Adaptive motor control in crayfish

International audienceThis article reviews the principles that rule the organization of motor commands that have been described over the past ®ve decades in cray®sh. The adaptation of motor behaviors requires the integration of sensory cues into the motor command. The respective roles of central neural networks and sensory feedback are presented in the order of increasing complexity. The simplest circuits described are those involved in the control of a single joint during posture (negative feedback±resistance re¯ex) and movement (modulation of sensory feedback and reversal of the re¯ex into an assistance re¯ex). More complex integration is required to solve problems of coordination of joint movements in a pluri-segmental appendage, and coordination of dierent limbs and dierent motor systems. In addition, beyond the question of mechanical ®tting, the motor command must be appropriate to the behavioral context. Therefore, sensory information is used also to select adequate motor programs. A last aspect of adaptability concerns the possibility of neural networks to change their properties either temporarily (such on-line modulation exerted, for example, by presynaptic mechanisms) or more permanently (such as plastic changes that modify the synaptic ecacy). Finally, the question of how``automatic'' local component networks are controlled by descending pathways, in order to achieve behaviors, is discussed.

Neural Mechanisms of Reflex Reversal in Coxo-Basipodite Depressor Motor Neurons of the Crayfish

International audienceNeural mechanisms of reflex reversal in coxo-basipodite depressor motor neurons of the crayfish. J. Neurophysiol. 77: 1963–1978, 1997. The in vitro preparation of the fifth thoracic ganglion of the crayfish was used to investigate the mechanisms underlying the reflex reversal in a sensory-motor pathway. Sensory afferent neurons from the coxo-basipodite chordotonal organ (CBCO), which senses vertical movements of the limb, connect monosynaptically with basal limb motor neurons (MNs). In tonically active preparation, stretching the CBCO (corresponding to downward movements of the leg) stimulates the levator MNs, whereas releasing the CBCO activates the depressor (Dep) MNs. These reflexes, opposed to the imposed movement, are termed resistance reflexes. By contrast, during fictive locomotion, the reflexes are reversed and termed assistance reflexes. Intracellular recordings from all 12 Dep MNs were performed in single experiments. It allowed us to characterize three types of Dep MNs according to their response to CBCO imposed step-and-ramp movements: 8 of the 12 Dep MNs are resistance MNs that are depolarized during release of the CBCO and are connected monosynaptically to release-sensitive CBCO neurons; 1 Dep MN is an assistance MN that is depolarized during stretching of the CBCO and is connected monosynaptically to exclusively velocity-coding stretch-sensitive CBCO neurons; in our experimental conditions, 3 Dep MNs do not display any response to CBCO stimulation. Assistance reflex interneurons (ARINs), involved in polysynaptic assistance reflexes recorded from depressor MNs, are presented. During low-velocity (0.05 mm/s) stretching ramps imposed on the CBCO, ARINs display compound excitatory postsynaptic potentials (EPSPs), whereas during high-velocity (0.25 mm/s) ramps, they display a mixed excitatory and inhibitory response. Whereas a single MN generally receives monosynaptic EPSPs from three to six CBCO neurons, ARINs receive monosynaptic EPSPs from up to eight velocity-coding stretch-sensitive CBCO neurons. In addition, ARINs receive disynaptic inhibitory phasic inputs from stretch-sensitive CBCO afferents. Injection of a depolarizing current pulse into ARINs elicits a fast transient voltage-dependent depolarization. Its time to peak decreases, and its peak amplitude increases with increasing current intensity. ARINs likely are to be connected directly to Dep MNs. The synaptic delay between these nonspiking ARINs and Dep MNs is short (<2 ms) and constant. The postsynaptic EPSP amplitude increases with increasing current pulse intensity injected into ARIN. The dual sensory control (excitatory and inhibitory) makes it likely that ARIN represents a key element in reflex reversal control

Active Motor Neurons Potentiate Their Own Sensory Inputs via Glutamate-Induced Long-Term Potentiation

