Emilio Bizzi

The Cognitive Neurosciences

Ed Michael S Gazzaniga MIT Press, pounds sterling64.95, pp 1447 ISBN 0 262 07157 6 The performance artist Laurie Anderson referred to her fathers death as being “like a library burning to the ground.” If the higher functions of human beings make up such a collection of texts then we are perhaps approaching some knowledge of their titles. More especially we are cognisant of the complexity that we face: an evolved network of interrelated systems capable of dynamic change; the coding of experience—memory; prefrontal systems which release us from the constraints of the immediate present, allowing us to reflect upon time future, past, and hypothetical; maps of cerebral activity which alter and adjust to the …

Convergent force fields organized in the frog's spinal cord

Microstimulation of the gray matter of the frogs spinal cord was used to elicit motor responses. Force responses were recorded with the frogs ankle clamped while EMG activity was monitored. The collections of force patterns elicited at different leg configurations were summarized as force fields. These force fields showed convergence to an equilibrium point. The equilibrium paths were calculated from the force fields with the leg clamped. These paths predicted free limb motion in 75% of trials. The force fields were separated into active and prestimulation resting responses. The active force field responses had a fixed position equilibrium. These active force fields were modulated in amplitude over time, although the balance and orientations of forces in the pattern remained fixed. The active fields grouped into a few classes. These included both convergent and parallel fields. The convergent force fields (CFFS) could be observed in deafferented preparations. Motoneuron (MN) activity underlying the force fields was marked using sulforhodamine. The marked activity covered several segments. Several simulations and MN stimulations show that topography, limb geometry, and random activation could not account for the results. It is likely that propriospinal interneurons distribute the activity that underlies the responses observed here. Experiments showed that CFFs that resemble those elicited by microstimulation also underlie natural behaviors. The full variety of fields revealed by microstimulation was larger than the repertoire elicited by cutaneous stimulation. It was concluded that fixed-pattern force fields elicited in the spinal cord may be viewed as movement primitives. These force fields could form building blocks for more complex behaviors.

The construction of movement by the spinal cord

We used a computational analysis to identify the basic elements with which the vertebrate spinal cord constructs one complex behavior. This analysis extracted a small set of muscle synergies from the range of muscle activations generated by cutaneous stimulation of the frog hindlimb. The flexible combination of these synergies was able to account for the large number of different motor patterns produced by different animals. These results therefore demonstrate one strategy used by the vertebrate nervous system to produce movement in a computationally simple manner.

Neuronal Correlates of Motor Performance and Motor Learning in the Primary Motor Cortex of Monkeys Adapting to an External Force Field

The primary motor cortex (M1) is known to control motor performance. Recent findings have also implicated M1 in motor learning, as neurons in this area show learning-related plasticity. In the present study, we analyzed the neuronal activity recorded in M1 in a force field adaptation task. Our goal was to investigate the neuronal reorganization across behavioral epochs (before, during, and after adaptation). Here we report two main findings. First, memory cells were present in two classes. With respect to the changes of preferred direction (Pd), these two classes complemented each other after readaptation. Second, for the entire neuronal population, the shift of Pd matched the shift observed for muscles. These results provide a framework whereby the activity of distinct neuronal subpopulations combines to subserve both functions of motor performance and motor learning.

Eye-Head Coordination in Monkeys: Evidence for Centrally Patterned Organization

Eye-head coordination was investigated by recording from the neck and eye muscles in monkeys. The results show that (i) during eye-head turning, neural activity reaches the neck muscles before the eye muscles, and (ii) all agonist neck muscles are activated simultaneously regardless of the initial head position. Since overt movement of the eyes precedes that of the head, it was concluded that the central neural command initiates the eye-head sequence but does not specify its serial order. Furthermore, it was determined that the compensatory eye movement is not initiated centrally but instead is dependent upon reflex activation arising from movement of the head.

Arm trajectory formation in monkeys

SummaryThe formation of forearm trajectories of moderate velocities (0.3–1.3 rad/s) was studied in monkeys performing a simple visuomotor task. The experiments were designed to test the hypothesis that the transition from one position to another is subserved by a rapid shift to a final equilibrium of forces in agonist and antagonist muscles. This idea is attractive because it suggests the possibility that in simple movements the trajectory is determined by the inherent inertial and viscoelastic properties of the limb and muscles around a joint. The results indicate that these moderate speed movements are controlled by a gradual, and not a step-like, shift to the final equilibrium position.

Generalization in vision and motor control

Learning is more than memory. It is not simply the building of a look-up table of labelled images, or a phone-directory-like list of motor acts and the corresponding sequences of muscle activation. Central to learning and intelligence is the ability to predict, that is, to generalize to new situations, beyond the memory of specific examples. The key to generalization, in turn, is the architecture of the system, more than the rules of synaptic plasticity. We propose a specific architecture for generalization for both the motor and the visual systems, and argue for a canonical microcircuit underlying visual and motor learning.

