Humans can guide their actions toward the realization of their intentions. Flexible, rapid and precise realization of intentions and goals relies on the brain learning to control its actions on external objects and to predict the consequences of this control. Neural mechanisms that mimic the input–output properties of our own body and other objects can be used to support prediction and control, and such mechanisms are called internal models. We first summarize functional neuroimaging, behavioral and computational studies of the brain mechanisms related to acquisition, modular organization, and the predictive switching of internal models mainly for tool use. These mechanisms support predictive control and flexible switching of intentional actions. We then review recent studies demonstrating that internal models are crucial for the execution of not only immediate actions but also higher-order cognitive functions, including optimization of behaviors toward long-term goals, social interactions based on prediction of others’ actions and mental states, and language processing. These studies suggest that a concept of internal models can consistently explain the neural mechanisms and computational principles needed for fundamental sensorimotor functions as well as higher-order cognitive functions.
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Baron-Cohen, S. (1997). Mindblindness: An essay on autism and theory of mind (learning, development and conceptual change). Cambridge: MIT Press.
Blakemore, S. J., & Decety, J. (2001). From the perception of action to the understanding of intention. Nature Reviews Neuroscience, 2(8), 561–567.
Blakemore, S. J., Frith, C. D., & Wolpert, D. M. (2001). The cerebellum is involved in predicting the sensory consequences of action. Neuroreport, 12(9), 1879–1884.
Blakemore, S. J., Wolpert, D. M., & Frith, C. D. (1998). Central cancellation of self-produced tickle sensation. Nature Neuroscience, 1(7), 635–640.
Bonda, E., Petrides, M., Ostry, D., & Evans, A. (1996). Specific involvement of human parietal systems and the amygdala in the perception of biological motion. Journal of Neuroscience, 16(11), 3737–3744.
Brashers-Krug, T., Shadmehr, R., & Bizzi, E. (1996). Consolidation in human motor memory. Nature, 382(6588), 252–255.
Bursztyn, L. L., Ganesh, G., Imamizu, H., Kawato, M., & Flanagan, J. R. (2006). Neural correlates of internal-model loading. Current Biology, 16(24), 2440–2445.
Clower, D. M., West, R. A., Lynch, J. C., & Strick, P. L. (2001). The inferior parietal lobule is the target of output from the superior colliculus, hippocampus, and cerebellum. Journal of Neuroscience, 21(16), 6283–6291.
Daw, N. D., Niv, Y., & Dayan, P. (2005). Uncertainty-based competition between prefrontal and dorsolateral striatal systems for behavioral control. Nature Neuroscience, 8(12), 1704–1711.
Decety, J., Jackson, P. L., Sommerville, J. A., Chaminade, T., & Meltzoff, A. N. (2004). The neural bases of cooperation and competition: An fMRI investigation. Neuroimage, 23(2), 744–751.
Diedrichsen, J., Criscimagna-Hemminger, S. E., & Shadmehr, R. (2007). Dissociating timing and coordination as functions of the cerebellum. Journal of Neuroscience, 27(23), 6291–6301.
Doya, K. (1999). What are the computations of the cerebellum, the basal ganglia and the cerebral cortex? Neural Networks, 12(7–8), 961–974.
Doya, K. (2000). Complementary roles of basal ganglia and cerebellum in learning and motor control. Current Opinion in Neurobiology, 10(6), 732–739.
Doya, K., Okada, G., Ueda, K., Okamoto, Y., & Yamawaki, S. (2001). Pediction of short- and long-term reward: A functional MRI study with a Markov decision problem. Paper presented at the Annual Meeting Society for Neuroscience.
Ebner, T. J., & Pasalar, S. (2008). Cerebellum predicts the future motor state. Cerebellum, 7(4), 583–588.
Flanagan, J. R., Nakano, E., Imamizu, H., Osu, R., Yoshioka, T., & Kawato, M. (1999). Composition and decomposition of internal models in motor learning under altered kinematic and dynamic environments. Journal of Neuroscience, 19(20), RC34.
Flanagan, J. R., & Wing, A. M. (1997). The role of internal models in motion planning and control: Evidence from grip force adjustments during movements of hand-held loads. Journal of Neuroscience, 17(4), 1519–1528.
Friederici, A. D., Bahlmann, J., Heim, S., Schubotz, R. I., & Anwander, A. (2006). The brain differentiates human and non-human grammars: Functional localization and structural connectivity. Proceedings of the National Academy of Sciences of the USA, 103(7), 2458–2463.
Friston, K. J., Harrison, L., & Penny, W. (2003). Dynamic causal modelling. Neuroimage, 19, 1273–1302.
