In the early 1990s, a team of neuroscientists at the University of Parma made a surprising discovery: Certain groups of neurons in the brains of macaque monkeys fired not only when a monkey performed an action – grabbing an apple out of a box, for instance – but also when the monkey watched someone else performing that action; and even when the monkey heard someone performing the action in another room.

In short, even though these “mirror neurons” were part of the brain's motor system, they seemed to be correlated not with specific movements, but with specific goals.

Over the next few decades, this “action understanding” theory of mirror neurons blossomed into a wide range of promising speculations. Since most of us think of goals as more abstract than movements, mirror neurons confront us with the distinct possibility that those everyday categories may be missing crucial pieces of the puzzle – thus, some scientists propose that mirror neurons might be involved in feelings of empathy, while others think these cells may play central roles in human abilities like speech.

Some doctors even say they've discovered new treatments for mental disorders by reexamining diseases through the mirror neuron lens. For instance, UCLA's Marco Iacoboni and others have put forth what Iacoboni called the “broken mirror hypothesis” of autism – the idea that malfunctioning mirror neurons are likely responsible for the lack of empathy and theory of mind found in severely autistic people.

Ever since these theories' earliest days, though, sharp criticism has descended on the claims they make. If it turns out that mirror neurons play only auxiliary roles – and not central ones – in action understanding, as many opponents of these claims contend, we may be looking in entirely the wrong place for causes of autism and speech disorders. We could be ignoring potential cures by focusing on a hypothesis that's grown too popular for its own good.

And through it all, the mirror neuron field continues to attract new inquisitive minds. September 2012 marked the first-ever Mirror Neurons: New Frontiers Summit in Erice, Sicily, where researchers championing all sides of the debate gathered to share their findings and hash out their differences.

In the wake of the Summit, I caught up with some of the world's top mirror neuron experts, and asked them to bring me up to date on their latest findings, debates, and discussions. Their insights paint a more subtle, nuanced picture of mirror neurons' role than anyone originally suspected.

Can mirror neurons understand?

There's something strange about the range of actions mirror neurons respond to. They don't respond to pantomimes, or to meaningless gestures, or to random animal sounds. They seem specially tuned to respond to actions with clear goals – whether those actions are perceived through sight, sound, or any other sensory pathway.

This realization led the discoverers of mirror neurons to put forth what they call the “action understanding” hypothesis - that mirror neurons are the neural basis for our ability to understand others' actions. On this hypothesis rests a kingdom: If it's true, Iacoboni may be right that we can treat autism and speech disorders by repairing the human mirror neuron system. But this kingdom's borders have fallen under relentless attack since its very earliest days.

One of the first scientists to question the “action understanding” hypothesis was UC Irvine's Greg Hickok. Though Hickok doesn't dispute the existence of mirror neurons, he's highly skeptical about their supposed central role in empathy, speech, autism and understanding – and he's spent the past 10 years publishing research regarding those doubts.

The question of whether mirror neurons allow us to understand movement gestures, Hickok explains, is only one of the “action understanding” school's unsupported claims – researchers who argue for a mirror neuron-centric model of speech comprehension also bear the burden of proving their claim that the motor system is involved in representing the meaning of action-related language.

What the “action understanding” school originally claimed, Hickok says, was that mirror neurons provide the neural mechanism for attaching meanings to motor actions – but in recent years, many of those same researchers have been leaning away from that claim, and toward the contention that mirror neurons themselves actually encode the meanings of actions. And both of these claims, according to Hickok, remain unsupported by hard evidence.

“Iacoboni and the other 'action understanding' supporters are conflating two logically independent questions,” Hickok explains. “Their original claim was that mirror neurons provide the mechanism for attaching meaning to actions like hand and speech gestures. But the second question – which they conflate with the first – is whether the meanings of actions are coded in motor systems.” In other words, before we can say for sure whether mirror neurons are necessary for understanding others' actions, we first need to establish whether these neurons associate actions with their meanings, code the meanings themselves, or neither.

“It could be that mirror neurons facilitate your understanding a reaching movement,” Hickok adds, “but don’t themselves represent the semantics of the concept 'reach' generally.” In short, even if mirror neurons do enable your brain to access the concept 'reach,' that doesn't mean they themselves are the neurons that encode that concept.

Over the years, Hickok has led several dozen studies that find dissociations between motor control and conceptual understanding. If he's right, and mirror neurons help code movements but not semantic concepts of them, researchers may be looking for the causes of autism and speech disorders in areas that merely reflect, rather than produce, the symptoms – like picking trash out of a creek while ignoring the garbage dump upstream.

Take patients with Broca's aphasia, for instance. These patients, who've suffered severe damage to the motor areas of their brain's left hemisphere, have major trouble joining words into coherent phrases. Ask a person with Broca's aphasia about the last time he visited the hospital, and he'll say something like, “hospital... and ah... Wednesday... Wednesday, nine o'clock... and oh... Thursday... ten o'clock, ah doctors.” Even so, a patient with Broca's aphasia can still understand sentences he hears others say. “If the neural system supporting speech production were critical to speech recognition,” Hickok says, “Broca's aphasia should not exist.”

