Recovery of Locomotion in Monkeys with Spinal Cord Lesions

This study reanalyzes kinematically (via film) the pre- and postoperative locomotor behavior of 4 of the 10 monkeys with partial spinal cord lesions (T8) briefly described by Eidelberg, Walden, and Nguyen (1981). The behavior of the remaining 6 monkeys is qualitatively described. The analysis reveals that 5 of the animals initially exhibited unilateral hind limb stepping. Hind and forelimb cycle durations often differed postoperatively; the hind limbs commonly showed increased values, whereas fore-limb cycle durations were reduced. Ipsilateral interlimb phase values were usually inconsistent.

A review of prior studies of primate spinal cord lesions indicates that sparing of the ventrolateral quadrant may not be essential for locomotor recovery (cf. Eidelberg, Walden, and Nguyen, 1981). Furthermore, this review as well as the kinematic analysis indicates that primates with very significant spinal lesions can still exhibit locomotor movements. Thus, although the primate's spinal cord seems less able than other mammals' to readily organize locomotor movements (Eidelberg, Walden, & Nguyen, 1981), the total absence of stepping in primates with completely transected cords is unexpected and warrants further research.     

An analysis of air-stepping in normal infant vervet monkeys

Limb movements during air-stepping were analyzed in three neonatal vervet monkeys over a three-week period. The movements had similar temporal organization both across animals and across time. For example, the duration of both the hind and the forelimb cycle equaled about 500 ms, with hind limb return strokes lasting much longer than the hind limb power strokes. Furthermore, there were clear indications of both intra- and interlimb coordination. Specifically, all the joints of a limb tended to flex and extend simultaneously, and contralateral and ipsilateral limb pairs had an average phase relationship of approximately 50% of cycle duration. Despite a qualitative similarity between limb movements during air-stepping in the neonates and overground locomotion in older animals, there were notable differences both in temporal relationships and joint displacement patterns. Finally, there appeared to be important similarities between air-stepping in these monkeys and stepping in newborn humans. Most notably, both tended to disappear after a limited period. The implications of these similarities, as well as the overall results, are discussed in relation to the understanding of the development of locomotor behavior in human and nonhuman primates, using approaches based both upon the hard-wired and dynamic models.     

An Analysis of Air-Stepping in Normal Infant Vervet Monkeys

Limb movements during air-stepping were analyzed in three neonatal vervet monkeys over a three-week period. The movements had similar temporal organization both across animals and across time. For example, the duration of both the hind and the forelimb cycle equaled about 500 ms, with the hind limb return strokes lasting much longer than the hind limb power strokes. Furthermore, there were clear indications of both intra- and interlimb coordination. Specifically, all the joints of a limb tended to flex and extend simultaneously, and contralateral and ipsilateral limb pairs had an average phase relationship of approximately 50% of cycle duration. Despite a qualitative similarity between limb movements during air-stepping in the neonates and overground locomotion in older animals, there were notable differences both in temporal relationships and joint displacement patterns. Finally, there appeared to be important similarities between air-stepping in these monkeys and stepping in newborn humans. Most notably, both tended to disappear after a limited period. The implications of these similarities, as well as the overall results, are discussed in relation to the understanding of the development of locomotor behavior in human and nonhuman primates, using approaches based both upon the hard-wired and dynamic models.     

Bilateral coordination in human infants: stepping on a split-belt treadmill

A motorized treadmill often elicits locomotor-like alternate stepping in 7-month-old infants who normally perform few, if any, stepping movements. The step cycle duration is a function of the speed of the treadmill. When infants were held so that each leg was on a separate treadmill belt, each of which was driven at a different speed, the overall cycle duration was intermediate between the cycle durations at the fast or slow speeds alone. Infants shortened the stance on the slow belt and increased the stance on the fast belt to maintain regularly alternating steps. Even before voluntary locomotion, both legs acted in a cooperative manner, with the dynamic status of one limb affecting the timespace behavior of the opposite limb.     

