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Human motor behavior is remarkably accurate and appropriate even though the properties of our own body as well as those of the environment with which we interact vary constantly over time. In order for motor performance to be efficiently organized, both contextual and sensory information have to be assembled and integrated to shape the motor output. Determining how sensory input and motor output are continuously coordinated remains a key problem for the understanding of the flexibility of sensorimotor behavior. Our working model is that the cortical architecture encompasses cognitive processes that are implemented in distributed neuronal networks. To study these questions, we use high-density multi-channel recordings in the cerebral cortex of awake, behaving monkeys.

1. Time Estimation and the Readiness to Go. Timing Processes involved in Movement Preparation

Anticipation of predictable events is crucial for organizing motor performance. It requires an internal representation of elapsed (or remaining) time. The manipulation of temporal aspects of an instructed delay task by systematically varying the delay duration has been shown to efficiently alter the preparatory state of the subject. Consequently, in tasks with multiple and randomly presented delay durations, reaction time decreases with increasing delay duration, as the conditional probability of a GO signal being presented increases (hazard function involved in decisional processes). Additionally, even when the delay duration is held constant across trials, reaction time fluctuates from trial to trial. As time estimation is at the core of anticipatory behavior, this may be related to the imprecision of timing processes. It is not clear, however, if time by itself is represented in the brain as an invariant process, separable from other processes such as movement preparation. Our research aims at identifying signatures of time estimation processes during preparation for action in motor cortical areas of the behaving monkey using multi-electrode recordings of single neuron spiking and local field potential activities. Work in collaboration with Bjørg Kilavik. External collaboration with William A. MacKay, UToronto, Canada.

Related references

Confais J, Kilavik BE, Ponce-Alvarez A, Riehle A (2012) On the anticipatory pre-cue activity in motor cortex. J Neurosci 32 : 15359-15368

Kilavik BE, Ponce-Alvarez A, Trachel R, Confais J, Takerkart S, Riehle A (2012) Context-related frequency modulations of motor cortical LFP beta oscillations. Cereb Cortex 22 : 2148-2159

Kilavik BE, Confais J, Ponce-Alvarez A, Diesmann M, Riehle A (2010) Evoked potentials of motor cortical LFPs reflect task timing and behavioral performance. J Neurophysiol 104 : 2338-2351

Kilavik BE, Riehle A (2010) Timing structures neuronal activity during preparation for action. In : Nobre AC, Coull JT (eds), Attention and Time, Oxford University Press : New York, pp. 257-271

Riehle A, Grammont F, MacKay WA (2006) Cancellation of a planned movement in motor cortex. NeuroReport 17 : 281-285 [Recommended by the Faculty of 1000 Biology : Kalaska J : 2006. F1000.com/1031384]

Roux S, MacKay WA, Riehle A (2006) The pre-movement component of motor cortical local field potentials reflects the level of expectancy. Behav Brain Res 169 : 335-351

Renoult L, Roux S, Riehle A (2006) Time is a rubberband : neuronal activity in monkey motor cortex in relation to time estimation. Eur J Neurosci 23 : 3098-3108

Riehle A (2005) Preparation for action : one of the key functions of motor cortex. In : Riehle A, Vaadia E (eds), Motor cortex in voluntary movements : a distributed system for distributed functions, CRC Press : Boca Raton, FL, pp. 213-240

Roux S, Coulmance M, Riehle A (2003) Context-related representation of timing processes in monkey motor cortex. Eur J Neurosci 18 : 1011-1016

Bastian A, Schöner G, Riehle A (2003) Preshaping and continuous evolution of motor cortical representations during movement preparation. Eur J Neurosci 18 : 2047-2058 [Recommended by the Faculty of 1000 Biology : Kalaska J : 2004. F1000.com/1015847]

Riehle A, Grün S, Diesmann M, Aertsen A (1997) Spike synchronization and rate modulation differentially involved in motor cortical function. Science 278 : 1950-1953

2. Temporal Organization of Cortical Activity and the Concept of Cell Assemblies

The modulation of firing rate and the modulation of neuronal cooperativity in terms of precise spike synchrony (in the millisecond range) suggest that the brain uses different strategies in different contextual situations. During preparation for action, (i) to deal with internal and purely cognitive processes such as expecting an event, increasing motivation or modifying an internal state, motor cortical neurons preferentially synchronize their spike occurrences without necessarily changing their firing rates. In contrast, (ii) when processing external, behaviorally relevant events such as the occurrence of a signal providing prior information and/or cueing the execution of the requested movement, motor cortical neurons mainly modulate their firing rates. Thus, both a temporal code (e.g. precise spike synchrony) and a rate code (firing rate modulation) may serve different and complementary functions, acting in concert at some times and independently at others, depending on the behavioral context. One may consider the temporal code not as an alternative, but rather as an extension to the rate code. Such a combination may allow the extraction of more information from patterns of neuronal activity and thereby increase the dynamics, the flexibility, and the representational strength of a distributed system such as the cerebral cortex. During movement preparation, in motor cortex particularly, abrupt changes in firing rate (transient bursts) are probably deliberately kept to a minimum, if not totally prevented. This could be to prevent accidental activation of downstream motor nuclei. Most often the changes in firing rate are gradual until movement onset. Therefore, during preparation, phasic signalling at a precise time would be preferentially mediated by a temporal code such as transitory spike synchronization, in order to indicate internal events and/or to modify the internal state. Work in collaboration with Bjørg Kilavik. External collaboration with Sonja Grün, FZ Jülich (http://www.fz-juelich.de/inm/inm-6/...).

