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MOTOR Neurophysiological underpinning of planning and predicting upcoming actions

CLAUDIA D. VARGAS Laboratório de Neurobiologia II Instituto de Biofísica Carlos Chagas Filho CAPES Universidade Federal do Rio de Janeiro LABORATÓRIO DE NEUROBIOLOGIA II/IBCCF Gustav Klimt ELIANE VOLCHAN JOAO GUEDES DA FRANCA CLAUDIA D. VARGAS

EQUIPE DE CONTROLE MOTOR EDUARDO MARTINS GHISLAIN SAUNIER MAITE DE MELO RUSSO MARIA LUIZA RANGEL MARCO A. GARCIA PAULA ESTEVES SEBASTIAN HOFLE THIAGO LEMOS VAGNER SA JOSE MAGALHAES MAGNO CADENGUE

COLABORADORES UNISUAM -ERIKA C. RODRIGUES, LAURA ALICE DE OLIVEIRA LABORATORIO DE NEUROANATOMIA CELULAR- CECILIA HEDIN PEREIRA LABORATORIO DE BIOMECANICA/EEFD -LUIS AURELIANO IMBIRIBA DEPTO DE FISIOTERAPIA/ HCUFF-ANA PAULA FONTANA LABORATORIO DE NEUROCIENCIA DO COMPORTAMENTO UFF-MIRTES G. P. FORTES SETOR DE FISIOTERAPIA/HFAG -SOLANGE CANAVARRO LABS- FERNANDA TOVAR MOLL INSTITUTO DE NEUROCIENCIAS DE NATAL/ SIDARTA RIBEIRO-DRAULIO DE ARAUJO NUMEC/USP- ANTONIO GALVES INSTITUT DES SCIENCES COGNITIVES-CNRS ANGELA SIRIGU & KAREN REILLY UNITE PLASTICITE ET MOTRICITE INSERM THIERRY POZZO VALERIA DELLA MAGGIORE-UBA, ARGENTINA THE MOTOR CONTROL GROUP INVESTIGATES

1. INTERACTIONS BETWEEN EMOTION AND ACTION

2. MENTAL SIMULATION OF ACTIONS (S STATES)

3. PREDICTION OF ACTIONS

4. PLASTICITY AFTER CENTRAL AND PERIPHERAL LESIONS THE MOTOR CONTROL GROUP INVESTIGATES

1. INTERACTIONS BETWEEN EMOTION AND ACTION

2. MENTAL SIMULATION OF ACTIONS (S STATES)

3. PREDICTION OF ACTIONS

4. PLASTICITY AFTER CENTRAL AND PERIPHERAL LESIONS MOVEMENTS Sensorimotor transformations occurring in time

Eadweard Muybridge, 1885 Scott, SH (2004) Nature Reviews Neuroscience vol. 5, pp.534-545. PARAMETERS FOR THE MOVEMENT (+ than 600 muscles!) How to represent movements? The curse of dimensionality (Bellman, 1957)

1) MOTOR PROGRAM FORCE, DIRECTION, TRAJECTORY KINEMATICS DYNAMICS

2) FINAL POSITION (GOAL) ANTICIPATING MOVEMENT OUTCOMES

Efferent copy : Von Helmholtz (1821 – 1894)

•High latencies in sensory processing •High noise

•Causal relationships between actions and their consequences

•Dynamic simulation of our body and of the context

•RdReduc tion of movement -proddduced uncert titiainties

•Motor learning

•Modeling of social interactions (predicting other’s mental states)….

A POWERFUL FORMALISM: THE BAYESIAN APPROACH

•The prior contains information about the structured way contexts change over time and how likely a context is before a movement. •Likelihood of a particular context is the probability of the current sensory feedback given that context. INTERNAL MODELS OF ACTION

von Helmholtz, 1867; Sperry, 1950; von Holst, 1954; Jeannerod et al., 1979

Kawato et al., 1987; Jordan and Rumelhart, 1992; Jordan, 1995; Wolpert et al., 1995; Miall and Wolpert, 1996; Wolpert,1997 Summary The brain represents movements through motor programs As we ggpenerate motor commands, we make predictions about their sensory consequences. When actual sen sor y f eedback arriv es, w e in tegr ate our observations with our predictions and form a belief about how our motor commands have affected the state of our body and the world around us.

This is called state estimation. A neurop hys iol ogi cal sub st rat e f or th e predi cti ve syst em? Brodmann’s areas (1907) somatic

autonomic

PHYSIOLOGIC MEASUREMENT OF MOVEMENT

Motor performance Brain imaging

electroencephalography

Transcranial magnetic stimulation Electrophysiological recording Brain imaging PHYSIOLOGIC MEASUREMENT OF MOVEMENT

behavior Tracer injections in the brain The tale of the blind monks examining an elephant , by Itcho Hanabusa. INTERCONNECTED BRAIN REGIONS ASSOCIATED WITH MOVEMENT PRODUCTION ( Bro dmann ’s areas )

Basal ganglia

Cerebellum MOTOR STIMULUS BRAIN RESPONSE

STIMULUS

PARAMETERS MOTOR PLANNING INTENTION ESTIMATES

THE COGNITIVE REVOLUTION ACTION MOTOR COGNITION

Eadweard Muybridge, 1885 Pretended actions, imagined actions, prospective action judgment, action prediction, action observation, action in dreams. Jeannerod, 2001 MOTOR COGNITION

