Spontaneous motor rhythms of the back and legs in a patient with a complete spinal cord transection.

BACKGROUND: Spontaneous activity originating from the spinal cord has been sporadically reported in humans. OBJECTIVES: Investigation of such rhythmic activity of the trunk and legs in a 49-year-old male patient who had a complete severance of the spinal cord at the fifth thoracic vertebra. METHODS: A multichannel electromyography (EMG) study was performed together with kinematics measurements obtained from an Optotrak system. RESULTS: Episodes of rhythmic trunk and lower limb movements started 6 to 7 years after the spinal lesion, recurred at 2 to 3 month intervals, and continued uninterrupted for 2 to 3 days despite continuous delivery of intrathecal baclofen. Several muscles discharged more or less synchronously on both sides but others clearly alternated, for instance, between hip flexors and knee or ankle extensors. Sensory stimuli (hip repositioning or skin pinch) altered significantly the baseline rhythm of about 1 Hz. The patient had both hips injected with corticosteroids and was free of these episodic rhythmic crises for more than 6 months. CONCLUSION: The rhythmic activity observed in the patient appeared related to the activation of a spinal pattern generator akin to what has been described in most animal species after complete spinal lesions.

Synchronization in primate cerebellar granule cell layer local field potentials: basic anisotropy and dynamic changes during active expectancy.

The cerebellar cortex is remarkable for its organizational regularity, out of which task-related neural networks should emerge. In Purkinje cells, both complex and simple spike network patterns are evident in sensorimotor behavior. However, task-related patterns of activity in the granule cell layer (GCL) have been less studied. We recorded local field potential (LFP) activity simultaneously in pairs of GCL sites in monkeys performing an active expectancy (lever-press) task, in passive expectancy, and at rest. LFP sites were selected when they showed strong 10-25 Hz oscillations; pair orientation was in stereotaxic sagittal and coronal (mainly), and diagonal. As shown previously, LFP oscillations at each site were modulated during the lever-press task. Synchronization across LFP pairs showed an evident basic anisotropy at rest: sagittal pairs of LFPs were better synchronized (more than double the cross-correlation coefficients) than coronal pairs, and more than diagonal pairs. On the other hand, this basic anisotropy was modifiable: during the active expectancy condition, where sagittal and coronal orientations were tested, synchronization of LFP pairs would increase just preceding movement, most notably for the coronal pairs. This lateral extension of synchronization was not observed in passive expectancy. The basic pattern of synchronization at rest, favoring sagittal synchrony, thus seemed to adapt in a dynamic fashion, potentially extending laterally to include more cerebellar cortex elements. This dynamic anisotropy in LFP synchronization could underlie GCL network organization in the context of sensorimotor tasks.

Functional role of unmyelinated tactile afferents in human hairy skin: sympathetic response and perceptual localization.

In addition to A-beta fibres the human hairy skin has unmyelinated (C) fibres responsive to light touch. Previous functional magnetic resonance imaging (fMRI) studies in a subject with a neuronopathy who specifically lacks A-beta afferents indicated that tactile C afferents (CT) activate insular cortex, whereas no response was seen in somatosensory areas 1 and 2. Psychophysical tests suggested that CT afferents give rise to an inconsistent perception of weak and pleasant touch. By examining two neuronopathy subjects as well as control subjects we have now demonstrated that CT stimulation can elicit a sympathetic skin response. Further, the neuronopathy subjects' ability to localize stimuli which activate CT afferents was very poor but above chance level. The findings support the interpretation that the CT system is well suited to underpin affective rather than discriminative functions of tactile sensations.

Unmyelinated tactile afferents underpin detection of low-force monofilaments.

Human hairy but not glabrous skin has unmyelinated (C) tactile (CT) afferents that project to insular cortex. We studied two subjects with the rare sensory neuronopathy syndrome who lack A-beta fibers but have relatively preserved C-fiber function. Weak monofilaments were detected on hairy skin alone. Hence, the ability to detect light touch does not depend entirely on the A-beta somatosensory system; CT afferents may contribute to the detection of weak monofilaments.

Local field potential oscillations in primate cerebellar cortex: synchronization with cerebral cortex during active and passive expectancy.

