Mirror neurons do not resonate with actions: two pieces of single-unit evidence

Gergley Csibra (2007) noticed a fundamental flaw in the logic of the mirror neuron theory of action understanding:

[there is] a tension between two conflicting claims about action mirroring implied by the direct-matching hypothesis: the claim that action mirroring reflects low-level resonance mechanisms, and the claim that it reflects high-level action understanding. The tension arises from the fact that the more it seems that mirroring is nothing else but faithful duplication of observed actions, the less evidence it provides for action understanding; and the more mirroring represents high-level interpretation of the observed actions, the less evidence it provides that this interpretation is generated by low-level motor duplication.  

Csibra's tension is evident in two famous and influential monkey mirror neuron studies by the Parma group.  In one, Umilta et al. 2001, mirror neurons were shown to fire during the observation of object-directed actions even when the object was hidden from view during the actual reaching (it was shown to the monkey before being hidden).  These same cells tended not to fire when there was no object behind the occluding screen (an empty platform was shown to the monkey).  The result was interpreted as evidence that mirror neurons are responding to the meaning or goal of the action, not the action itself. They write,

In order to activate the neurons in the hidden condition, two requirements need to be met: the monkey must “know” that there is an object behind the occluder and must see the hand of the experimenter disappearing behind the occluder. It appears therefore that the mirror neurons responsive in the hidden condition are able to generate a motor representation of an observed action, not only when the monkey sees that action, but also when it knows its outcome without seeing its most crucial part (i.e., hand-object interaction).

But if the monkey already knows the outcome, what is the point of simulating it with a motor response?  Note that the action, the movement itself, is the same in both cases.  What causes the mirror neurons to fire, then, is not the movement, but the presence or absence of the object (in the monkey's memory).  It is not a simple resonance.

The other experiment is even more famous, the report on parietal lobe mirror neurons in Science by Fogassi, et al. 2005. In this experiment, monkeys observed an experimenter reaching for an object and either bringing it to the mouth or placing it in a container. The figure here, from a 2006 Scientific American piece by Rizzolatti, shows a schematic of the set up:

The figure shows the response of a grasping-to-eat mirror neuron responding both when the monkey performs the action (1) and when he observes the action (2).  Notice, though, the the point in time when the cell starts firing during observation: it is during the reach toward the object, prior to the grasp (the red line=moment of grasp).  This is puzzling because the reach toward the object is identical in both conditions.  Only the subsequent movement, bringing to mouth or placing in container, distinguishes the action. How could the mirror neuron know ahead of time?  Is it mystically reading the mind of the experimenter?  Not at all.  

The figure is actually misleading.  If you look in the online supplemental material of the original report in Science you find this:

The container was present only in the trials in which the grasped object was subsequently placed into it. The presence of the container acted as a cue allowing the monkey to predict the most likely subsequent motor act.

It was the visual context that told the monkey ahead of time what was going to happen.  So again like the occlusion study, what determines mirror neuron activity is not the action itself but the monkey's broader understanding of the action context.  

Monkeys do not understanding because their motor system resonates with observed actions. The motor system resonates with observed actions because the monkey understands already what's going to happen.  

References

Csibra, G. (2007). Action mirroring and action understanding: An alternative account. In P. Haggard, Y. Rosetti & M. Kawato (Eds.), Sensorimotor foundations of higher cognition. Attention and Performance XII (pp. 453-459). Oxford: Oxford University Press. 

Fogassi, L., Ferrari, P. F., Gesierich, B., Rozzi, S., Chersi, F., & Rizzolatti, G. (2005). Parietal lobe: from action organization to intention understanding. Science, 308(5722), 662-667.

Hickok, G. (2014). The Myth of Mirror Neurons. New York: Norton

Umiltà, M., Kohler, E., Gallese, V., Fogassi, L., Fadiga, L., Keysers, C., & Rizzolatti, G. (2001). I know what you are doing. a neurophysiological study. Neuron, 31, 155-165. 

Aphasia and the brain: from syndromes to symptoms to computations

For the first 100 years of modern aphasia research (~since the 1860s) the focus was mainly on syndromes: motor (Broca's) aphasia, sensory (Wernicke's) aphasia, conduction aphasia, and so on.  Things changed after the Cognitive... er, make that the Information Processing Revolution (see discussion here or here) when symptoms came more into focus.  The symptom approach was an important advance and is still dominant, as the popular method, voxel-based lesion-symptom mapping (VLSM), highlights.

