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A behavioral method for studying mirror neurons: Repetitive action affects visual perception
Arthur M.
1,2
Glenberg ,
Gabriel
1Arizona
1
Lopez-Mobilia ,
State University,
2University
Michael
1
McBeath ,
of Wisconsin -
Michael
3
Madison, University
1
Toma ,
of Grenoble,
Marc
3
Sato ,
4University
and Luigi
4
Cattaneo
of Trento
Ago, ergo Cogito
Abstract
Mirror neurons may underlie the ability to make sensorimotor predictions
when observing action, and thus contribute to “reading” intentions of other
animals and facilitating social interaction. Neurophysiological and brain
imaging studies have shown that observation of both biological and nonbiological movements activates a fronto-parietal network of motor regions
which forms the core of the human mirror-neuron system (MNS).
However, many past findings are intrinsically correlational. We developed
a behavioral method to study mirror neurons, based on use-induced
plasticity. Participants engage in a repetitive motor task of moving beans
from one location to another, thereby adapting the neural systems used in
control of the action. Participants then engage in a second task, which
measures if performance is affected by the motor adaptation. In the current
study, the second task measures perceptual bias of ambiguous apparent
motion in one direction or another. We found that the direction of bean
movement (toward or away from the participant) systematically increases
the bias to experience ambiguous movement in the opposite direction
(consistent with habituation). The results corroborate previous findings in
which the second tasks were language-based The findings support the
claim that a MNS is being tapped, and confirm functionality of our method
for studying the causal contribution of MNS to cognitive processes.
Participants move beans, one at a time, from a wide-mouth container to a
narrow-mouth container an arms-length away (Figure 1.) Half of the
participants move the beans in a direction Away from the self, and half
move the beans in a direction Toward the self. Note that very similar
muscles are used in the two conditions. Thus the actions are defined in
terms of target location and specifics of the movement (e.g., a power grip is
used in the Away movement but not the return toward the body, and vice
versa in the Toward movement).
3.
Last, bias in motion perception was measured again for the three
stimuli.
Measuring bias in movement perception
1. Because the fMRI voxel is sensitive to activity from many neurons,
simply showing that an area is active both during action and perception
does not guarantee that the same neurons are responding to both action
and perception (e.g., Dinstein et al, 2007).
Procedure
1.
Bias in motion perception was measured for the three stimulus
shapes: a hand holding a bean, an open hand with palm up, and a plain
diamond (see Figure 3a). The three stimuli were used to determine if we
are tapping “strictly-congruent” (only the hand stimulus should show
evidence of change in bias) or “broadly-congruent” mirror neurons (all
directional stimuli may show a change in bias). The type of stimulus was
manipulated within-subjects, and the tests of bias for each of the three
stimuli were interleaved so that a participant might see a diamond shift, a
hand holding a bean shift, and then an open hand shift.
2.
Next, 48 participants moved 600 beans in one direction or another.
The movement direction was manipulated between-subjects.
Figure 1. Bean containers illustrating the Away condition.
Why not fMRI?
Experiment 1
The bi-directional action task
Our measure of visual perception (that could be adapted by movement
practice) is the bias to see ambiguous apparent movement toward the
observer or away from the observer. The staircase procedure used to
measure the bias was developed by Lewis & McBeath (2004). Participants
view on a computer monitor a screen tiled with stimuli that appear to
recede into the distance (Figure 2).
2. In most fMRI experiments, the signal only indicates a correlation, not a
causal or functional relation.
3. fMRI is difficult to use with children.
Results
Figure 3 (right) shows the change in measured bias as a function of bean
movement direction on the second, post-movement, measure of bias. The
interaction of bean movement direction and pre-movement or postmovement measure of bias was significant, F(1, 46) = 5.16, p= .03.
Repetitive practice of a movement can produce a temporary re-organization
of the brain. For example, Classen et al. (1998) used a TMS pulse over
motor cortex controlling the thumb and elicited a movement in a particular
direction. Then participants practiced moving the thumb in a different
direction for about 20 minutes. Finally, TMS over the same area of motor
cortex now tended to elicit movement in the practiced direction.
Figure 3.
Stimuli (left) &
Results (right)
for Exp. 1.
Conclusions
1.
Direction of action (bean movement) systematically affects visual
perception of ambiguous apparent motion in aligned directions. Findings
support the claim that we tapped into a mirror neuron system.
2.