International audienceAdaptive motor control is based mainly on the processing and integration of proprioceptive feedback information. In crayfish walking leg, many of these operations are performed directly by the motor neurons (MNs), which are connected monosynapti-cally by sensory afferents (CBTs) originating from a chordotonal organ that encodes vertical limb movements. An in vitro preparation of the crayfish CNS was used to investigate a new control mechanism exerted directly by motor neurons on the sensory inputs themselves. Paired intracellular recordings demonstrated that, in the absence of any presynaptic sensory firing, the spiking activity of a leg MN is able long-lastingly to enhance the efficacy of the CBT-MN synapses. Moreover, this effect is specific to the activated MN because no changes were induced at the afferent synapses of a neighboring silent MN. We report evidence that long-term potentiation (LTP) of the monosynaptic EPSP involves a retrograde system of glutamate transmission from the postsynaptic MN, which induces the activation of a metabotropic glutamate receptor located presynaptically on the CBTs. We demonstrate that LTP at crayfish sensory-motor synapses results exclusively from the long-lasting enhancement of release of acetylcholine from presynaptic sensory af-ferent terminals, without inducing any modifications in postsyn-aptic MN properties. Our data indicate that this positive feedback control represents a functional mechanism that may play a key role in the auto-organization of sensory-motor networks

Direct glutamate-mediated presynaptic inhibition of sensory afferents by the postsynaptic motor neurons

International audienceAn in vitro preparation of the crayfish central nervous system was used to study a negative feedback control exerted by the glutamatergic motor neurons (MNs) on to their presynaptic cholinergic sensory afferents. This negative control consists in small amplitude, slowly developing depolarizations of the primary afferents (sdPADs) strictly timed with MN bursts. They were not blocked by picrotoxin, but were sensitive to glutamate non-N-methyl-D-aspartate (NMDA) antagonists. Intracellular recordings were performed within thin branches of sensory terminals while electrical antidromic stimulation were applied to the motor nerves, or while glutamate (the MN neurotransmitter) was pressure-applied close to the recording site. Electrical motor nerve stimulations and glutamate pressure application had similar effects on to sensory terminals issued from the coxo-basipodite chordotonal organ (CBTs): like sdPADs, both stimulation-induced depolarizations were picrotoxin-resistant and were dramatically reduced by non-NMDA antagonist bath application. These results indicate that sdPADs are likely directly produced by MNs during locomotor activity. A functional scheme is proposed

Efferent controls in crustacean mechanoreceptors

International audienceSince the 1960s it has been known that central neural networks can elaborate motor patterns in the absence of any sensory feedback. However, sensory and neuromodulatory inputs allow the animal to adapt the motor command to the actual mechanical configuration or changing needs. Many studies in invertebrates, particularly in crustacea, have described several mechanisms of sensory-motor integration and have shown that part of this integration was supported by the efferent control of the mechanosensory neurons themselves. In this article, we review the findings that support such an efferent control of mechanosensory neurons in crustacea. Various types of crustacean proprioceptors feeding information about joint movements and strains to central neural networks are considered, together with evidence of efferent controls exerted on their sensory neurons. These efferent controls comprise (1) the neurohormonal modulation of the coding properties of sensory neurons by bioamines and peptides; (2) the presynaptic inhibition of sensory neurons by GABA, glutamate and histamine; and (3) the long-term potentiation of sensory-motor synapses by glutamate. Several of these mechanisms can coexist on the same sensory neuron, and the functional significance of such multiple modulations is discussed

Alteration of size perception: serotonin has opposite effects on the aggressiveness of crayfish confronting either a smaller or a larger rival

International audienceWe injected serotonin (5-HT) into adult male crayfish before pairing them with size-matched non-injected competitors, and observed dyadic agonistic interactions. Paradoxically, 5-HT elicited opposite behavioral responses if the injected animal was opposed by a smaller or larger rival: the level of aggressiveness of the injected crayfish was higher when facing a larger rival but lower when facing a smaller rival. Our results indicate that the effects of 5-HT on aggressiveness are dependent on the perception of the relative size difference of the opponent. In both cases, however, 5-HT significantly delayed the decision to retreat. We conclude that 5-HT does not primarily act on aggressiveness but rather on the brain centers that integrate risk assessment and/or decision making, which then modulate the aggressive response. Our findings support a reinterpretation of the role of 5-HT in crustacean agonistic behavior that may be of interest for studies of other animals

Neural Circuit Reconfiguration by Social Status

The social rank of an animal is distinguished by its behavior relative to others in its community. Although social-status-dependent differences in behavior must arise because of differences in neural function, status-dependent differences in the underlying neural circuitry have only begun to be described. We report that dominant and subordinate crayfish differ in their behavioral orienting response to an unexpected unilateral touch, and that these differences correlate with functional differences in local neural circuits that mediate the responses. The behavioral differences correlate with simultaneously recorded differences in leg depressor muscle EMGs and with differences in the responses of depressor motor neurons recorded in reduced, in vitro preparations from the same animals. The responses of local serotonergic interneurons to unilateral stimuli displayed the same status-dependent differences as the depressor motor neurons. These results indicate that the circuits and their intrinsic serotonergic modulatory components are configured differently according to social status, and that these differences do not depend on a continuous descending signal from higher centers