But mapping symptoms isn't the goal.  What we are really after are the computations that underlie the symptoms. Recent work by Gary Dell and colleagues suggests that this might be possible using what they call, voxel-based lesion parameter mapping (VLPM). The basic idea is this. Start with an explicit computational model of the process of interest; Dell et al. use the two-step naming model. Collect data on the symptoms in brain injured patients; for Dell et al, this is the distribution of types of naming errors. Adjust the parameters of your model to fit each patient's error pattern; semantic and phonological weights in the Dell model.  Then run your voxel-based analysis using the parameter values as your dependent measure instead of say error rate.  And it actually works.  To the extent that the model is a reasonable approximation to what's going on in the wetware (no model is "right" of course), you are now mapping computations.  Pretty cool.  All we need now is to improve our models.

Dell, G. S., Schwartz, M. F., Nozari, N., Faseyitan, O., & Branch Coslett, H. (2013). Voxel-based lesion-parameter mapping: Identifying the neural correlates of a computational model of word production. Cognition, 128(3), 380-396. doi: 10.1016/j.cognition.2013.05.007

The right theory of mirror neuron function. Guess who said it.

A quote on mirror neuron function.  I think it is spot on, as discussed in The Myth of Mirror Neurons.  Who said it? (It wasn't me.)

One of the fundamental functions of the premotor cortex is that of retrieving appropriate motor acts in response to sensory stimuli. Evidence has been provided that action retrieval can occur in response to two-dimensional patterns, color, and size and shape of three-dimensional objects. The present data indicate that in addition to these physical factors, retrieval can also occur in response to the meaning of the gestures made by other individuals. If one considers the rich social interactions within a monkey group, the understanding by a monkey of actions performed by other monkeys must be a very important factor in determining action selection. Thus, the capacity of inferior premotor neurons to select actions according to gesture meanings fits well in the conceptual framework of current theory on the functions of premotor cortex and expands it to include movement selection related to interpersonal relations.

Two tenure-track jobs at SDSU

We are writing to let you know of two tenure/tenure-track positions for Fall 2015 that we are currently conducting in the School of Speech, Language and Hearing Sciences at San Diego State University. 

Language Clinical Scientist, Bilingual emphasis,  Assistant Professor (Dr. Sonja Pruitt, Search Chair)

Tenure-track position in Bilingualism and Language Science. Required: Ph.D. in Language Science and Disorders or related field, excellence in teaching, strong research abilities, and commitment to students from diverse backgrounds. Preferred: CCC-SLP and eligibility for California licensure.  Responsibilities: undergraduate and graduate (MA/Ph.D.) teaching, supervising theses/dissertations and pursuing a research program.

Brain–based disorders and neuroplasticity, Associate Professor (Dr. Tracy Love, Search Chair)

Tenure-track position in brain-based disorders of speech, language, or cognitive processing, with adult and/or child populations, and with neuroplasticity as one focus.  Required: Ph.D. in Communication Sciences and Disorders, Linguistics, Psychology, Neurosciences or a related field, excellence in teaching, strong research abilities, and commitment to students from diverse backgrounds. Responsibilities: undergraduate and graduate (MA/Ph.D.) teaching, supervising theses/dissertations and pursuing a research program in specialty area.

Details for both positions can be found on our website (http://slhs.sdsu.edu/open-positions/)

Job announcement: Department Head, Communication Sciences & Disorders (CSD), Penn State

Department Head, Communication Sciences & Disorders (CSD)

The Pennsylvania State University

Work Unit: College of Health & Human Development

Department: Communication Sciences & Disorders

Job Number: 52263

Date Announced: July 9, 2014

The Department of Communication Sciences and Disorders (CSD), College of Health and Human Development (HHD), at The Pennsylvania State University, invites applications for the position of Department Head to begin Fall 2015. Penn State seeks an innovative and energetic leader to build upon the existing strengths of this nationally and internationally acclaimed department.

