimb) was also examined. In intact turtles, two forms of swimming were examined: forward swimming and back-paddling. The symmetrical behavior of bilateral forward same-form swimming and the asymmetric behavior of turning mixed-form swimming (forward swimming of 1 hindlimb and back-paddling of the other hindlimb) were studied. For all behaviors examined, most episodes displayed absolute or 1:1 coordination; in this type of coordination, during each movement cycle that began and ended with the onset of ipsilateral hip flexion, there was a single onset of contralateral hip flexion. For most of these episodes there was out-of-phase coordination between hip movements; the onset of contralateral hip flexion occurred near the onset of ipsilateral hip extension midway through the ipsilateral movement cycle. Bilateral caudal/caudal same-form scratching displayed out-of-phase 1:1 coordination during some episodes and in-phase 1:1 coordination during other episodes. During in-phase coordination, the onset of contralateral hip flexion occurred near the onset of ipsilateral hip flexion close to the start of the ipsilateral movement cycle. In a few cases of bilateral same-form scratching there were episodes of relative or 2:1 coordination; in this type of coordination, during each movement cycle of the slowly moving limb that began and ended with ipsilateral hip flexion, there were two distinct occurrences of the onset of contralateral hip flexion. The observation that out-of-phase movements of the hip occurred during symmetrical as well as asymmetric behaviors is consistent with the hypothesis that timing signals related to hip movement play a major role in interlimb phase control. The neural mechanisms responsible for interlimb phase control are not well understood in vertebrates. The present demonstration of bilateral scratching in spinal turtles suggests that this preparation may be suitable for additional experiments to examine mechanisms of vertebrate interlimb phase control.     

Early walking in the neonatal rat: a kinematic study

The development of the early stage of locomotion (between Postnatal Days 3 and 10) was studied in newborn rats. At this age, rats are known to perform limited locomotor activities, consisting of an inefficient nonpostural gait termed crawling. By providing appropriate olfactory stimulation, it was possible to override the pups' reluctance to walk and to discover their actual locomotor abilities. The step period decreased from 1,200 ms to 900 ms from Postnatal Days 4 to 9, showing both a regular decrease in the swing and a discontinuous decrease in the stance phase. The fore- and hindlimb periods stabilized early on an alternate pattern of coupling. The ipsilateral coupling shifted progressively from 220 degrees to 260 degrees in relation with the change in the gait pattern. In parallel with the change in timing, the newborn rats showed gradual changes in the foot position and in the interlimb spatial coordination. These results show that quadruped locomotion develops before postural control is acquired, in a continuous process as the nervous system develops.     

Videos of conspecifics elicit interactive looking patterns and facial expressions in monkeys.

A broader understanding of the neural basis of social behavior in primates requires the use of species-specific stimuli that elicit spontaneous, but reproducible and tractable behaviors. In this context of natural behaviors, individual variation can further inform about the factors that influence social interactions. To approximate natural social interactions similar to those documented by field studies, we used unedited video footage to induce in viewer monkeys spontaneous facial expressions and looking patterns in the laboratory setting. Three adult male monkeys (Macaca mulatta), previously behaviorally and genetically (5-HTTLPR) characterized, were monitored while they watched 10 s video segments depicting unfamiliar monkeys (movie monkeys) displaying affiliative, neutral, and aggressive behaviors. The gaze and head orientation of the movie monkeys alternated between “averted” and “directed” at the viewer. The viewers were not reinforced for watching the movies, thus their looking patterns indicated their interest and social engagement with the stimuli. The behavior of the movie monkey accounted for differences in the looking patterns and facial expressions displayed by the viewers. We also found multiple significant differences in the behavior of the viewers that correlated with their interest in these stimuli. These socially relevant dynamic stimuli elicited spontaneous social behaviors, such as eye-contact induced reciprocation of facial expression, gaze aversion, and gaze following, that were previously not observed in response to static images. This approach opens a unique opportunity to understanding the mechanisms that trigger spontaneous social behaviors in humans and nonhuman primates. (PsycINFO Database Record (c) 2011 APA, all rights reserved)     

Russell Lee De Valois: Distinguished Scientific Contribution Awards for 1977.

