(Mis)understanding mirror neurons

This may be a bit technical for many MindBlog readers, but Hickok and Hauser offer a simple, succinct, and incisive critique of the current dogma about mirror neurons that is sufficiently important that I would like to pass it on.  They suggest, as an alternative to the common assumption that mirror neurons are involved in action understanding, that their activity instead might reflect sensory-motor learning. They illustrate this distinction with a simple graphic (in which ventral stream refers to pathways moving more through the temporal lobe of the brain - the 'what' pathway, with dorsal stream routing more through the parietal lobe - the 'where' pathway. Both pathways converge in pre-motor cortical areas such as F5):

Summary
It is hard to imagine a class of neurons that has generated more excitement than mirror neurons, cells discovered by Rizzolatti and colleagues [1] in macaque area F5 that fire both during action execution and action observation. We suggest, however, that the interpretation of mirror neurons as supporting action understanding was a wrong turn at the start, and that a more appropriate interpretation was lying in wait with respect to sensorimotor learning. We make a number of arguments, as follows. Given their previous work, it would have been natural for Rizzolatti's group to interpret mirror neurons as involved in action selection rather than action understanding. They did not make this assumption because, at the time, the data suggested that monkey behavior did not support such an interpretation. Recent evidence shows that monkeys do, in fact, exhibit behaviors that support this alternative interpretation. Thus, the original basis for claiming that mirror neurons mediate action understanding is no longer compelling. There are independent arguments against the action understanding claim and in support of a sensorimotor learning origin for mirror neurons. Therefore, the action understanding theory of mirror neuron function requires serious reconsideration, if not abandonment.
Main Text
Mirror neurons were discovered in the context of research aimed at understanding how the visual properties of objects are integrated with motor codes for action. Cells in area F5 were found to respond to visually presented objects as well as during grasping actions towards those objects. The interpretation of this circuit was that it coded a “vocabulary of motor acts and that this vocabulary can be accessed by … visual stimuli” (p. 491) [2] and that it was critical for “learning associations, including arbitrary associations between stimuli and [motor] schemas” (p. 317) [3]. This is a “‘pragmatic’ mode of processing, the function of which is to extract parameters that are relevant to action, and to generate the corresponding motor commands” (p. 320), as opposed to “‘semantic’ analysis [which is] performed in the temporal lobe” (p.314) [3]. Thus, the meaning of objects is not coded in F5, although clearly, “the semantic system can influence the pragmatic system” (p. 320) [3] (for example, we want to reach for food not snakes).

Mirror neurons were discovered within this same circuit and found to have similar sensorimotor properties [1,4]. It was even suggested that “the actions performed by other monkeys must be a very important factor in determining action selection” (p. 179) [4] and that “the [motor] vocabulary of F5 can be addressed in two ways: by objects and by events [actions]” (p. 317) [3]. Thus, the theoretical and empirical pieces were in place to interpret mirror neurons as sensorimotor association cells relevant to action selection, just like object-oriented cells (Figure 1). But this interpretation was not considered — why?

Figure 1 (click to enlarge)
Schematic models of dorsal and ventral stream function.
(A) The current dominant model [1], which holds that object- and action-oriented processes for sensorimotor integration and ‘understanding’ are organized differentially, with action understanding part of the dorsal sensorimotor stream and object ‘understanding’ part of the ventral stream. (B) A more conventional model in which object- and action-oriented processes for sensory-motor integration and understanding are organized similarly. Both models assume that semantic information from the ventral stream can modulate sensorimotor processes in the dorsal stream.

It was the mirroring property of mirror neurons that steered investigators away from a straightforward sensorimotor interpretation. The logic was, if mirror actions (for example, imitation) are not in the species' repertoire, then mirror neurons can have no motor selection function. Rizzolatti and Craighero used this argument, pitting “two main hypotheses” of mirror neuron function, imitation and action understanding; because macaques do not imitate, they argued, mirror neurons must support action understanding (p. 172) [1]. However, these authors, and the field generally, have failed to notice that other forms of mirror actions are in the macaque motor repertoire. For example, field studies show that rhesus monkeys perceive human gestures as goal-directed, including those that mimic the rhesus monkeys' species-specific signal for coalition recruitment [5]. Macaques also engage in contagious yawning, where perception of another's yawn triggers a yawn in the observer [6]. Further, experimental work has found that another's grasping actions toward one of two food receptacles serves as a cue to goal-directed grasping toward that same receptacle [7] — an experimental situation reminiscent of the mirror neuron studies. Even domesticated dogs mirror goal-directed actions of a model dog [8]; one would expect to find mirror neurons in dogs given this behavioral evidence. And lastly, rhesus monkeys comprehend actions that they are physically incapable of producing. In particular, though rhesus monkeys do not throw, they can recognize a throwing action in humans, realizing that throwing a rock is dangerous whereas throwing food is not [5].

Observed actions can serve as important inputs to action selection, including, but not necessarily limited to, mirror actions. Therefore, the motivating argument for the action understanding theory over a sensorimotor theory (for example [9]) does not hold.

Can we distinguish the sensorimotor and action understanding theories of mirror neurons? Yes: empirical findings favor the sensorimotor account by showing that action understanding and motor system function dissociate [10], that motor actions alone are insufficient to explain action understanding [5], that animals comprehend many actions that they cannot execute [10], and that sensorimotor learning can transform the mirror system [9].

In summary, a sensorimotor theory can explain the response properties of mirror neurons, does so more straightforwardly, and does not suffer the empirical roadblocks of the action understanding theory [5,10]. It is time to reconsider mirror neuron function and the neural basis of action understanding.

References
1 Rizzolatti, G., and Craighero, L. (2004). The mirror-neuron system. Annu. Rev. Neurosci. 27, 169–192.
2 Rizzolatti, G., Camarda, R., Fogassi, L., Gentilucci, M., Luppino, G., and Matelli, M. (1988). Functional organization of inferior area 6 in the macaque monkey. II. Area F5 and the control of distal movements. Exp. Brain Res. 71, 491–507.
3 Jeannerod, M., Arbib, M.A., Rizzolatti, G., and Sakata, H. (1995). Grasping objects: the cortical mechanisms of visuomotor transformation. Trends Neurosci. 18, 314–320.
4 di Pellegrino, G., Fadiga, L., Fogassi, L., Gallese, V., and Rizzolatti, G. (1992). Understanding motor events: a neurophysiological study. Exp. Brain Res. 91, 176–180.
5 Hauser, M., and Wood, J. (2010). Evolving the capacity to understand actions, intentions, and goals. Annu. Rev. Psychol 61, 303–324, C301.
6 Paukner, A., and Anderson, J.R. (2006). Video-induced yawning in stumptail macaques (Macaca arctoides). Biol. Lett. 2, 36–38.
7 Wood, J.N., Glynn, D.D., Phillips, B.C., and Hauser, M.D. (2007). The perception of rational, goal-directed action in nonhuman primates. Science 317, 1402–1405.
8 Range, F., Viranyi, Z., and Huber, L. (2007). Selective imitation in domestic dogs. Curr. Biol. 17, 868–872.
9 Heyes, C. (2010). Where do mirror neurons come from?. Neurosci. Biobehav. Rev. 34, 575–583.
10 Hickok, G. (2009). Eight problems for the mirror neuron theory of action understanding in monkeys and humans. J. Cogn. Neurosci. 21, 1229–1243.