The Department Head is expected to be a leader who promotes excellence in the full range of missions that are embodied at a comprehensive, land-grant and research intensive university such as Penn State. As a key academic leader, and in keeping with the strategic initiatives of the University and the College, the Department Head must have the ability to stimulate and facilitate research productivity, encourage interdisciplinary research, and promote and assist faculty with securing external funds to fulfill the mission of the department. The Department Head must also expand upon the current strengths of the faculty by identifying and facilitating new opportunities in undergraduate, graduate, and on-line education.

The CSD Department has a long history of tradition and excellence, and has consistently ranked in the top 10% of the communication sciences and disorders programs in the nation. Further information about the College of HHD and the Department of CSD can be found at: http://www.hhdev.psu.edu/

Qualifications: Earned doctorate; evidence of an active, focused program of research in speech, language, or hearing, or a related field; previous college teaching and administrative experience; and be eligible for appointment as a full tenured professor at The Pennsylvania State University. CCC-SLP or CCC-A certification is preferred. Significant leadership experience in a university setting, including coordination and fiscal management of department programs, is highly desirable.

Application procedures: Review of applications and nominations will begin immediately and continue until a suitable candidate is found. Candidates must apply on-line by going to the PSU Jobs Website at: https://app2.ohr.psu.edu/Jobs/External/EVMS2_External/currentap1.cfm#52263

Candidates should be prepared to provide contact information (name, address, phone number and email address) for three professional references upon request. References will not be contacted without the consent of the candidate. Direct questions to: Kathryn Drager, Ph.D., CCC-SLP, CSD Search Committee Chair, Interim Associate Dean for Research and Graduate Education, College of Health and Human Development, University Park, PA 16802-1307, 814-863-2426, or kdd5@psu.edu. Please indicate CSD Department Head Search in the subject line of email correspondence. All inquiries will be held in confidence and all applications will be held in confidence until finalists are invited to the University Park campus.

We encourage applications from individuals of diverse backgrounds. We are supportive of dual career situations.

CAMPUS SECURITY CRIME STATISTICS: For more about safety at Penn State, and to review the Annual Security Report which contains information about crime statistics and other safety and security matters, please go to http://www.police.psu.edu/clery/ , which will also provide you with detail on how to request a hard copy of the Annual Security Report.
Penn State is an equal opportunity, affirmative action employer, and is committed to providing employment opportunities to minorities, women, veterans, disabled individuals, and other protected groups.

Clarifying the auditory dorsal stream, again: a comment on Rauschecker 2014

Josef Rauschecker has a new paper out in Frontiers titled, "Is there a tape recorder in your head? How the brain stores and retrieves melodies." It's worth a look.  The problem of coding sequences of information is an important, and poorly understood one.

But that's not I want to highlight here.  Instead I want to put some comments of Rauschecker's in their proper context, i.e., the context of the neuroscience of hearing that exists outside of his laboratory. He writes,  

The dorsal stream was originally defined by its involvement in auditory spatial processing (Rauschecker and Tian, 2000) and movement in space (Warren et al., 2002). This is still believed to be correct (Rauschecker, 2012), but the role of the dorsal stream has been expanded to include sensorimotor integration and control in more general terms (Rauschecker and Scott, 2009; Rauschecker, 2011), including the representation of sequences.

As I pointed out in this post, the idea of dual streams in auditory processing pre-date Rauschecker and Tian by at least a half a century, and can trace their route back even farther to Carl Wernicke who argued for the existence of two auditory pathways, one that projects to the motor system and on that projects to the conceptual system.

Secondly, the idea that the dorsal auditory stream processes spatial information has been questioned and re-questioned by the likes of Robert Zatorre, John Middlebrooks, as well as by work in my own lab headed by former grad student Kevin Smith.  A discussion of why, from a purely conceptual standpoint, "spatial processing" cannot possibly be a "stream" can be found in this review by Hickok & Saberi.  To summarize our point, streams are organized around computational tasks (what you do with information) not around information types.  So "This is still believed to be correct" is better stated as, "This is still believed to be correct, by Rauschecker."

Good to see, though, that Rauschecker has correctly acknowledged the "expansion" of the role of the dorsal stream to include sensorimotor integration.  I'm sure his omission of Hickok & Poeppel, 2000, 2004, 2007, Wise et al. 2001, Buchsbaum et al. 2001, Hickok et al. 2003, 2009, 2011, Pa & Hickok, 2008, Isenberg et al. 2012, to name few, was a merely a proofing error.