Mechanisms underlying recovery of eye-head coordination following bilateral labyrinthectomy in monkeys

SummarySince during active eye-head turning the eyes move first and with higher velocity than the head, the lines of sight reach the target while the head is still moving. Then for the remaining duration of the head movement the eyes maintain their fixation by performing a movement which is counter to that of the head and perfectly compensates for it. It is agreed that this compensatory eye movement is critically influenced by visual, vestibular and neck afferents and that it is not initiated centrally. We have investigated a) the relative contribution of the vestibular and neck afferents to the compensatory eye movement made during active and passive head turning in monkeys and b) the mechanisms underlying the recovery of compensatory eye movements following either the removal of the vestibular or neck loop or both. Our results have shown that 1. normal monkeys display perfect ocular stability in darkness, 2. at least 95% of ocular stability is due to the vestibular loop, and 3. the contribution of the neck loop is negligible. Following bilateral vestibulectomy the recovery of compensatory eye movements occurs gradually and reaches 90% within seven weeks but only during active head movements. We have shown that there are at least three mechanisms underlying this recovery: 1. an increase in gain of the neck loop. 2. the occurrence of a centrally programmed compensatory eye movement, and 3. a recalibration of the saccadic and head motor system.

Central and Sensory Contributions to the Activation and Organization of Muscle Synergies during Natural Motor Behaviors

Previous studies have suggested that the motor system may simplify control by combining a small number of muscle synergies represented as activation profiles across a set of muscles. The role of sensory feedback in the activation and organization of synergies has remained an open question. Here, we assess to what extent the motor system relies on centrally organized synergies activated by spinal and/or supraspinal commands to generate motor outputs by analyzing electromyographic (EMG) signals collected from 13 hindlimb muscles of the bullfrog during swimming and jumping, before and after deafferentation. We first established that, for both behaviors, the intact and deafferented data sets possess low and similar dimensionalities. Subsequently, we used a novel reformulation of the non-negative matrix factorization algorithm to simultaneously search for synergies shared by, and synergies specific to, the intact and deafferented data sets. Most muscle synergies were identified as shared synergies, suggesting that EMGs of locomotor behaviors are generated primarily by centrally organized synergies. Both the amplitude and temporal patterns of the activation coefficients of most shared synergies, however, were altered by deafferentation, suggesting that sensory inflow modulates activation of those centrally organized synergies. For most synergies, effects of deafferentation on the activation coefficients were not consistent across frogs, indicating substantial interanimal variability of feedback actions. We speculate that sensory feedback might adapt recruitment of muscle synergies to behavioral constraints, and the few synergies specific to the intact or deafferented states might represent afferent-specific modules or feedback reorganization of spinal neuronal networks.

Controlling multijoint motor behavior.

Much can be learned about the central nervous system from a study of motor coordination, but its true richness and complexity become evident only in a multiarticular system. Despite the intrinsic complexity of multiarticular actions, they offer an unparalleled opportunity to learn about the central nervous system in a quantitative and experimentally testable way. For example, the observation that unconstrained, unperturbed arm movements are coordinated in terms of hand motion shows that motor control is organized in a hierarchy of increasing levels of abstraction. These arm motions are organized as though a disembodied hand could be moved in space; the details of how this is to be achieved must then be supplied by a different level in the hierarchy. The essence of human behavior is its adaptability. Just as the true complexity of coordination is evident only in multiarticular actions, the sophistication and subtlety of adaptive behavior are evident only in dynamic, interactive tasks. A study of movement alone is not sufficient to understand this behavior. The dynamic response of the limbs becomes the overriding concern and must be controlled by the central nervous system. The dynamic response of a limb is usually associated with its posture, rather than its movement, but in a functional task such as the use of a tool, the postural dynamics are an integral part of the action. This perspective on motor behavior leads to some useful insights. Coordination is not a problem for movement alone; in a multiarticular system, even posture requires coordination and control. Muscles do not merely act reciprocally to generate forces about the joints; the net mechanical impedance of the limb may be controlled by synergistic activation of all muscles, including antagonists. Controlling dynamic behavior is a far more demanding task than controlling motion. Consequently, features of the neuromusculoskeletal system that appear to be redundant or unnecessary for movement control can play a functional role in controlling dynamic behavior. Polyarticular muscles contribute to the mechanical impedance in a unique way. Skeletal redundancies have a profound influence on all aspects of dynamic behavior, including the apparent inertia of the limbs. Redundancies are commonly perceived as a complicating factor in the control of motion, a problem that must be solved by the central nervous system. Rather than presenting a problem requiring solution, they may present a solution to a problem. Posture is not merely the outcome of a motor act; it is one of the important preparatory stages in the production of motor behavior.