ArticlePDF Available
Two Eyes for an Eye: The
Neuroscience of Force Escalation
Sukhwinder S. Shergill,
1,2
Paul M. Bays,
1
Chris D. Frith,
1
Daniel M. Wolpert
1
*
Physical conflicts tend to escalate. For exam-
ple, as tit-for-tat exchanges between two chil-
dren escalate, both will often assert that the
other hit him or her harder. Here we show
that, in such situations, both sides are report-
ing their true percept and that the escalation is
a natural by-product of neural processing.
Six pairs of naı¨ve participants took part in a
tit-for-tat experiment. Each member of a pair
rested his or her left index finger in a molded
support. A force transducer, which was attached
to a lightweight lever of a torque motor, was
placed on top of this finger (Fig. 1, inset). A trial
was started by one torque motor producing a
0.25 N force on one participant’s finger. Partic-
ipants then took turns to press with their right
index finger down for3sontheforce transducer
resting on the other’s left index finger. They
were instructed to apply the same force on the
other participant that had just been exerted on
them. Each participant was unaware of the in-
structions given to the other. In all cases, the
forces escalated rapidly (Fig. 1A). Across the six
pairs, there was a significant (F
1,5
12.1, P
0.05) average increase of 3.2 N over the eight
turns corresponding to a 38% mean escalation on
each turn. The increase was also significant (P
0.05) within every pair of participants. Thus,
force escalation occurs rapidly even under in-
structions designed to achieve parity.
To investigate the basis of the escalation
process, we examined the perception of
force in an additional 12 naı¨ve participants
tested individually. A torque motor applied
a brief constant force to the tip of the
participant’s left index finger that was rest-
ing in a molded support. When participants
were required to use their right index finger
to match the perceived force, by pushing on
their left index finger through the force
transducer, they consistently overestimated
the force required [Fig. 1B (Y)]. This ob-
servation suggests that self-generated forc-
es are perceived as weaker than externally
generated forces of the same magnitude.
This could arise from a predictive process
(13) in which the sensory consequences of a
movement are anticipated and used to attenuate
the percepts related to these sensations. Such a
mechanism removes some of the predictable
component of the sen-
sory input to self-gen-
erated stimuli, thereby
enhancing the salience
of sensations that have
an external cause (4
7). In a second condi-
tion, participants were
required to reproduce
the experienced force
using their right index
finger to move a joy-
stick that controlled
the force output of the
torque motor. The ac-
tive hand does not
generate the force di-
rectly; the hand’s
movement is trans-
lated into a force
through the torque
motor. In this unusu-
al situation, predic-
tive mechanisms are
not employed (8).
When the force was
generated via the joy-
stick, the reproduced
force matched the original force much more
accurately [Fig. 1B ()]. A regression analy-
sis showed a significant increase in both the
intercept (F
1,11
18.1, P 0.01) and slope
(F
1,11
25.7, P 0.001) when the force was
applied directly rather than via the joystick.
The average increase across the 12 partici-
pants was 0.53 N (0.12 N, SE) for the
intercept and 49% (9%, SE.) for the slope.
The attenuation of self-generated forces
occurred in our experiments even though
accurate perception of force was the prima-
ry requirement of the task, suggesting that
such attenuation is very unlikely to be me-
diated via attentional mechanisms. Previ-
ous studies have shown that sensory per-
ception is attenuated in a moving arm or
finger (911). Here we have shown sub-
stantial attenuation in the resting finger
when the tactile stimulus is self-generated
(12). Despite the stimuli being identical at
the level of peripheral sensation, the per-
ception of force is reduced by about a half
when the force is self-generated. Force es-
calation can, therefore, be seen as a by-
product of predictive sensory attenuation.
References and Notes
1. W. Sperry, J. Comp. Physiol. Psychol. 43, 482
(1950).
2. E. Von Holst, Brit. J. Anim. Behav. 2, 89 (1954).
3. D. M. Wolpert, Z. Ghahramani, M. I. Jordan, Science
269, 1880 (1995).
4. L. Weiskrantz, J. Elliot, C. Darlington, Nature 230, 598
(1971).
5. G. Claxton, Percept. Motor Skills 41, 335 (1975).
6. S. J. Blakemore, D. M. Wolpert, C. D. Frith, Nature
Neurosci. 1, 635 (1998).