Social Interactions Determine Postural Network Sensitivity to 5-HT

The excitability of the leg postural circuit and its response to serotonin (5-HT) were studied in vitro in thoracic nervous system preparations of dominant and subordinate male crayfishes. We demonstrate that the level of spontaneous tonic activity of depressor and levator motoneurons (MNs) (which control downward and upward movements of the leg, respectively) and the amplitude of their resistance reflex are larger in dominants than in subordinates. Moreover, we show that serotonergic neuromodulation of the postural circuit also depends on social status. Depressor and levator MN tonic firing rates and resistance reflex amplitudes were significantly modified in the presence of 10 M5-HT in dominants but not in subordinates. Using intracellular recording from depressor MNs,we show that their input resistance was not significantly different in dominants and subordinates in control conditions. However, 5-HT produced a marked depolarization in dominants and a significantly weaker depolarization in subordinates. Moreover, in the presence of 5-HT, the amplitude of the resistance reflex and the input resistance of MNs increased in dominants and decreased in subordinates. The peak amplitude and the decay phase of unitary EPSPs triggered by sensory spikes were significantly increased by 5-HT in dominants but not in subordinates. These observations suggest that neural networks are more reactive in dominants than in subordinates, and this divergence is even reinforced by 5-HT modulation

Perceptually-guided deep neural networks for ego-action prediction: Object grasping

We tackle the problem of predicting a grasping action in ego-centric video for the assistance to upper limb amputees. Our work is based on paradigms of neuroscience that state that human gaze expresses intention and anticipates actions. In our scenario, human gaze fixations are recorded by a glass-worn eye-tracker and then used to predict the grasping actions. We have studied two aspects of the problem: which object from a given taxonomy will be grasped, and when is the moment to trigger the grasping action. To recognize objects, we using gaze to guide Convolutional Neural Networks (CNN) to focus on an object-to-grasp area. However, the acquired sequence of fixations is noisy due to saccades toward distractors and visual fatigue, and gaze is not always reliably directed toward the object-of-interest. To deal with this challenge, we use video-level annotations indicating the object to be grasped and a weak loss in Deep CNNs. To detect a moment when a person will take an object we take advantage of the predictive power of Long-Short Term Memory networks to analyze gaze and visual dynamics. Results show that our method achieves better performance than other approaches on a real-life dataset. (C) 2018 Elsevier Ltd. All rights reserved.This work was partially supported by French National Center of Scientific research with grant Suvipp PEPS CNRS-Idex 215-2016, by French National Center of Scientific research with Interdisciplinary project CNRS RoBioVis 2017–2019, the Scientific Council of Labri, University of Bordeaux, and the Spanish Ministry of Economy and Competitiveness under the National Grants TEC2014-53390-P and TEC2014-61729-EXP.Publicad

Model and experiments to optimize co-adaptation in a simplified myoelectric control system

Objective. To compensate for a limb lost in an amputation, myoelectric prostheses use surface electromyography (EMG) from the remaining muscles to control the prosthesis. Despite considerable progress, myoelectric controls remain markedly different from the way we normally control movements, and require intense user adaptation. To overcome this, our goal is to explore concurrent machine co-adaptation techniques that are developed in the field of brain-machine interface, and that are beginning to be used in myoelectric controls. Approach. We combined a simplified myoelectric control with a perturbation for which human adaptation is well characterized and modeled, in order to explore co-adaptation settings in a principled manner. Results. First, we reproduced results obtained in a classical visuomotor rotation paradigm in our simplified myoelectric context, where we rotate the muscle pulling vectors used to reconstruct wrist force from EMG. Then, a model of human adaptation in response to directional error was used to simulate various co-adaptation settings, where perturbations and machine co-adaptation are both applied on muscle pulling vectors. These simulations established that a relatively low gain of machine co-adaptation that minimizes final errors generates slow and incomplete adaptation, while higher gains increase adaptation rate but also errors by amplifying noise. After experimental verification on real subjects, we tested a variable gain that cumulates the advantages of both, and implemented it with directionally tuned neurons similar to those used to model human adaptation. This enables machine co-adaptation to locally improve myoelectric control, and to absorb more challenging perturbations. Significance. The simplified context used here enabled to explore co-adaptation settings in both simulations and experiments, and to raise important considerations such as the need for a variable gain encoded locally. The benefits and limits of extending this approach to more complex and functional myoelectric contexts are discussed