To use a more familiar example, babies – and, arguably, even dogs – clearly understand the meanings of many words without having the motor ability to say them. By the same token, we can understand the meaning of a verb like “echolocate” without having any understanding of how to perform it.

Thus, Hickok says, “hearing the word 'kiss' activates motor lip systems not because you need lips to understand the action,” but because your previous experiences with the word “kiss” are associated with movements involved in kissing. Mirror neurons, then, don't encode the meaning of the word “kiss” itself; they simply happen to fall downstream of that understanding in your brain's river of associations.

What all this implies, Hickok says, is that “action understanding is clearly not a function of the motor system.” If we want to find the neural correlates of understanding itself, Hickok suggests, we should concentrate our search upstream from the motor cortex, in brain regions like the superior temporal sulcus (STS), which plays a central role in our ability to associate objects with goals – to decide, in other words, what an action or object is “for.”

Not everyone's thrilled by this line of argument, though. “When one looks at the data,” Iacoboni says, “true examples of dissociation between action understanding and action production are very rare.” Action understanding doesn't always require motor-cortex activity, he agrees; but in many instances, mirror neurons do indeed appear to be crucial for it.

For example, patients with damaged motor cortices seem to have trouble placing photos of people's actions in chronological order – though they have no trouble ordering photos of, say, a falling ball. Cases like these, Iacoboni says, argue strongly for mirror neurons' importance in understanding the intentions of other people's actions. This means, he says, that the concepts of “action” and “understanding” need to be integrated into a single model of mirror neuron function – not picked further apart.

But action execution and action understanding fall apart naturally, Hickok contends. “This is evident in the fact that the inability to produce speech following brain damage or in developmental speech disorders, for example, does not cause speech recognition deficits. It is also plainly evident in the fact that we can understand actions that we can’t perform, such as fly, slither, or coil.”

As you may have noticed by now, a specter that's even harder to pin down lurks throughout this whole debate: We have no empirical rubric for action understanding; no experiment that can tell us for sure whether it's happening – because there's no real agreement about what exactly “understanding” is. It's a weirdly recursive question: Understanding implies meaning; and so far, neither Hickok nor his opponents have been able to pin down what “meaning” means in neurological terms. “The fact is, we don't know exactly how semantic understanding is achieved neurally,” Hickok says. “I certainly don't know.”

Does association mean understanding?

It doesn't always take a brand-new discovery to shake up an old debate - sometimes what's needed is a new way of seeing the data. In the mirror neuron debate, that fresh approach comes courtesy of Cecilia Heyes, a professor of psychology at Oxford's All Souls College. At the 2012 New Frontiers Summit, Heyes presented her case for an altogether different approach to studying mirror neuron function. The really important question, she says, isn't whether mirror neurons encode understanding, but whether they qualify as a special class of neuron at all.

Mirror neurons, in Heyes' view, aren't evolved specifically “for” understanding, imitation, or any other purpose – rather, they're simply ordinary motor-cortex neurons that happen to take on special roles as we learn to associate motor actions with sounds, feelings, goals and so on. “Special-purpose mechanisms can be forged by evolution or by learning,” Heyes says – and if we can figure out what makes certain neurons, but not others, take on mirror properties in the first place, we'll be in a much better position to examine what they're up to.

As for the question of whether mirror neurons “do” meaning, association, or both, Heyes thinks it may boil down to how we choose to define “meaning” and “understanding.” “I I don't think it's right to contrast meaning and association,” she says. “In principle, mirror neurons could be a product of associative learning and help us to understand the meaning of actions.” But before we can find that out with a lab experiment, she adds, supporters and defenders of the “action understanding” hypothesis will need to explain what exactly it is that they’re claiming or denying, so we know what we're looking for.

Hickok, for his part, says Heyes' hypothesis actually supports his argument that mirror neurons don't constitute the basis of action understanding – after all, he explains, if mirror neurons associate incoming stimuli with motor responses, why does the concept of “understanding” need to enter the picture at all? “The mirror neuron system links sensory stimuli to the motor system for the control of action,” he says. “It's a system that acts reflexively and adaptively.” So as far as describing mirror neurons' function in terms of sensory-motor association, Hickok says, Heyes is right on the money.

While Iacoboni also agrees that Heyes' hypothesis is reasonable, he cautions that mirror neurons are still a special kind of associative cell: One that's specialized for action-oriented associations. “Why should mirror neurons respond to specific actions,” Iacobini asks, “if they're just learning visuomotor associations?” Why, in other words, do they respond not to just any action-related stimulus, but only to actions that have goals?