Human lumbar cord circuitries can be activated by extrinsic tonic input to generate locomotor-like activity

We have demonstrated that non-patterned electrical stimulation of the lumbar cord can induce stepping-like activity in the lower limbs of complete spinal cord injured individuals. This result suggested the existence of a human lumbar locomotor pattern generator, which can convert a tonic input to a rhythmic motor output. We have studied the human lumbar cord in isolation from supraspinal input but under extrinsic tonic input delivered by spinal cord stimulation. Large-diameter afferents within the posterior roots are directly depolarized by the electrical stimulation. These afferents project to motoneurons as well as to lumbar interneurons involved in the motor control of lower limbs. Stimulation at 25-50 Hz can elicit rhythmic alternating flexion/extension movements of the lower limbs in supine individuals. Reducing the tonic input frequency to 5-15 Hz initiates lower limb extension. Epidural stimulation applied during manually assisted treadmill stepping in complete spinal cord injured persons immediately increases the central state of excitability of lumbar cord networks and enhances stepping-like functional motor outputs. Sustained, non-patterned tonic input via the posterior roots can activate human lumbar cord networks. Pattern generating configurations of these multifunctional circuitries can be set-up depending on the stimulation parameters and particularly on the input frequency.     

Behavior of larval and juvenile bullfrogs (Rana catesbeiana) following chronic spinal transection

The behavior of larval and juvenile bullfrogs (Rana catesbeiana) was examined for 32 days following cervical spinal transection. The threshold for cutaneously elicited hindlimb withdrawal was not changed at either stage of development but righting reflexes were abolished. Forelimb postural support of juveniles was abolished by the transection but recovered within 3 days. Hindlimb posture was normal and hopping could be elicited by stimulation of the rump with a blunt wire probe. Undulatory swimming of larvae was abolished by the transection but began to recover approximately 1 week later. The hindlimbs of larvae were very active following the transection and displayed long sequences of coordinated stepping in response to a variety of stimuli. Gross examination of the spinal cord in situ after 32 days suggested that fibers may have grown across the transection site. Retransection at the site of the original transection on Postoperative Day 33 had no discernable effect on the behavior juveniles or on the stepping of larvae, but it abolished recovered swimming of larvae. Deafferentation of lumbar segments of larvae eliminated stepping but had no effect on swimming. Deafferentation of cervical segments eliminated forelimb support in juveniles. These results suggest that recovery of larval swimming depends at least in part upon the growth of fibers across the transection site. Stepping of spinal larvae appears to be mediated by proprioceptive reflexes rather than by central pattern generators, and in the normal animal is probably under the control of descending inhibition. Recovery of posture and hopping in juveniles was much more rapid than that described for adult frogs and does not depend on growth across the transection site.     

Effects of repetitive motor training on movement representations in adult squirrel monkeys: role of use versus learning

Current evidence indicates that repetitive motor behavior during motor learning paradigms can produce changes in representational organization in motor cortex. In a previous study, we trained adult squirrel monkeys on a repetitive motor task that required the retrieval of food pellets from a small-diameter well. It was found that training produced consistent task-related changes in movement representations in primary motor cortex (M1) in conjunction with the acquisition of a new motor skill. In the present study, we trained adult squirrel monkeys on a similar motor task that required pellet retrievals from a much larger diameter well. This large-well retrieval task was designed to produce repetitive use of a limited set of distal forelimb movements in the absence of motor skill acquisition. Motor activity levels, estimated by the total number of finger flexions performed during training, were matched between the two training groups. This experiment was intended to evaluate whether simple, repetitive motor activity alone is sufficient to produce representational plasticity in cortical motor maps. Detailed analysis of the motor behavior of the monkeys indicates that their retrieval behavior was highly successful and stereotypical throughout the training period, suggesting that no new motor skills were learned during the performance of the large-well retrieval task. Comparisons between pretraining and posttraining maps of M1 movement representations revealed no task-related changes in the cortical area devoted to individual distal forelimb movement representations. We conclude that repetitive motor activity alone does not produce functional reorganization of cortical maps. Instead, we propose that motor skill acquisition, or motor learning, is a prerequisite factor in driving representational plasticity in M1.     