Frith, C. D., Blakemore, S. J., & Wolpert, D. M. (2000). Abnormalities in the awareness and control of action. Philosophical Transactions of the Royal Society of London Series B Biological Sciences, 355(1404), 1771–1788.
Frith, C. D., & Frith, U. (1999). Interacting minds—A biological basis. Science, 286(5445), 1692–1695.
Gallese, V., Fadiga, L., Fogassi, L., & Rizzolatti, G. (1996). Action recognition in the premotor cortex. Brain, 119(Pt 2), 593–609.
Gandolfo, F., Mussa-Ivaldi, F. A., & Bizzi, E. (1996). Motor learning by field approximation. Proceedings of the National Academy of Sciences of the USA, 93(9), 3843–3846.
Ghahramani, Z., & Wolpert, D. M. (1997). Modular decomposition in visuomotor learning. Nature, 386(6623), 392–395.
Gomi, H., Shidara, M., Takemura, A., Inoue, Y., Kawano, K., & Kawato, M. (1998). Temporal firing patterns of purkinje cells in the cerebellar ventral paraflocculus during ocular following responses in monkeys I. Simple spikes (in process citation). Journal of Neurophysiology, 80(2), 818–831.
Graydon, F. X., Friston, K. J., Thomas, C. G., Brooks, V. B., & Menon, R. S. (2005). Learning-related fMRI activation associated with a rotational visuo-motor transformation. Brain Research Cognitive Brain Research, 22, 373–383.
Grodd, W., Hulsmann, E., Lotze, M., Wildgruber, D., & Erb, M. (2001). Sensorimotor mapping of the human cerebellum: fMRI evidence of somatotopic organization. Human Brain Mapping, 13(2), 55–73.
Haruno, M., & Kawato, M. (in press). Activity in the superior temporal sulcus highlights learning competence in an interaction game. Journal of Neuroscience.
Haruno, M., Kuroda, T., Doya, K., Toyama, K., Kimura, M., Samejima, K., et al. (2004). A neural correlate of reward-based behavioral learning in caudate nucleus: A functional magnetic resonance imaging study of a stochastic decision task. Journal of Neuroscience, 24(7), 1660–1665.
Haruno, M., Wolpert, D. M., & Kawato, M. (2001). Mosaic model for sensorimotor learning and control. Neural Computation, 13(10), 2201–2220.
Hauser, M. D., Chomsky, N., & Fitch, W. T. (2002). The faculty of language: What is it, who has it, and how did it evolve? Science, 298(5598), 1569–1579.
Higuchi, S., Imamizu, H., Chaminade, T., & Kawato, M. (2004). Broca’s area during tool—use and linguistic processing. Paper presented at the Annual Meeting Society for Neuroscience.
Higuchi, S., Imamizu, H., & Kawato, M. (2007). Cerebellar activity evoked by common tool-use execution and imagery tasks: An fMRI study. Cortex, 43(3), 350–358.
Hoshi, E., Tremblay, L., Feger, J., Carras, P. L., & Strick, P. L. (2005). The cerebellum communicates with the basal ganglia. Nature Neuroscience, 8(11), 1491–1493.
Hurley, S. (2008). The shared circuits model (SCM): How control, mirroring, and simulation can enable imitation, deliberation, and mindreading. The Behavioral and Brain Sciences, 31(1), 1–22. (discussion 22–58).
Iacoboni, M., Koski, L. M., Brass, M., Bekkering, H., Woods, R. P., Dubeau, M. C., et al. (2001). Reafferent copies of imitated actions in the right superior temporal cortex. Proceedings of the National Academy of Sciences of the USA, 98(24), 13995–13999.
Imamizu, H., Higuchi, S., Toda, A., & Kawato, M. (2007a). Reorganization of brain activity for multiple internal models after short but intensive training. Cortex, 43(3), 338–349.
Imamizu, H., & Kawato, M. (2008). Neural correlates of predictive and postdictive switching mechanisms for internal models. Journal of Neuroscience, 28(42), 10751–10765.
Imamizu, H., Kuroda, T., Miyauchi, S., Yoshioka, T., & Kawato, M. (2003). Modular organization of internal models of tools in the human cerebellum. Proceedings of the National Academy of Sciences of the USA, 100(9), 5461–5466.
Imamizu, H., Kuroda, T., Yoshioka, T., & Kawato, M. (2004). Functional magnetic resonance imaging examination of two modular architectures for switching multiple internal models. Journal of Neuroscience, 24(5), 1173–1181.