Many brain regions, such as the cerebellum, primary somatosensory cortex (SI), and primary motor cortex (MI), interact to produce coordinated actions. Synchronization of local field potentials (LFPs) in sensorimotor cerebral areas has been related to motor performance, often through 10- to 25-Hz oscillatory LFPs. The macaque cerebellar paramedian lobule (PM) also shows 10- to 25-Hz LFP oscillations, which are modulated in a stimulus-response lever press task to get reward (active condition), but also, albeit differently, in a similarly timed stimulus-reward relation (passive condition). This study focuses on simultaneous LFP activity in primate SI or MI and the PM cerebellum during the active (left- or right-hand lever presses) and passive conditions. Results show a similar modulation pattern of 10- to 25-Hz oscillations in the cerebellum, MI, and SI during the active condition (left or right hand), decreasing after stimulus onset, returning, and again decreasing after movement onset. In the passive condition, when the monkey did not move but got reward, all 3 areas show an oscillatory profile where oscillations increase after stimulus onset and last until reward, denoting a role for these oscillations in passive expectancy. However, synchronization between cerebellar LFPs and SI LFPs is higher during the active condition than during the passive condition, and highest for the interested hand. This greater PM-SI synchronization, when the monkey had to press the lever, could represent a form of cerebro-cerebellar communication, perhaps to serve somatosensory processing to accomplish the task; PM-MI synchronization was less selective for the hand used and might carry a more general type of information.

Production and perception of grip force without proprioception: is there a sense of effort in deafferented subjects?

We assessed the ability of healthy subjects (n = 7) and a patient deprived of proprioception (GL) to produce and assess different levels of isometric forces. They first produced a target force with one hand (the reference control hand) and then, after a delay of 3 s, they attempted to match it with the other hand (the experimental matching hand). Despite abnormal variations in motor outputs, we found that GL could, as could the control subjects, maintain a constant relationship between the force exerted by the control hand and the force exerted by the experimental hand. As GL was deprived of proprioceptive cues, these results suggest that she indirectly perceived muscular force through central effort. Interestingly, when carrying out the task the patient reported neither feelings of fatigue nor awareness of how hard she tried to perform the matches. Hence, under certain circumstances (such as in our motor task), it seems possible to assess and scale muscular force on the basis of endogenous signals only. However, internally generated signals related to the size of the motor command may need to interact with afferent input to gain full access to consciousness.

The effects of digital anesthesia on force control using a precision grip.

A total of 20 right-handed subjects were asked to perform a grasp-lift-and-hold task using a precision grip. The grasped object was a one-degree-of-freedom manipuladum consisting of a vertically mounted linear motor capable of generating resistive forces to simulate a range of object weights. In the initial study, seven subjects (6 women, 1 man; ages 24-56 yr) were first asked to lift and hold the object stationary for 4 s. The object presented a metal tab with two different surface textures and offered one of four resistive forces (0.5, 1.0, 1.5, and 2.0 N). The lifts were performed both with and without visual feedback. Next, the subjects were asked to perform the same grasping sequence again after ring block anesthesia of the thumb and index finger with mepivacaine. The objective was to determine the degree to which an internal model obtained through prior familiarity might compensate for the loss of cutaneous sensation. In agreement with previous studies, it was found that all subjects applied significantly greater grip force after digital anesthesia, and the coordination between grip and load forces was disrupted. It appears from these data, that the internal model alone is insufficient to completely compensate for the loss of cutaneous sensation. Moreover, the results suggest that the internal model must have either continuous tonic excitation from cutaneous receptors or at least frequent intermittent reiteration to function optimally. A subsequent study performed with 10 additional subjects (9 women, 1 man; ages 24-49 yr) indicated that with unimpaired cutaneous feedback, the grasping and lifting forces were applied together with negligible forces and torques in other directions. In contrast, after digital anesthesia, significant additional linear and torsional forces appeared, particularly in the horizontal and frontal planes. These torques were thought to arise partially from the application of excessive grip force and partially from a misalignment of the two grasping fingers. These torques were further increased by an imbalance in the pressure exerted by the two opposing fingers. Vision of the grasping hand did not significantly correct the finger misalignment after digital anesthesia. Taken together, these results suggest that mechanoreceptors in the fingertips signal the source and direction of pressure applied to the skin. The nervous system uses this information to adjust the fingers and direct the pinch forces optimally for grasping and object manipulation.

