The "Neuronal Dynamics and Learning" Team

    The objective of the Neuroal Dynamics and Learning Team is to understand how the frontal cortex and basal ganglia mediate visually guided actions and associative visuomotor learning. Experiments are carried out both in humans and non-human primates, with the aim of bridging data obtained in the two species. To do so, we put much emphasis on two issues: (1) the use of behavioral tasks developed in monkeys to study the human brain; (2) the links between different levels of analysis (neuron, populations of neurons, cerebral networks, behavior, computational models). Our multidisciplinary approach leads to a cross fertilization of data from neurophysiology, neuroimaging and clinical data.

Research topics

1. Neural bases of arbitrary visuomotor learning. Humans and monkeys have a remarkable capacity to learn arbitrary relations between a visual stimulus, or context, an action and its outcome (Hadj-Bouziane et al., 2003). Arbitrary visuomotor learning is a form of instrumental (or operant) conditioning, and it allows us and other animals to learn the consequence of our actions in a given context (e.g., not to touch an electric stove when it is on). It assures a flexible adaptation to novel situations (e.g., learning to read a new language) and it grants the formation of habits when the context is stable. In addition, pathological conditions such as obsessive-compulsive disorders and, most probably, addiction are tightly linked to this cognitive ability. Arbitrary associations can be learnt via different mechanisms both in humans and primates: learning by trial-and-error and learning by observation. Two complementary projects are identifying the neural bases of such extraordinary learning abilities.

• Learning by observation (LeO). This project brings together experimental social psychology, brain imaging and behavioural neurophysiology and it is part of a collaborative research programme funded by the French ANR (National Research Agency). The aim is to understand how the basal ganglia and the frontal cortex mediate learning by observation. The project combines behavioural neurophysiology in awake monkeys, neuroimaging in humans (Monfardini et al., submitted) and behavioral studies both in humans and monkeys (Meunier et al., 2007).
• Learning by trial-and-error. The objective of this project is to understand the neural bases of instrumental learning from single neurons to brain networks (Fig.1). The approach is to predict the underlying computations from associative learning theory, estimate their evolution from behavioral data (Brovelli et al., 2007) and probe their neural implementation on brain signals. Through this approach, we recently identified the neural computations of arbitrary visuomotor learning at the network level by means of fMRI (Brovelli et al., in press). The project also combines neural activity from single neurons and neural populations (Hadj-Bouziane & Boussaoud, 2003) to understand how assemblies are shaped by experience to produce learning. 
2. Skill Learning through physical practice and motor imagery. Behavioral studies on this topic rely on a state-of-the-art technique of recording of  movement kinematics, to study visuomotor skill learning by mental imagery. We recently showed that mental rehearsal can be beneficial for motor learning and suggest that imagery might be used to supplement or partly replace physical practice in clinical rehabilitation (Allami et al., 2008). The goal of this project is to understand the neuronal dynamics during learning through physical practice and motor imagery (Allami et al., in preparation).
3. Neural bases of eye-hand coordination. The dorsal premotor cortex (PMd) and frontal eye field (FEF) control respectively arm and eye movements. We have long been interested in how these areas integrate information from other body parts. Recording of neuronal activity in the awake monkey is used to demonstrate cross-influence in these regions: the influence of gaze direction on PMd cells, and of arm position on FEF cells (Fig. 2, Thura D et al., 2008).
4. Parkinson's disease. Parkinson's disease is the main pathology affecting the fronto-striatal system. Akinesia, rigidity and tremor are accompanied by non-motor troubles which remain poorly known. This question is studied in parallel in parkinsonian patients and in the monkey model of the disease (MPTP), using different cognitive tasks (including conditional associative learning). The aim is to define the nature of these non-motor disorders, and to assess the impact of the disease's treatments: pharmacological (dopatherapy) and surgical (high frequency subthalamic stimulation) (Kaphan et al., 2003; Witjas et al., 2007a, 2007b; Laksiri et al., 2007).