Imamizu, H., Miyauchi, S., Tamada, T., Sasaki, Y., Takino, R., Putz, B., et al. (2000). Human cerebellar activity reflecting an acquired internal model of a new tool. Nature, 403(6766), 192–195.
Imamizu, H., Sugimoto, N., Osu, R., Tsutsui, K., Sugiyama, K., Wada, Y., et al. (2007b). Explicit contextual information selectively contributes to predictive switching of internal models. Experimental Brain Research, 181(3), 395–408.
Ito, M. (1984). The cerebellum and neural motor control. New York: Raven Press.
Jacobs, R. A., Jordan, M. I., Nowlan, S. J., & Hinton, G. E. (1991). Adaptive mixture of local experts. Neural Computation, 3, 79–87.
Johansson, R. S., & Westling, G. (1988). Coordinated isometric muscle commands adequately and erroneously programmed for the weight during lifting task with precision grip. Experimental Brain Research, 71(1), 59–71.
Karniel, A., & Mussa-Ivaldi, F. A. (2002). Does the motor control system use multiple models and context switching to cope with a variable environment? Experimental Brain Research, 143(4), 520–524.
Kawato, M. (1999). Internal models for motor control and trajectory planning. Current Opinion in Neurobiology, 9(6), 718–727.
Kawato, M., Furukawa, K., & Suzuki, R. (1987). A hierarchical neural-network model for control and learning of voluntary movement. Biological Cybernetics, 57(3), 169–185.
Kawato, M., Kuroda, T., Imamizu, H., Nakano, E., Miyauchi, S., & Yoshioka, T. (2003). Internal forward models in the cerebellum: fMRI study on grip force and load force coupling. Progress in Brain Research, 142, 171–188.
Kawato, M., & Samejima, K. (2007). Efficient reinforcement learning: Computational theories, neuroscience and robotics. Current Opinion in Neurobiology, 17(2), 205–212.
Kawawaki, D., Shibata, T., Goda, N., Doya, K., & Kawato, M. (2006). Anterior and superior lateral occipito-temporal cortex responsible for target motion prediction during overt and covert visual pursuit. Neuroscience Research, 54(2), 112–123.
Kerns, J. G., Cohen, J. D., MacDonald, A. W., 3rd, Cho, R. Y., Stenger, V. A., & Carter, C. S. (2004). Anterior cingulate conflict monitoring and adjustments in control. Science, 303(5660), 1023–1026.
Kitazawa, S., Kimura, T., & Yin, P. B. (1998). Cerebellar complex spikes encode both destinations and errors in arm movements. Nature, 392(6675), 494–497.
Krakauer, J. W., Ghilardi, M. F., & Ghez, C. (1999). Independent learning of internal models for kinematic and dynamic control of reaching. Nature Neuroscience, 2(11), 1026–1031.
Krakauer, J. W., Ghilardi, M. F., Mentis, M., Barnes, A., Veytsman, M., Eidelberg, D., et al. (2004). Differential cortical and subcortical activations in learning rotations and gains for reaching: A PET study. Journal of Neurophysiology, 91(2), 924–933.
Kravitz, J. H., & Yaffe, F. L. (1972). Conditionned adaptation to prismatic displacement with a tone as the conditioal stimulus. Perception & Psychophysics, 12(3), 305–308.
Maquet, P., Schwartz, S., Passingham, R., & Frith, C. (2003). Sleep-related consolidation of a visuomotor skill: Brain mechanisms as assessed by functional magnetic resonance imaging. Journal of Neuroscience, 23(4), 1432–1440.
Martin, A., & Chao, L. L. (2001). Semantic memory and the brain: Structure and processes. Current Opinion in Neurobiology, 11(2), 194–201.
Miall, R. C. (2003). Connecting mirror neurons and forward models. Neuroreport, 14(17), 2135–2137.
Miall, R. C., Keating, J. G., Malkmus, M., & Thach, W. T. (1998). Simple spike activity predicts occurrence of complex spikes in cerebellar Purkinje cells. Nature Neuroscience, 1(1), 13–15.
Miall, R. C., Reckess, G. Z., & Imamizu, H. (2001). The cerebellum coordinates eye and hand tracking movements. Nature Neuroscience, 4(6), 638–644.
Miall, R. C., Weir, D. J., Wolpert, D. M., & Stein, J. F. (1993). Is the cerebellum a Smith predictor? Journal of Motor Behavior, 25, 203–216.