The mirror neuron response is “broadly-congruent” with the same
effect found for all three stimuli (all exhibited a similar habituation bias).
Experiment 2
Use-induced plasticity and mirror neurons:
The logic
Mirror neurons play a role in both producing action and perceiving action.
Thus, if practice adapts part of a mirror neuron system, then the effects of
that practice should be revealed in a perceptual task that uses the same
mirror neuron system.
In our experiments, we rule out non-specific effects of practice by adapting
the motor system using two opposing practice directions. Showing
different effects of the direction of practice on visual perception rules out
non-specific (e.g., fatigue) effects.
Figure 2. The tiling for one stimulus, the bean hand
A second screen frame is presented one second later with shape tiles
slightly shifted, which induces an illusion of motion that can be in either
depth direction. A shift of 50% of the inter-tile distance is completely
ambiguous, whereas a shift of 20% in either direction is perceived as
movement in the smaller direction of shift. We start with a shift of 20% and
then small increments in shift are added until the observer perceives
movement in the opposite direction (a turn point). The increment is then
reduced and the turn point measured in the opposite direction. Two sets of
eight turn points are collected, and the averages of the last seven (in each
set) are used as the measure of the threshold, or bias, to perceive movement
in one direction or another.
Glenberg, Sato, and Cattaneo (2008) used the same bean task as in
Experiment 1. Participants then read and responded to sentences
describing action Toward the participant (e.g., “Art gives the pen to you”)
or Away from the participant (e. g., “You give the pen to Art”). The
response was whether the sentence was sensible or nonsense (e.g., “You
give Art to the pen”). Participants indicated sensible by depressing a key
with the right index finger, and they indicated nonsense by depressing a
key with the left index finger. Neither response required arm movements.
The findings indicated an interaction such that the time to respond sensible
to Toward sentences was faster when the beans were moved in the away
direction and the time respond sensible to the Away sentences was faster
when the beans were moved in the toward direction. Interestingly, the same
effects were found for sentences describing the transfer of concrete objects
and sentences describing the transfer of abstractions (e.g., “Anna delegates
the responsibilities to you”). Apparently, neural systems used in action
control were also used for comprehending sentences describing actions of
the same general sort.
Plasticity and speech perception
Sato, Brisebois, Grabski, Basirat, Menard, Glenberg, & Cattaneo (2008)
had participants purse their lips 150 times to induce changes in
corticomotor control of the orofacial musculature. Subsequently, they
performed a speeded two-choice identification task of acoustically
presented /pa/ and /ta/ CV syllables either embedded in acoustic noise or
not. A control task was identical but without the lip pursing. They
observed a decrease in “pa” responses in the control session and overall
faster RTs in the motor session.
4. It’s expensive.
Use-induced plasticity
Plasticity and language comprehension
We made several changes in the methodology to rule out alternative
explanations. Most importantly, participants were blindfolded during the
bean movement task. Thus, any affect of movement on the bias measure
can be more securely attributed to adapting an action system rather than
visual stimulation. Second, to eliminate any sensitization to toward and
away movement due to the initial bias measure, the 24 participants first
moved 300 beans in one direction, and then we measured bias.
Participants then moved an additional 300 beans in the same direction, and
the bias was measured again.
The data for the first, post-movement bias measure are in Figure 4. The
effect of bean movement direction was significant, F(1,22) = 5.89, p = .02.
The effects were not significant when measured after the second set of bean
movements.
Two-frame apparent motion tasks show
promise as a hit with some observers!
Figure 4. Experiment 2: Results for the first, post-movement bias
measure. Error bars are one standard error. A = bean movement away from
the body; T = bean movement toward the body.
Conclusions
Our technique appears to have adapted a neural system tuned to multiple
modalities including motor, visual, and language processes. Although more
research is needed, so far these results are consistent with claims that a
human mirror neuron system exists and that it contributes to action
perception, speech perception, and language comprehension. Furthermore,
this simple method provides researchers with a promising instrument to
study the role of mirror neuron systems in these and other cognitive
processes without the expense and inconvenience of fMRI.
References
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Sato, M., Brisebois, A., Grabski, K., Basirat, A, Ménard, L, Glenberg, A. M., & Cattaneo, L. (October,
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Author Note: This research was support in part by NSF grant BCS 0744105. Any opinions, findings, and
conclusions or recommendations expressed in this material are those of the author and do not necessarily
reflect the views of the National Science Foundation. Direct correspondence to Arthur Glenberg,
[email protected]