The rest of the references for Rauschecker 2014:

Buchsbaum, B., Hickok, G., & Humphries, C. (2001). Role of Left Posterior Superior Temporal Gyrus in Phonological Processing for Speech Perception and Production. Cognitive Science, 25, 663-678. 

Hickok, G., & Poeppel, D. (2000). Towards a functional neuroanatomy of speech perception. Trends Cogn Sci, 4, 131-138. 

Hickok, G., & Poeppel, D. (2004). Dorsal and ventral streams: A framework for understanding aspects of the functional anatomy of language. Cognition, 92, 67-99. 

Hickok, G., & Poeppel, D. (2007). The cortical organization of speech processing. Nature Reviews Neuroscience, 8(5), 393-402. 

Hickok, G., Buchsbaum, B., Humphries, C., & Muftuler, T. (2003). Auditory-motor interaction revealed by fMRI: Speech, music, and working memory in area Spt. Journal of Cognitive Neuroscience, 15, 673-682. 

Hickok, G., Okada, K., & Serences, J. T. (2009). Area Spt in the human planum temporale supports sensory-motor integration for speech processing. J Neurophysiol, 101(5), 2725-2732. doi: 91099.2008 [pii]

10.1152/jn.91099.2008

Hickok, G., Houde, J., & Rong, F. (2011). Sensorimotor integration in speech processing: computational basis and neural organization. Neuron, 69(3), 407-422. doi: S0896-6273(11)00067-5 [pii]10.1016/j.neuron.2011.01.019

Isenberg, A. L., Vaden, K. I., Jr., Saberi, K., Muftuler, L. T., & Hickok, G. (2012). Functionally distinct regions for spatial processing and sensory motor integration in the planum temporale. Hum Brain Mapp, 33(10), 2453-2463. doi: 10.1002/hbm.21373

Middlebrooks, J. C. (2002). Auditory space processing: here, there or everywhere? Nat Neurosci, 5(9), 824-826.

Pa, J., & Hickok, G. (2008). A parietal-temporal sensory-motor integration area for the human vocal tract: Evidence from an fMRI study of skilled musicians. Neuropsychologia, 46, 362-368. 

Smith, K. R., Okada, K., Saberi, K., & Hickok, G. (2004). Human cortical motion areas are not motion selective. Neuroreport, 9, 1523-1526.

Smith, K. R., Saberi, K., & Hickok, G. (2007). An event-related fMRI study of auditory motion perception: no evidence for a specialized cortical system. Brain Res, 1150, 94-99. 

Smith, K. R., Hsieh, I. H., Saberi, K., & Hickok, G. (2010). Auditory spatial and object processing in the human planum temporale: no evidence for selectivity. Journal of Cognitive Neuroscience, 22(4), 632-639. doi: 10.1162/jocn.2009.21196

Wise, R. J. S., Scott, S. K., Blank, S. C., Mummery, C. J., Murphy, K., & Warburton, E. A. (2001). Separate neural sub-systems within "Wernicke's area". Brain, 124, 83-95. 

Zatorre, R. J., Bouffard, M., Ahad, P., & Belin, P. (2002). Where is 'where' in the human auditory cortex? Nat Neurosci, 5(9), 905-909. 

Why "embodied simulation" is a vacuous concept - from Myth of Mirror Neurons

From "Chapter 6: The Embodied Brain" in The Myth of Mirror Neurons:

To say that a cognitive operation is accomplished via simulation doesn’t simplify the problem, it just hands it off to another domain of inquiry, in this case sensory and motor information processing. It’s akin to a hypothetical rogue head-of-state who calls in his top physicists and demands that they work out how to build a nuclear weapon. The physicists come back a week later and proclaim that they’ve got it all figured out: 

PHYSICISTS: We have determined that Oppenheimer and his team have succeeded in building a nuclear weapon. All we need to do is simulate what they did.
HEAD-OF-STATE: Great! So how did they do it?
PHYSICISTS: We don’t know. But simulating their methods will definitely work.
.
.
. 

MIRROR NEURON THEORISTS: We have determined that when we carry out an action of our own we understand the meaning of that action. When we observe someone else’s action, all we need to do is simulate that action in our own motor system and we will achieve understanding.
SKEPTIC: Yes, but how do we understand the meaning of our own actions in the first place?
MIRROR NEURON THEORISTS: We don’t know, but we know that simulating that process will work.