Russell Lee De Valois received a Distinguished Scientific Contribution Award for pioneering studies of color and pattern discrimination in primates. He discovered individual cells in the visual pathways that respond oppositely when a monkey sees red versus green, or blue versus yellow. He also found nonopponent cells and explored the receptive fields of each type. Furthermore, he showed that simple cortical cells are selectively activated by grating patterns of particular spatial frequencies. These studies, together with equally imaginative psychophysical measurements, have revealed the near identity of monkey and human visual systems. He has thus established a firm neural foundation for current theories of color and pattern perception. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Kinematics of locomotion by cats with a single hindlimb deafferented

1. Cinematographic measurements were made of stepping by cats on a motor-driven treadmill, both normally and 2-3 wk after deafferentation of the LH (left hind) limb. 2. After surgery, rhythmic cycling of the LH limb was blurred whether the leg was dragged, as by some cats, or if it was lifted from the surface, as by others. 3. Interlimb coordination was also blurred with respect to normal, although distinct rhythms were still seen. The RH (right hind) limb descended prematurely and, in the walk, had a prolonged stance phase. The interval between touchdowns of hind- and forelimb on the left side no longer equaled that interval on the right side. 4. As is true for a normal cat, if the LH-deafferented animal stumbled, relatively normal single and interlimb cyclings were regained after several strides. 5. By kinematic analysis, force deficits were found in the deafferented LH limb both during the stance, when extensors should be most active, and the swing, when the limb failed to attain a normal position above the surface of the belt. Weight bearing by the LF (left fore) limb was altered in some animals. 6. At high speed, mean LH stance duration failed to decrease in the normal fashion. Inter-limb timings were reset to greater extent than in low-speed walking, as if the LH limb was being used only minimally. 7. It was concluded that both rhythm and force were impaired in the deafferented limb and also in the three intact limbs, whose weight bearing had to compensate for LH weakness. The changed mechanical demands after surgery were probably met by interactions between the remaining afferent input and central pattern generators so as to secure fairly effective and expedient locomotion.     

The dynamics of bimanual circle drawing

A bimanual circle drawing task was employed to elucidate the dynamics of intralimb and interlimb coordination. Right-handed subjects were required to produce circles with both hands in either a symmetrical (mirror) mode (i.e. one hand moving clockwise, the other counter-clockwise) or in an asymmetrical mode (i.e. both hands moving clockwise or counter-clockwise). The frequency of movement was scaled by an auditory metronome from 1.50 Hz to 3.25 Hz in 8 (8-sec) steps. In the asymmetrical mode, distortions of the movement trajectories, transient departures from the target pattern of coordination, and phase wandering were evidence as movement frequency was increased. These features suggested loss of stability. Deviations from circular trajectories were most prominent for movements of the left hand. Transient departures from the required mode of coordination were also largely precipitated by the left hand. The results are discussed with reference to manual asymmetries and mechanisms of interlimb and intersegmental coordination.     

Sex differences in adult chimpanzee positional behavior: the influence of body size on locomotion and posture

Focal animal instantaneous sampling of adult male and female chimpanzee positional behavior was conducted during a 7-month study in the Tai Forest, Ivory Coast, in order to determine whether there are sex differences in the locomotion, posture, substrate use, and height preference of sexually dimorphic adult chimpanzees, and if so, whether these differences support predictions based on body size differences. Results indicate that as predicted, adult male and female chimpanzees differ in their arboreal locomotor behavior, with the larger males using less quadrupedalism and more climbing, scrambling, and aided bipedalism than females during feeding locomotion. There is a sex difference in height preference as well, with female chimpanzees consistently using more arboreal behavior than males, primarily during resting. Although it has been previously demonstrated that separate primate species of differing body size differ in locomotor and postural activities (Fleagle and Mittermeier, 1980; Crompton, 1984), this study clearly demonstrates that body size differences within a species can also be correlated with differences in locomotor behavior. These findings may influence how we interpret sex differences in body size of extinct species.     

The biomechanics of skipping gaits: a third locomotion paradigm?

Skipping, a gait children display when they are about four- to five-years-old, is revealed to be more than a behavioural peculiarity. By means of metabolic and biomechanical measurements at several speeds, the relevance of skipping is shown to extend from links between bipedal and quadrupedal locomotion (namely galloping) to understanding why it could be a gait of choice in low-gravity conditions, and to some aspects of locomotion evolution (ground reaction forces of skipping seem to originate from pushing the walking gait to unnaturally high speeds). When the time-courses of mechanical energy and the horizontal ground reaction force are considered, a different locomotion paradigm emerges, enabling us to separate, among the bouncing gaits, the trot from the gallop (quadrupeds) and running from skipping (bipeds). The simultaneous use of pendulum-like and elastic mechanisms in skipping gaits, as shown by the energy curve analysis, helps us to understand the low cost of transport of galloping quadrupeds.     

Disentangling the effects of attentional and amplitude asymmetries on relative phase dynamics.