Eadweard Muybridge, 1885 Pretended actions, imagined actions, prospective action judgment, action prediction, action observation, action in dreams. Jeannerod, 2001 (1935-2011) Human frontiers research grant “VISUOMOTOR TRANFORMATION”

In Kandel, 1991 MIRROR NEURONS

Gallese et al., 1996 MIRROR NEURONS IN THE PARIETAL CORTEX

MOTOR VISUAL

Fogassi et al., 2005 SOMATOTOPIC ACTIVATION DURING ATION OBSERVATION

mouth hand feet Buccino et al., 2001 MOTOR RESONANCE

Arbib, 2005 Opening Lecture Kandel E. The Social Brain Final Lecture Rizzolatti G. New Frontiers in mirror neurons research

1.Basic findinggps and concepts in action-ppperception theor y Fogassi L. Monkey mirror neurons Luppino G. Neuroanatomy Hari R. EEG-MEG Iacoboni M. fMRI

2. Emotion and communication Gallese V. , Monkey and humans Decety J. Empathy, Human studies Aglioti S.M. TMS and pain FdiFadiga L. Language Arbib M. Language Evolution Gentilucci M. Humans, Development and TMS

3. Development and evolution Orban G. Comparative cortical organization, Humans vs Monkey Iriki A. Neural substrates of social behavior Mooney R. Birds' Mirror neurons Ferrari P.F. Monkey development, EEG Nathan Fox Development of the mu -thythm in humans Woodward A Human Infant Development Bekkering H. Infant EEG and development of action and intention

4. Theoretical and clinical implications PiPrinz W. IittiImitation Keysers C. Plasticity Ramachandran S.* Plasticity Sinigaglia C. Phylosophical implications Buccino G. Rehabilitation

Coggpnitive development MOTOR Imitation RESONANCE Learning Rehabilitation

Physiological basis of langgguage

Mind reading Empathy AtiAction predi ditiction ?

EXECUTION EXECUTION OBSERVATION START NO MOVEMENT Capes/Cofecub (2002-2006) Angela Sirigu/CNRS

Summary Predicting an upcoming action involves the recruitment of a network of sensorimotor regions, as inferred by the Readiness potential (a marker of motor preparation). Lesions in the posterior parietal cortex but not in the premotor cortex abolish this action prediction marker. These lesions affect the estimation of an upcoming movement.

Vision of movement EXPLORING THE NEURAL BASIS OF CODING WITH POINT LIGHTS DISPLAYS (PLD): KINEMATICS

Marey (1884).

Joh ansson, 1973, de Giese e Pogg io (2003). BRAIN ACTIVITY ASSOCIATED TO THE SIGHT OF BIOLOGICAL MOTION

Saygin et al., 2004 PREDICTING A BIOLOGICAL MOVEMENT DISAPPEARANCE: NEURAL BASIS FOR MOVEMENT PERMANENCE

Umilta et al., 2001

Ba ker et a l., 2001 Papaxanthis et al. (2003) Postural control in cerebellar patients CEREBEL-5 .MOV CEREBEL-3 .MOV

Patient HF

DEFICIT IN PREDICTIVE MODELS? control Miall, 2003, Shadmher et al. 2008, Bastian, 2003, 2010 Cerebellar Control

STS 5 cm STS N

BTS BTS N Summary

Lesions in the cerebellum impair the inference of a complex biological movement in absence of its visual fdbkfeedback A prediction network? Electrophysiological correlates of biological motion permanence in humans Ghis lai n S auni er , Ed uard o F . M arti ns , Elisa C. Dias, J osé MdM. de OliiOliveira , Thierry Pozzo and Claudia D. Vargas

EEG

Capes/Cofecub (2008- 2012 Thierry Pozzo/INSERM

BIOLOGICAL p -v a nnels VS lue Cha

Time (ms) SCRAMBLED

Saunier et al., submitted BIOLOGICAL p -va nnels l aa VS ue Ch

SCRAMBLED Time (ms) BIOLOGICAL p -v a nels

VS lue chan

SCRAMBLED

Time (()ms) Saunier et al., submitted ?

2300

1350 - 1850 3650 - 4150 p-value

Time (ms)

nais a a c Summary There i s a net work of sensori mot or areas i nvol ved i n predicting both an upcoming biological motion and its disappearance. Such automatic mechanism present very early in phylogeny and in infant babies might allow species survival (estimating potential predators in nature!) WHY AVOIDING THE NEW FRENOLOGY

Gustav Klimt ...attr ibuti ng func tion to iso la te d b rai n regi ons i s mi sl eadi ng ...lesions can be localized but not their impairments...

DYNAMICS OF INTERACTIONS IN THE PREDICTIVE BRAIN Daniel Fraiman, Ghislain Saunier, C. Vargas, Antonio Galves SdbNSponsored by Neuromat

Average path length L =1.8 Clustering coefficient C=0.21

Small-world INSTITUTO DE NEUROLOGIA DEOLINDO COUTO ‐ UFRJ

NUCLEO DE PESQUISA EM NEUROFISIOLOGIA DO MOVIMENTO E DA REABILITAÇÃO MOTORA EQUIPE DE CONTROLE DE MOTOR LABORATORIO DE NEUROBIOLOGIA II [email protected] . br