Methods

• Neuropsychology
• Psychophysics
• Neurophysiology (multi-electrodes single unit recordings and LFP (see video 1); EEG and SEEG)
• Functional imaging (fMRI)
• Computational modeling

Members

Collaborations

• Martine Meunier recently moved to the lab Espace et Action of the INSERM (Lyon), but she is still involved in several projects of the team.
• Abdelhamid Benazzouz from the Laboratoire de Neuropsychologie, CNRS UMR 5543, Université Victor Segalen, Bordeaux . The collaboration is centred on MPTP models.
• Hélène Frankowska, CREA, Ecole Polytechnique, Paris. Computer modeling of arbitrary visuomotor learning.
• Philippe Kahane, CHU de Grenoble, and Jean-Philippe Lachaux, Dynamique Cérébrale et Cognition INSERM, Lyon, for intracranial EEG recordings in epileptic patients
• Patrick Chauvel, from the Unité Epilsepsie et Cognition, INSERM U751, Marseille.
• Yves Paulignan from the Laboratoire sur le Langage, le Cerveau et la Cognition,  CNRS UMR 5230, Lyon. The collaboration is based on the study of  the kinematics of reaching and grasping, learning with physical practice and motor imagery.
• Christoph Segebarth, Neuroimagerie Fonctionnelle et Métabolique, Unité Mixte INSERM / Université Joseph Fourier U594, Centre Hospitalier Universitaire, Grenoble.

Publications (last update jan. 2008)

1. Brovelli A, Laksiri N, Nazarian B, Meunier M, Boussaoud  D (in press). Understanding the Neural Computations of Arbitrary Visuomotor Learning through fMRI and Associative Learning Theory. Cereb. Cortex. Nov 27 [Epub ahead of print].
2. Allami N, Paulignan Y, Brovelli A, Boussaoud D (2008). Visuo-motor learning with combination of different rates of motor imagery and physical practice. Exp. Brain Res., 184(1):105-13.
3. Thura D, Hadj-Bouziane F, Meunier M, Boussaoud D (2008). Hand position modulates saccadic activity in the frontal eye field. Behavi Brain Res., 186(1):148-53.
   
4. Brovelli A, Coquelin PA, Boussaoud D (2007). Estimating the hidden learning representations. J. Physiol. Paris, 101(1-3):110-7.
5. Meunier M, Monfardini E, Boussaoud D (2007). Learning by observation in rhesus monkeys. Neurobiol. Learn. Mem., 88(2):243-8.
6. Laksiri N, Kaphan E, Pellissier JF, Ali Chérif A (2007). Brain magnetic resonance imaging and neuropathology of cortical laminar necrosis. Rev. Neurol. (Paris), 163(3):365-8.
7. Witjas T, Kaphan E, Azulay JP (2007a).Non-motor fluctuations in Parkinson's disease. Rev. Neurol (Paris), 163(8-9):846-50.
8. Witjas T, Kaphan E, Régis J, Jouve E, Chérif AA, Péragut JC, Azulay JP (2007b). Effects of chronic subthalamic stimulation on nonmotor fluctuations in Parkinson's disease. Mov. Disord., 15;22(12):1729-34.
9. Roy A.C., Paulignan Y., Meunier M., Boussaoud D.(2006) Prehension movements in the macaque monkey: effects of perturbation of object size and location. Exp. Brain Res., 169(2):182-93.
10. Brovelli A, Lachaux JP, Kahane P, Boussaoud D (2005). High gamma frequency oscillatory activity dissociates attention from intention in the human premotor cortex.  NeuroImage, 28(1):154-64.
11. Hadj-Bouziane F, Meunier M, Boussaoud D (2003). Conditional visuo-motor learning in primates : a key role for the basal ganglia. J. of Physiol. Paris, 97(4-6):567-79.
12. Hadj-Bouziane F & Boussaoud D (2003). Neuronal activity in the monkey striatum during conditional visuomotor learning. Exp. Brain Res., 153(2):190-6.
13. Kaphan E, Eusebio A, Donnet A, Witjas T, Ali Chérif A (2003). Shortlasting, unilateral, neuralgiform headache attacks with conjunctival injection and tearing (SUNCT syndrome) and tumour of the cavernous sinus.Cephalalgia, 23(5):395-7.
    
14. Meunier M., Bachevalier, J. (2002) Comparison of emotional responses in monkeys with rhinal cortex or amygdala lesions. Emotion, 2, 147-161.
15. Simon S., Meunier M., Piettre L., Berardi A., Segebarth C., Boussaoud D. (2002) Spatial attention and memory versus motor preparation: premotor cortex involvement as revealed by fMRI. J. of Neurophysiol., 88: 2047-2057.
16. Boussaoud D. (2001) Attention vs. Intention in the Primate premotor cortex. Neuroimage. 14:S40-45.
17. Bachevalier B., Meunier M. Neurobiology of social-emotional cognition in nonhuman primates. In: The cognitive neuroscience of social behaviour. Eds. A. Easton and N. Emery, Psychology Press. pp 19-58.