Internal forward models -- New insight or just hype?

In case you haven't noticed, the concept of internal forward models -- an internal prediction about a future event or state -- are all the rage. The concept comes out of the motor control literature where one can find pretty solid evidence that motor control makes use of forward predictions of the sensory consequences of motor commands (e.g., check out the seminal paper by Wolpert, Ghahramani, & Jordan, 1995). These concepts have been extended to speech (e.g., Tourville et al. 2008; van Wassenhove et al., 2005) and there has been a ton of work trying to establish the neural correlates of these networks (e.g., see Golfinopoulos et al. 2009; Shadmehr & Krakauer, 2008), recent work suggesting an association with clinical conditions such as aspects of schizophrenia (Heinks-Maldonado, et al. 2007) and stuttering (Max et al. 2004), and even applications of the concept of high-level cognition such as "thought" (Ito, 2008), as well as applications to social cognition (Wolpert et al. 2003) with links to the mirror system (Miall, 2003).

I'm a big fan of control theory in general and I think there is a lot to be gained by thinking about speech processes in these terms. At the same time, I'm a little uncomfortable with the widespread application of these models. It kind of reminds me of the mirror neuron situation in that a framework for thinking about one problem is generalized to all kinds of situations. I'm also a bit uncomfortable about the assumed tethering between forward models and the motor system. A forward model is just a prediction. In the context of motor control, it makes sense to make predictions (e.g., sensory predictions) based on the likely outcomes of motor commands. But more generally, predictions can come from lots of sources. Perceptual fill-in processes are a kind of forward model: the visual system for example makes predictions about the color and texture of a given portion of the visual scene based on the color and texture around that region. One can predict the consequences of an ocean wave hitting a rock based on past perceptual experiences. So forward models don't have to come from the motor system and there are probably lots of systems and mechanisms that generate predictions (forward models). It is worth having a look at Karniel's (2002) short comment, "Three creatures named 'forward model'" for some cautionary discussion.

So is the internal forward model concept just hype? No, I don't think so. It has already demonstrated its utility in the motor control literature and there are systems in the brain that appear to support motor-related forward models (cerebellum is one, posterior parietal cortex is another). There are some real insights to be gained from this framework in the speech domain as well, but I think there is the danger of over-application of the concept and we need to proceed cautiously.

References

Golfinopoulos, E., Tourville, J.A., and Guenther, F.H. (2009). The integration of large-scale neural network modeling and functional brain imaging in speech motor control. Neuroimage 52, 862-874.

Heinks-Maldonado, T.H., Mathalon, D.H., Houde, J.F., Gray, M., Faustman, W.O., and Ford, J.M. (2007). Relationship of imprecise corollary discharge in schizophrenia to auditory hallucinations. Arch Gen Psychiatry 64, 286-296.

Ito, M. (2008). Control of mental activities by internal models in the cerebellum. Nat Rev Neurosci 9, 304-313.

Karniel, A. (2002). Three creatures named 'forward model'. Neural Networks 15, 305-307.

Max, L., Guenther, F.H., Gracco, V.L., Ghosh, S.S., and Wallace, M.E. (2004). Unstable or insufficiently activated internal models and feedback-biased motor control as sournces of dysfluency: A theoretical model of stuttering. Contemporary Issue in Communication Science and Disorders 31, 105-122.

Miall, R.C. (2003). Connecting mirror neurons and forward models. Neuroreport 14, 2135-2137.

Shadmehr, R., and Krakauer, J.W. (2008). A computational neuroanatomy for motor control. Exp Brain Res 185, 359-381.

Tourville, J.A., Reilly, K.J., and Guenther, F.H. (2008). Neural mechanisms underlying auditory feedback control of speech. Neuroimage 39, 1429-1443.

van Wassenhove, V., Grant, K.W., and Poeppel, D. (2005). Visual speech speeds up the neural processing of auditory speech. Proc Natl Acad Sci U S A 102, 1181-1186.

Wolpert, D., Ghahramani, Z., & Jordan, M. (1995). An internal model for sensorimotor integration Science, 269 (5232), 1880-1882 DOI: 10.1126/science.7569931

Wolpert, D.M., Doya, K., and Kawato, M. (2003). A unifying computational framework for motor control and social interaction. Philos Trans R Soc Lond B Biol Sci 358, 593-602.