7. G. Curio, G. Neuloh, J. Numminen, V. Jousmaki, R.
Hari, Hum. Brain Mapp. 9, 183 (2000).
8. S. J. Blakemore, S. J. Goodbody, D. M. Wolpert, J. Neu-
rosci. 18, 7511 (1998).
9. R. W. Angel, R. C. Malenka, Exp. Neurol. 77, 266
(1982).
10. R. J. Milne, A. M. Aniss, N. E. Kay, S. C. Gandevia, Exp.
Brain Res.70:569 (1988).
11. C. E. Chapman, M. C. Bushnell, D. Miron, G. H. Dun-
can, J. P. Lund, Exp. Brain Res. 68, 516 (1987).
12. The perception of force in the relaxed finger is me-
diated through mechanoreceptors. In the second
group of participants, we also examined a condition
in which they actively flexed their left finger during
force presentation and matching so that afferents
from the muscles and joints could also contribute to
force perception. Attenuation in this contracted con-
dition was not significantly different from that of the
relaxed condition.
13. We thank J. Ingram for technical assistance and R.
Flanagan for comments. Supported by the McDonnell
Foundation, the Human Frontiers Science Pro-
gramme, and Wellcome Trust.
4 April 2003; accepted 8 May 2003
1
Institute of Neurology, University College London,
Queen Square, London WC1N 3BG, U.K.
2
Institute of
Psychiatry, De Crespigny Park, London, U.K.
*To whom correspondence should be addressed, E-
mail: wolpert@hera.ucl.ac.uk
Fig. 1. (A) Force escalation in a typical pair (participant 1, solid circles;
participant 2, empty circles; mean SE across four trials). The initial
force (white square) was generated on participant 1 by the torque motor.
(B) Matching force generated using the right finger (solid circles) and
joystick (white circles) as a function of the externally generated force
(mean SE across participants). Dotted line, perfect performance. On
each trial, the torque motor generated a force between 0.5 and 2.75 N
for 3 s (40 pseudo-randomized trials). Each participant experienced both
conditions in a counterbalanced order (participant 1, gray hands and solid
circles; participant 2, white hands and open circles; mean SE across
four trials).
BREVIA
www.sciencemag.org SCIENCE VOL 301 11 JULY 2003 187
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Cutaneous sensory thresholds were measured at the index fingertip of eight normal subjects. Electric shocks were applied with the finger at rest or tracking a target, which oscillated at one of three frequencies. For each subject, the sensory threshold was positively correlated with the frequency of oscillation. The correlations between sensory suppression and speed of movement agree with previous findings obtained using experimental animals and somatosensory-evoked responses. Possible mechanisms are discussed.
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During self-generated movement it is postulated that an efference copy of the descending motor command, in conjunction with an internal model of both the motor system and environment, enables us to predict the consequences of our own actions (von Helmholtz, 1867; Sperry, 1950; von Holst, 1954; Wolpert, 1997). Such a prediction is evident in the precise anticipatory modulation of grip force seen when one hand pushes on an object gripped in the other hand (Johansson and Westling, 1984; Flanagan and Wing, 1933). Here we show that self-generation is not in itself sufficient for such a prediction. We used two robots to simulate virtual objects held in one hand and acted on by the other. Precise predictive grip force modulation of the restraining hand was highly dependent on the sensory feedback to the hand producing the load. The results show that predictive modulation requires not only that the movement is self-generated, but also that the efference copy and sensory feedback are consistent with a specific context; in this case, the manipulation of a single object. We propose a novel computational mechanism whereby the CNS uses multiple internal models, each corresponding to a different sensorimotor context, to estimate the probability that the motor system is acting within each context.
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Using Sphaeroides spengleri (Bloch), the southern swell-fish, visual inversion of one eye was secured by 180° surgical rotation. The other eye was blinded. Visual inversion was accompanied by forced circling movements, which survived bilateral ablation of the forebrain, the cerebellum, or the inferior lobes of the infundibulum. Circling was not eliminated by bilateral labyrinthectomy and severance of the extraocular muscles, but was abolished if the eye was returned to its normal orientation, and if the optic lobe of the rotated eye was removed. (PsycINFO Database Record (c) 2012 APA, all rights reserved)