Middleton, F. A., & Strick, P. L. (1997). Dentate output channels: Motor and cognitive components. In C. I. de Zeeuw, P. Strata, & J. Voogd (Eds.), The cerebellum: From structure to control (pp. 553–566). Amsterdam: Elsevier Science BV.
Middleton, F. A., & Strick, P. L. (2001). Cerebellar projections to the prefrontal cortex of the primate. Journal of Neuroscience, 21(2), 700–712.
Milner, T. E., Franklin, D. W., Imamizu, H., & Kawato, M. (2007). Central control of grasp: Manipulation of objects with complex and simple dynamics. Neuroimage, 36(2), 388–395.
Obayashi, S., Suhara, T., Kawabe, K., Okauchi, T., Maeda, J., Akine, Y., et al. (2001). Functional brain mapping of monkey tool use. Neuroimage, 14(4), 853–861.
O’Reilly, J. X., Mesulam, M. M., & Nobre, A. C. (2008). The cerebellum predicts the timing of perceptual events. Journal of Neuroscience, 28(9), 2252–2260.
Osu, R., Hirai, S., Yoshioka, T., & Kawato, M. (2004). Random presentation enables subjects to adapt to two opposing forces on the hand. Nature Neuroscience, 7(2), 111–112.
Oztop, E., Kawato, M., & Arbib, M. (2006). Mirror neurons and imitation: A computationally guided review. Neural Network, 19(3), 254–271.
Oztop, E., Wolpert, D., & Kawato, M. (2005). Mental state inference using visual control parameters. Brain Research Cognitive Brain Research, 22(2), 129–151.
Raichle, M. E., Fiez, J. A., Videen, T. O., MacLeod, A. M., Pardo, J. V., Fox, P. T., et al. (1994). Practice-related changes in human brain functional anatomy during nonmotor learning. Cerebral Cortex, 4(1), 8–26.
Sakai, K. L. (2005). Language acquisition and brain development. Science, 310(5749), 815–819.
Sasaki, K., Oka, H., Kawaguchi, S., Jinnai, K., & Yasuda, T. (1977). Mossy fibre and climbing fibre responses produced in the cerebellar cortex by stimulation of the cerebral cortex in monkeys. Experimental Brain Research, 29(3–4), 419–428.
Schmid, A., Rees, G., Frith, C., & Barnes, G. (2001). An fMRI study of anticipation and learning of smooth pursuit eye movements in humans. Neuroreport, 12(7), 1409–1414.
Schultz, W., Apicella, P., & Ljungberg, T. (1993). Responses of monkey dopamine neurons to reward and conditioned stimuli during successive steps of learning a delayed response task. Journal of Neuroscience, 13(3), 900–913.
Schultz, J., Imamizu, H., Kawato, M., & Frith, C. D. (2004). Activation of the human superior temporal gyrus during observation of goal attribution by intentional objects. Journal of Cognitive Neuroscience, 16(10), 1695–1705.
Shadmehr, R., & Holcomb, H. H. (1997). Neural correlates of motor memory consolidation. Science, 277(5327), 821–825.
Shidara, M., Kawano, K., Gomi, H., & Kawato, M. (1993). Inverse-dynamics model eye movement control by Purkinje cells in the cerebellum. Nature, 365(6441), 50–52.
Sutton, R. S., & Barto, A. G. (1998). Reinforcement learning. Cambridge, MA: MIT Press.
Tamada, T., Miyauchi, S., Imamizu, H., Yoshioka, T., & Kawato, M. (1999). Cerebro-cerebellar functional connectivity revealed by the laterality index in tool-use learning. Neuroreport, 10(2), 325–331.
Tankersley, D., Stowe, C. J., & Huettel, S. A. (2007). Altruism is associated with an increased neural response to agency. Nature Neuroscience, 10(2), 150–151.
Wolpert, D. M., Doya, K., & Kawato, M. (2003). A unifying computational framework for motor control and social interaction. Philosophical Transactions of the Royal Society of London Series B Biological Sciences, 358(1431), 593–602.
Wolpert, D. M., Ghahramani, Z., & Jordan, M. I. (1995). An internal model for sensorimotor integration. Science, 269(5232), 1880–1882.
Wolpert, D. M., & Kawato, M. (1998). Multiple paired forward and inverse models for motor control. Neural Networks, 11, 1317–1329.
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Imamizu, H., Kawato, M. Brain mechanisms for predictive control by switching internal models: implications for higher-order cognitive functions. Psychological Research 73, 527–544 (2009). https://doi.org/10.1007/s00426-009-0235-1
- Functional Connectivity
- Internal Model
- Grip Force
- Inferior Parietal Lobule
- Superior Parietal Lobule