Local field potential oscillations in primate cerebellar cortex: modulation during active and passive expectancy.

Cerebellar local field potential (LFP) oscillations were recorded in the paramedian lobule of one hemisphere, while monkeys were in two behavioral conditions: actively performing an elbow flexion-extension or a lever-press task in response to an auditory or visual stimulus to get reward (active condition), or waiting quietly for the reward to come in the same time window after the appearance of the stimulus (passive condition). The oscillations in the paramedian lobule were first characterized in four monkeys, and they showed an idiosyncratic frequency for each monkey, between 13 and 25 Hz. The granule cell layer multi-unit activity was phase-locked with the negative phase of the LFP oscillations, while Purkinje cell simple spikes were also sometimes phase-locked with the LFP. Three monkeys were trained to perform the motor tasks: the LFP oscillations were modulated, in the active condition, in a systematic manner in relation to the lever-press or elbow flexion-extension tasks. During periods when the monkey was waiting to initiate movement, LFP oscillations appeared and then stopped with movement initiation. This modulation was valid for the task being executed with either hand. Surprisingly, the LFP oscillations were also systematically modulated during the passive condition; as the monkey was waiting for the usual time to get a reward passively, oscillations appeared stronger and were stopped by the end of the usual delay, whether the monkey was rewarded or not. This type of modulation was not affected by the length of the stimulus, as long as the reward window was known to the monkey. If the monkey had not been previously trained to the active condition, the modulation appeared in the passive condition. These results show that cerebellar LFP oscillations in the paramedian lobule are reliably present when the monkey is involved in a waiting period, whether this period ends with an active or passive event. This study provides electrophysiological evidence for a specific pattern of activity in the cerebellum for the expectancy of events that are known to be bound to happen, either externally, or from voluntary action.

Haptic discrimination of object shape in humans: contribution of cutaneous and proprioceptive inputs.

Using two-dimensional (2D) angles composed of two straight, 8-cm-long arms that formed an angle, we investigated the importance of cutaneous feedback from the exploring index finger, and proprioceptive feedback from the shoulder (scanning movements made with the outstretched arm), to the human ability to discriminate small differences in the angles. Using a two-alternative forced-choice paradigm, subjects identified the larger angle in each pair explored (standard angle, 90 degrees; comparison angles, 91 degrees to 103 degrees). Subjects were tested under four experimental conditions: (1) active touch (reference condition); (2) active touch with digital anaesthesia; (3) passive touch (a computer-controlled device displaced the angle under the subject's immobile digit); and (4) passive touch with digital anaesthesia. When only proprioceptive feedback from the shoulder was available (condition 2), there was a significant increase in discrimination threshold, from 4.0 degrees in the reference condition (condition 1) to 7.2 degrees, indicating that cutaneous feedback from the exploring digit contributed to task performance. When only cutaneous feedback from the finger was available (condition 3), there was also a significant increase in threshold from 4.2 degrees in the active condition to 8.7 degrees. This suggested that proprioceptive feedback from the shoulder, potentially from a variety of deep (muscle and joint) but also cutaneous receptors, contributed to the ability to discriminate small changes in 2D angles. When both sources of feedback were eliminated (condition 4), subjects were unable to discriminate even the largest difference presented (13 degrees). The results suggest that this sensory task is truly an integrative task drawing on sensory information from two different submodalities and so, following the definition of Gibson, is haptic in nature. The results are discussed in relation to the potential neural mechanisms that might underlie a task that requires integration across two anatomically separate body parts and two distinct modalities.

Lack of conscious recognition of one's own actions in a haptically deafferented patient.

How do we become aware of our own actions? This classical question is still a matter of debate: does consciousness depend on central efferent signals or derive from peripheral information? In this paper, we had the opportunity to study a haptically deafferented patient using a well-tested experimental paradigm where a cognitive conflict is produced between motor intention, proprioception and visual feedback. Our results show that the patient was able to solve the conflict and to generate accurate movements to a target in the absence of proprioceptive feedback and with very limited visual feedback from her movements. Yet, she could not report any conscious perception of the conflict and showed no conscious knowledge of her actual performance. We suggest that information derived from efferent processes cannot in themselves be a source for conscious experience about our own actions.