Androgens and aggressive behavior in primates: A review

This review deals with possible central and peripheral effects of androgens upon primate aggressive behavior. One problem that clouds interpretation of experimental work is that measurements of dominance have often been employed, such as competition tests for food and water. Such measures often do not correlate with those obtained by quantifying aggressive interactions. It should be remembered that very few of the 188 primate species have been studied experimentally and that great behavioral and physiological diversity occurs within the order. Therefore, generalizations about the effects of androgens upon aggressive behavior in primates (including man) should be made with caution. Testosterone has an organizing influence upon the foetal brain of rhesus monkeys and may affect the development of neural mechanisms which govern aggression in males. More data are required on primates, however, since rhesus monkeys show some important differences from rodents as regards the effects of androgen upon sexual differentiation of the hypothalamus. In future, marmosets may provide a suitable model for such studies, because there is evidence that sexual differentiation of brain by androgen occurs postnatally in these monkeys. At puberty, male primates show a variety of behavioral changes and, during adulthood, males of seasonally breeding species may be more aggressive during the mating season, when testosterone levels are maximal. This does not indicate a causative relationship between testosterone and aggressive responses, because castration and androgen treatments have little effect upon aggression in prepubertal or adult males of several primate species. Androgens have pronounced effects on sexual responses in adult male monkeys, but their central effects upon aggression are much less important than among rodents. Elec trical stimulation of hypothalamic pathways has been employed to evoke aggressive behavior in marmosets and rhesus monkeys. In the rhesus, preliminary evidence indicates that such pathways show some sensitivity to androgens. In rodents it is known that these areas are richly supplied with monoaminergic neurons, which play an important role in aggressive behavior. There is little evidence on primates, however, and this remains a crucial topic for future research. Peripheral effects of androgens should also be considered. Many prosimians and New World monkeys use scent-marking behaviors and, in males, androgen-dependent chemical cues may be involved in sexual recognition and territorial behavior. This possibility awaits investigation. Finally, plasma testosterone levels may alter as a function of aggression itself; thus levels decrease if male rhesus monkeys are defeated by conspecifics. This might occur because neural events associated with giving (or receiving) aggression also influence pituitary function and hence alter gonadal testosterone secretion. Theoretically, it is possible that such changes in circulating testosterone might affect aggressive behavior via a feedback action on the brain, but the experimental evidence does not support such a view.     

Grasp-Based Functional Coupling Between Reach- and Grasp-Related Components of Forelimb Muscle Activity

How are appropriate combinations of forelimb muscles selected during reach-to-grasp movements in the presence of neuromotor redundancy and important task-related constraints? The authors tested whether grasp type or target location preferentially influence the selection and synergistic coupling between forelimb muscles during reach-to-grasp movements. Factor analysis applied to 14–20 forelimb electromyograms recorded from monkeys performing reach-to-grasp tasks revealed 4–6 muscle components that showed transport/preshape- or grasp-related features. Weighting coefficients of transport/preshape-related components demonstrated strongest similarities for reaches that shared the same grasp type rather than the same target location. Scaling coefficients of transport/preshape- and grasp-related components showed invariant temporal coupling. Thus, grasp type influenced strongly both transport/preshape- and grasp-related muscle components, giving rise to grasp-based functional coupling between forelimb muscles.     

Synergistic influences of sensory and central stimuli on non-voluntary rhythmic arm movements

In recent years, neuromodulation of the cervical spinal circuitry has become an area of interest for investigating rhythmogenesis of the human spinal cord and interaction between cervical and lumbosacral circuitries, given the involvement of rhythmic arm muscle activity in many locomotor tasks. We have previously shown that arm muscle vibrostimulation can elicit non-voluntary upper limb oscillations in unloading body conditions. Here we investigated the excitability of the cervical spinal circuitry by applying different peripheral and central stimuli in healthy humans. The rationale for applying combined stimuli is that the efficiency of only one stimulus is generally limited. We found that low-intensity electrical stimulation of the superficial arm median nerve can evoke rhythmic arm movements. Furthermore, the movements were enhanced by additional peripheral stimuli (e.g., arm muscle vibration, head turns or passive rhythmic leg movements). Finally, low-frequency transcranial magnetic stimulation of the motor cortex significantly facilitated rhythmogenesis. The findings are discussed in the general framework of a brain-spinal interface for developing adaptive central pattern generator-modulating therapies.     

Neural basis of motor control and its cognitive implications

It has recently been demonstrated that human subjects and nonhuman primates adapt their arm movements when subjected to complex patterns of disturbing forces. The presence of aftereffects following the removal of the disturbing forces indicates that adaptation takes place through the development of an internal model of the disturbing force. The experimental evidence described in this paper has identified some important properties of this internal model: (1) it is limited to a region surrounding that part of the space where the disturbances had been experienced; (2) there is an enhancement of the internal model that depends only on the passage of time; and (3) there is a process of consolidation of the internal model, which takes a minimum of four hours. Anatomically, the substrate of the internal model is distributed; the motor cortex, basal ganglia, and cerebellum are interconnected structures that are active to different degrees during the acquisition of motor skills. Recent investigation of the spinal cord has suggested the existence of modules that organize the motor output in a discrete set of synergies. The outputs of these modules combine by addition, and might thus form the building blocks for the internal models represented by supraspinal structures.     