And it's on this question of goal-orientedness – and what it implies about the human mind – that the views of Hickok, Heyes, and the Parma school all diverge once again.

Does empathy depend on mirror neurons?

No matter whose side of the debate you're on, Vittorio Gallese cuts an imposing figure. One of the original discoverers of macaque mirror neurons – and a father of the “action understanding” theory – Gallese has spent the past three decades vigorously defending the centrality of mirror neurons in our ability to know what others' actions are “for.”

“The data strongly suggest that mirror neurons map between an observer's goals and the acting animal's motor goals,” Gallese says. These neurons fire in relation to the goal of grasping, he explains, whether it's performed by a hand, a pincer, or another tool; whether it's performed by oneself or another individual; whether the other's movement is seen or merely heard. The only common factor in all these events, Gallese says, is the goal they aim to achieve.

Gallese actually agrees with Hickok that understanding can take place without mirror neuron activation. However, he notes, “only through the activation of mirror neurons can we grasp the meaning of others' behavior from within.” In other words, mirror neurons enable us to understand other people's actions in terms of our own movements and goals – to empathize with them.

Hickok will have none of it. Gallese, he says, is trying to quietly slip out of his original hypothesis that mirror neurons associate meanings with actions, and into a more evasive “claim that they allow 'understanding from the inside,' whatever that means.”

Gallese has an answer at the ready: If not in mirror neurons, then where else should we look for action understanding? Surely not in the STS, as Hickok advocates. “Evidence demonstrates that only the motor system – not the STS – can generalize a motor goal independently from the effector accomplishing it,” Gallese says: When it comes to directly mapping others' motor goals against our own, mirror neurons are still the only serious contenders in town. That kind of perceptual mapping, says Gallese, is what he means by “understanding from the inside.” More work is necessary, he acknowledges, to establish the exact nature of this kind of understanding – but nevertheless, its dependence on mirror neurons is clear.

Iacoboni is somewhat less sanguine. “Admittedly, it is very difficult to obtain empirical evidence that unequivocally proves this hypothesis,” he says – though he's quick to add that “both imaging and neurological evidence are compellingly consistent with it.” The evidence is also consistent, he adds, with the idea that mirror neuron function is significantly altered in people on the autism spectrum of disorders (ASD) – implying a correlation between autism and “broken” mirror neurons.

That may be so, Heyes interjects – but ASD is too complex a range of disorders to lay at the feet of a single malfunctioning neuron system. “Iacoboni doesn't ask,” she says, “whether atypical mirror mechanism activity generates – rather than merely accompanies - autism spectrum disorders.” If, as Hickok contends, mirror neurons lie far downstream in the process of action understanding, this abnormal mirror-neuron activation may simply be another symptom of autism, rather than its cause.

Gallese agrees – partially. “It is very unlikely that autism can be simply equated to a mere malfunctioning of the mirror neuron mechanism,” he says – but nevertheless, “many of the social cognitive impairments manifested by ASD individuals might be rooted in their incapacity to organize and directly grasp the intrinsic goal-related organization of motor behavior.” Mirror neurons map others' motor goals to our own; autistic individuals have trouble grasping others' goals; therefore, Gallese argues, some kind of correlation clearly exists.

But there's an even more serious problem with this line of reasoning, says Morton Ann Gernsbacher, a prominent autism researcher at the The University of Wisconsin-Madison. “It has been repeatedly demonstrated,” Gernsbacher says, “that autistic persons of all ages have no difficulty understanding the intention of other people's actions.” Not only that – decades of research have also shown that autistic people can perform imitation tasks as well as or better than non-autistic participants, and that they can be highly responsive to imitation by others.

And so, once again, we come back to the question of what kind of understanding it is that we're talking about here: Can people with autism really be said to “understand” an action they can't readily imitate it? Gernsbacher says that, obviously, the answer's yes. Gallese would argue that this isn't “understanding from the inside,” but a more abstract kind.

Iacoboni, as usual, takes a more integrative view: “Current theories of empathy suggest a multilayer functional structure, with a core layer of automatic responses to reproduce the affective states of others. Mirror neurons are likely cellular candidates for the core layer of empathy.” And it's that core layer of empathy, Iacobini says, that likely lies at the root of true action understanding.

In the final analysis, the one conclusion that's emerged loud and clear from all these debates is that mirror neurons aren't the end-all of understanding, empathy, autism, or any other brain function. The closer we examine the parts these neurons play, the more we find ourselves peering between the cracks of these mental processes – watching them unravel into threads that run throughout the brain. It may very well turn out that “meaning” and “understanding” aren't single processes at all, but tangled webs of processes involving motor emulation, abstract cognition, and other emotional and instinctual components whose roles we're only beginning to guess.

After decades of research, these strange cells continue to astound and confound us – not only with their unique abilities, but with the hidden complexity to which they may provide a key. But, as so often happens in neuroscience, we may end up having to pick the lock before we understand exactly how the key fits into it.