Related references

Riehle A, Roux S, Kilavik BE, Grün S (2011) Dynamics of motor cortical networks : the complementarity of spike synchrony and firing rate. In : Danion F, Latash ML (eds), Motor Control : Theories, experiments, and applications, Oxford University Press : New York, pp. 141-158

Kilavik BE, Roux S, Ponce-Alvarez A, Confais J, Grün S, Riehle A (2009) Long-term modifications in motor cortical dynamics induced by intensive practice. J Neurosci 29 : 12653-12663

Grün S, Riehle A, Aertsen A, Diesmann M (2003) Temporal scales of cortical interactions. Nova Acta Leopoldina NF 88, Nr. 332 : 189-206

Grün S, Riehle A, Diesmann M (2003) Effect of across trial non-stationarity on joint spike events. Biol Cybern 88 : 335-351

Grammont F, Riehle A (2003) Spike synchronization and firing rate in a population of motor cortical neurons in relation to movement direction and reaction time. Biol Cybern 88 : 360-373

Riehle A, Grammont F, Diesmann M, Grün S (2000) Dynamical changes and temporal precision of synchronized spiking activity in monkey motor cortex during movement preparation. J Physiol (Paris) 94 : 569-582

Grün S, Diesmann M, Grammont F, Riehle A, Aertsen A (1999) Detecting Unitary Events without discretization of time. J Neurosci Meth 94 : 67-79

Grammont F, Riehle A (1999) Precise spike synchronization in monkey motor cortex involved in preparation for movement. Exp Brain Res 128 : 118-122

Riehle A, Grün S, Diesmann M, Aertsen A (1997) Spike synchronization and rate modulation differentially involved in motor cortical function. Science 278 : 1950-1953 [Perspective in Science by : Fetz EE (1997) Temporal coding in neural populations ? Science 278 : 1901-1902]

3. The Dynamics of Motor Cortical Maps. Proximo-Distal Organization

The various spatio-temporal features of proximo-distal movements present many advantages to tackle the complex problem of the cerebral control of movement. We use a 100 electrode Utah array, chronically implanted in monkey motor cortex, to study how proximal and distal motor representations are functionally coupled during preparation and execution of complex movements. This allows us to decipher spatio-temporal network dynamics by relating massively parallel recordings of multiple spiking activities and LFPs to the identified spatial positions of the electrodes and to follow them during days or even weeks. The study of proximo-distal movements provides essential knowledge to understand how sensorimotor control and predictive mechanisms are implemented for voluntary actions. This basic knowledge is critically needed to optimize the real-time decoding of cortical activity in the context of BMI research for the control of robotic hand and arm movements. Work in collaboration with Thomas Brochier. External collaboration with Sonja Grün, FZ Jülich (http://www.fz-juelich.de/inm/inm-6/...).

Related references

Riehle A, Wirtssohn S, Grün S, Brochier B (2013) Mapping the spatio-temporal structure of motor cortical LFP and spiking activities during reach-to-grasp movements. Frontiers Neural Circuits 7 : 48

Brochier T, Zaepffel M, Riehle A (2012) Spatio-temporal structure of beta band oscillations in macaque motor cortex during grasp. Soc Neurosci Abstr 2012

Denker M, Zehl L, Brochier T, Riehle A, Grün S (2012) Spatial organization of synchronized activity expressed by joint spiking and local field potentials in motor cortex. FENS 2012, Barcelona, Spain


  • Brochier T., Zehl L., Hao Y., Duret M., Sprenger J., Denker M., Grün S., et Riehle A. (2018). Massively parallel recordings in macaque motor cortex during an instructed delayed reach-to-grasp task. Scientific Data, 5: 180055.

  • de Haan M.J., Brochier T.G., Grün S., Riehle A., et Barthelemy F.V. (2018). Real-time visuomotor behavior and electrophysiology recording setup for use with humans and monkeys. Journal of Neurophysiology.

  • Denker M., Zehl L., Kilavik B.E., Diesmann M., Brochier T., Riehle A., et Grün S. (2018). LFP beta amplitude is linked to mesoscopic spatio-temporal phase patterns. Scientific Reports, 8.

  • Kilavik B.E., Roux S., Ponce-Alvarez A., Confais J., Grün S., et Riehle A. (2009). Long-term modifications in motor cortical dynamics induced by intensive practice. The Journal of neuroscience: the official journal of the Society for Neuroscience, 29: 12653-12663.

  • Kilavik B.E., Confais J., Ponce-Alvarez A., Diesmann M., et Riehle A. (2010). Evoked potentials in motor cortical local field potentials reflect task timing and behavioral performance. Journal of neurophysiology, 104: 2338-2351.

  • Kilavik B.E., Ponce-Alvarez A., Trachel R., Confais J., Takerkart S., et Riehle A. (2012). Context-related frequency modulations of macaque motor cortical LFP beta oscillations. Cerebral cortex (New York, N.Y.: 1991), 22: 2148-2159.

  • Kilavik B.E., Zaepffel M., Brovelli A., MacKay W.A., et Riehle A. (2013). The ups and downs of β oscillations in sensorimotor cortex. Experimental Neurology, 245: 15-26.

  • Milekovic T., Truccolo W., Grün S., Riehle A., et Brochier T. (2015). Local field potentials in primate motor cortex encode grasp kinetic parameters. NeuroImage, 114: 338-355.

  • Riehle A., Wirtssohn S., Grün S., et Brochier T. (2013). Mapping the spatio-temporal structure of motor cortical LFP and spiking activities during reach-to-grasp movements. Frontiers in Neural Circuits, 7.
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