Coordination of eye and leg movements during visually guided stepping

In the present study, 2 related hypotheses were tested: first, that vision is used in a feedforward control mode during precision stepping onto visual targets and, second, that the oculomotor and locomotor control centers interact to produce coordinated eye and leg movements during that task. Participants' (N = 4) eye movements and step cycle transition events were monitored while they performed a task requiring precise foot placement at every step onto irregularly placed stepping stones under conditions in which the availability of visual information was either restricted or intermittently removed altogether. Accurate saccades, followed by accurate steps, to the next footfall target were almost always made even when the information had been invisible for as long as 500 ms. Despite delays in footlift caused by the temporary removal (and subsequent reinstatement) of visual information, the mean interval between the start of the eye movement and the start of the swing toward a target did not vary significantly (p >.05). In contrast, the mean interval between saccade onset away from a target and a foot landing on that target (stance onset) did vary significantly (p <.05) under the different experimental conditions. Those results support the stated hypotheses.     

Age-Related Differences in Locomotor Strategies During Adaptive Walking

Simultaneous control of lower limb stepping movements and trunk motion is important for skilled walking; adapting gait to environmental constraints requires frequent alternations in stepping and trunk motion. These alterations provide a window into the locomotor strategies adopted by the walker. The authors examined gait strategies in young and healthy older adults when manipulating step width. Anteroposterior (AP) and mediolateral (ML) smoothness (quantified by harmonic ratios) and stepping consistency (quantified by gait variability) were analyzed during narrow and wide walking while controlling cadence to preferred pace. Results indicated older adults preserved ML smoothness at the expense of AP smoothness, shortened their steps, and exhibited reduced stepping consistency. The authors conclude that older adults prioritized ML control over forward progression during adaptive walking challenges.     

A comparative review of the primate motor system

Primates have evolved separately from other mammals since the late Cretaceous, and during this time the two major extant primate groups, prosimians (lorises, lemurs, and tarsiers) and anthropoids (monkeys, apes, and humans) arose. Concurrently, structures within the central nervous system acquired primate characteristics. Not all of the uniquely primate features have been identified in the brain, but several are well known. The pyramidal system, the best studied motor system, shows a distinct primate pattern in its terminal connections in the spinal cord. Other descending systems are less well known, but primate specializations in the vestibular system and red nucleus have been observed. The primary and secondary motor cortices are topographically separated in primates, suggesting one basis for increased complexity. Given the size of the brain, structures in the basal ganglia are relatively enlarged in primates as compared with other mammals, whereas the cerebellum has the same relative size.     

The Role of Similarity Analysis in Understanding Movement

Primates have evolved separately from other mammals since the late Cretaceous, and during this time the two major extant primate groups, prosimians (lorises, lemurs, and tarsiers) and anthropoids (monkeys, apes, and humans) arose. Concurrently, structures within the central nervous system acquired primate characteristics. Not all of the uniquely primate features have been identified in the brain, but several are well known. The pyramidal system, the best studied motor system, shows a distinct primate pattern in its terminal connections in the spinal cord. Other descending systems are less well known, but primate specializations in the vestibular system and red nucleus have been observed. The primary and secondary motor cortices are topographically separated in primates, suggesting one basis for increased complexity. Given the size of the brain, structures in the basal ganglia are relatively enlarged in primates as compared with other mammals, whereas the cerebellum has the same relative size.     

Coordination of Eye and Leg Movements During Visually Guided Stepping

In the present study, 2 related hypotheses were tested: first, that vision is used in a feedforward control mode during precision stepping onto visual targets and, second, that the oculomotor and locomotor control centers interact to produce coordinated eye and leg movements during that task. Participants' (N = 4) eye movements and step cycle transition events were monitored while they performed a task requiring precise foot placement at every step onto irregularly placed stepping stones under conditions in which the availability of visual information was either restricted or intermittently removed altogether. Accurate saccades, followed by accurate steps, to the next footfall target were almost always made even when the information had been invisible for as long as 500 ms. Despite delays in footlift caused by the temporary removal (and subsequent reinstatement) of visual information, the mean interval between the start of the eye movement and the start of the swing toward a target did not vary significantly (p > .05). In contrast, the mean interval between saccade onset away from a target and a foot landing on that target (stance onset) did vary significantly (p < .05) under the different experimental conditions. Those results support the stated hypotheses.     