Attentional asymmetry in rhythmic interlimb coordination induces an asymmetry in relative phase dynamics, allegedly reflecting an asymmetry in coupling strength. However, relative phase asymmetries may also be engendered by an attention-induced difference between the amplitudes (and hence the preferred frequencies) of the limb movements. The authors conducted 3 experiments to dissociate those (not mutually exclusive) potential effects. Controlled manipulations of amplitude disparity and attentional focus, both alone and combined, revealed that variations in amplitude disparity had the expected effects, but produced evidence against the currently prevailing interpretation that attentional asymmetry affects the relative phase dynamics through an asymmetry in coupling strength. Implications of these findings are discussed vis-à-vis recent empirical findings and extant dynamical models. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Reciprocal chromosome painting between human and prosimians (Eulemur macaco macaco and E. fulvus mayottensis)

We used fluorescence in situ hybridisation to delineate the homology between the human karyotype and those of two lemur species (Eulemur macaco macaco and E. fulvus mayottensis). Human and lemur chromosome-specific probes were established by bivariate fluorescence-activated flow sorting (FACS) and subsequent degenerate oligonucleotide-primed PCR (DOP-PCR). Reciprocal painting of human probes to lemur chromosomes and vice versa allowed a detailed analysis of the interchromosomal rearrangements that had occurred during the evolution of these species. The results indicate that the genomes of both species have undergone only a few translocations during more that 45 million years of lemur and human evolution. The synteny of homologs to human chromosomes 3, 9, 11, 13, 14, 17, 18, 20, 21, X, and Y was found to be conserved in the two lemur species. Taking non-primate mammals as the outgroup for primates, ancestral conditions for various primate chromosomes were identified and distinguished from derived forms. Lemur chromosome painting probes were also used for cross-species hybridization between the two lemur species. The results support an earlier assumption, made on the basis of chromosome banding, that the karyotypes of the two species have evolved exclusively by Robertsonian transformations. All probes derived from E. f. mayottensis chromosomes specific for homologs involved in rearrangements in E. m. macaco exclusively painted entire chromosome arms. The results further indicate that E. f. mayottensis most probably has a more ancestral karyotype than E. m. macaco. Probes derived from prosimians will be useful in comparing the karyotypes of other lower primates, which will improve our understanding of early primate genome evolution.     

Posture and support use of Old World monkeys (Cercopithecidae): the influence of foraging strategies, activity patterns, and the spatial distribution of preferred food items

A common objective in field studies of positional behavior is to establish functional links between locomotion, body size, habitat use, foraging strategies, and maintenance activities. In contrast, there has been relatively little effort to examine posture in a similar, comparative context. Although various studies have shown that particular postures are employed in specific contexts, the theory which could provide the basis for understanding posture on a more general level has not been explicitly stated. This is particularly true for primates lacking specializations such as prehensile tails, claws for clinging, or adaptations for forelimb suspension. Consequently, there are few a priori reasons for predicting postural differences among generalized arboreal quadrupeds. Six sympatric cercopithecid monkeys were studied for 14 months in the Ivory Coast's Tai Forest to determine if more general relationships do exist between posture and other aspects of behavior. The results demonstrate that the postural diversity with these primates can, to varying degrees, be understood within the context of differences in the spatial distribution of preferred food items, activity patterns, support use, and foraging strategies.     

Intersegmental coordination of limb movements during locomotion: mathematical models predict circuits that drive swimmeret beating

Normal locomotion in arthropods and vertebrates is a complex behavior, and the neural mechanisms that coordinate their limbs during locomotion at different speeds are unknown. The neural modules that drive cyclic movements of swimmerets respond to changes in excitation by changing the period of the motor pattern. As period changes, however, both intersegmental phase differences and the relative durations of bursts of impulses in different sets of motor neurons are preserved. To investigate these phenomena, we constructed a cellular model of the local pattern-generating circuit that drives each swimmeret. We then constructed alternative intersegmental circuits that might coordinate these local circuits. The structures of both the model of the local circuit and the alternative models of the coordinating circuit were based on and constrained by previous experimental results on pattern-generating neurons and coordinating interneurons. To evaluate the relative merits of these alternatives, we compared their dynamics with the performance of the real circuit when the level of excitation was changed. Many of the alternative coordinating circuits failed. One coordinating circuit, however, did effectively match the performance of the real system as period changed from 1 to 3.2 Hz. With this coordinating circuit, both the intersegmental phase differences and the relative durations of activity within each of the local modules fell within the ranges characteristic of the normal motor pattern and did not change significantly as period changed. These results predict a mechanism of coordination and a pattern of intersegmental connections in the CNS that is amenable to experimental test.     

Gaze following and joint attention in rhesus monkeys (Macaca mulatta).

Gaze and attention direction provide important sources of social information for primates. Behavioral studies show that chimpanzees spontaneously follow human gaze direction. By contrast, non-ape species such as macaques fail to follow gaze cues. The authors investigated the reactions of rhesus macaques (Macaca mulatta) to attention cues of conspecifics. Two subjects were presented with videotaped images of a stimulus monkey with its attention directed to 1 of 2 identical objects. Analysis of eye movements revealed that both subjects inspected the target (object or position attended by the stimulus monkey) more often than the distractor (nonattended object or position). These results provide evidence that rhesus monkeys follow gaze and use the attention cues of other monkeys to orient their own attention to objects. (PsycINFO Database Record (c) 2010 APA, all rights reserved)