One-sided limb preference is linked to alternating-limb locomotion in anuran amphibians

Amphibians provide a unique opportunity for identifying possible links between lateralized behaviors, locomotion, and phylogeny and for addressing the origin of lateralized behaviors of higher vertebrates. Five anuran species with different locomotive habits were tested for forelimb and hind limb preferences during 2 stereotyped behavior sequences--wiping a foreign object off their snout and righting themselves from the overturned position. The experiments were analyzed in a broader context of previous findings on anuran lateralization involving 11 anuran species that were studied within the same experimental paradigms. This analysis shows that one-sided forelimb and hind limb motor lateralization in anurans is strongly associated with alternating-limb locomotion and other unilateral limb activity. Conclusions reached for anuran amphibians may be applicable to other vertebrates possessing paired appendages-the degree of lateralization in motor response depends on the mode of locomotion used by a species.     

An anatomically constrained, stochastic model of eye movement control in reading

This article presents SERIF, a new model of eye movement control in reading that integrates an established stochastic model of saccade latencies (LATER; R. H. S. Carpenter, 1981) with a fundamental anatomical constraint on reading: the vertically split fovea and the initial projection of information in either visual field to the contralateral hemisphere. The novel features of the model are its simulation of saccade latencies as a race between two stochastic rise-to-threshold LATER units and its probabilistic selection of the target for the next saccade. The model generates simulated eye movement behavior that exhibits important characteristics of actual eye movements made during reading; specifically, simulations produce realistic saccade target distributions and replicate a number of critical reading phenomena, including the effects of word frequency on fixation durations, the inverted optimal viewing position effect, the trade-off between first and second fixation durations of refixated words, and the dependence of parafoveal preview benefit on eccentricity.     

Effects of the menstrual cycle on looking preferences for faces in female rhesus monkeys

Fluctuations of ovarian hormones across the menstrual cycle influence a variety of social and cognitive behaviors in primates. For example, female rhesus monkeys exhibit heightened interest for males and increased agonistic interactions with other females during periods of high estrogen levels. In the present study, we hypothesized that females’ preference for males during periods of high estrogen levels is also expressed at the level of face perception. We tested four intact females on two face-tasks involving neutral portraits of male and female rhesus monkeys, chimpanzees and humans. In the visual preference task (VP), monkeys had to touch a button to view a face image. The image remained on the screen as long as the button was touched, and the duration of pressing was taken as an index of the monkey's looking time for the face stimulus. In the Face-Delayed Recognition Span Test (Face-DRST), monkeys were rewarded for touching the new face in an increasing number of serially presented faces. Monkeys were tested 5 days a week across one menstrual cycle. Blood was collected every other day for analysis of estradiol and progesterone. Two of the four females were cycling at the time of testing. We did not find an influence of the cycle on Face-DRST, likely due to a floor effect. In the VP however, the two cycling individuals looked longer at conspecific male faces than female faces during the peri-ovulatory period of the cycle. Such effects were absent for human and chimpanzee faces and for the two noncycling subjects. These data suggest that ovarian hormones may influence females’ preferences for specific faces, with heightened preference for male faces during the peri-ovulatory period of the cycle. Heightened interest for stimuli of significant reproductive relevance during periods of high conception risk may help guide social and sexual behavior in the rhesus monkey.     

A behavioral frequency discrimination paradigm for use in adult primates

A psychophysical apparatus and procedure that can be used to define the performance and estimate the thresholds of frequency discrimination in adult primates is described. This protocol has been used to train adult owl monkeys to discriminate differences in the frequencies of successively presented sinusoidal tactile stimuli delivered to a restricted skin surface of a single digit, and to train a second set of adult owl monkeys to discriminate. differences in frequencies between paired auditory tonal stimuli. The thresholds estimated with this procedure are comparable to those measured in other primates. The advantages of using this procedure for combined behavioral and physiological studies are discussed.