Please cite this article in press as: R. Wood, et al., Visuotactile empathy within the primary somatosensory cortex revealed by short-latency
afferent inhibition, Neurosci. Lett. (2010), doi:10.1016/j.neulet.2010.02.012
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Neuroscience Letters xxx (2010) xxx–xxx
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Neuroscience Letters
journal homepage: www.elsevier.com/locate/neulet
Visuotactile empathy within the primary somatosensory cortex revealed by
short-latency afferent inhibition
1
2
Rachel Wood
a
, Vittorio Gallese
a,c
, Luigi Cattaneo
b,∗
3
a
Dipartimento di Neuroscienze, Università di Parma, Parma, Italy 4
b
Centro Interdipartmentale Mente/Cervello, Università di Trento, 38100 Mattarello (Trento), Via delle Regole 101, 38123 Trento, Italy Q1 5
c
IIT, Italian Institute of Technology, Section of Parma, Parma, Italy 6
7
article info 8
9
Article history: 10
Received 26 November 2009 11
Received in revised form 4 February 2010 12
Accepted 5 February 2010 13
14
Keywords: 15
Empathy 16
Touch 17
Short-latency afferent inhibition Q2 18
Mirror 19
Transcranial magnetic 20
Stimulation 21
Embodiment 22
abstract
Intersubjectivity entails the taking of another’s perspective in order to understand their experience of
the world. This perspective taking capacity extends to the intra-individual sharing of tactile experience.
Previous studies have shown modulation of motor cortex excitability in response to the observation of
aversive tactile stimulation to the hand of another person. Here we used transcranial magnetic stimulation
(TMS) and peripheral stimulation to induce a short-latency afferent inhibition (SAI) effect, which we
then sought to modulate via observation of non-noxious tactile stimulation to the hand of a model. Side
congruency between the observed (model) and the recorded (participant) hand induced an increase of SAI
and this effect was found to hold for motor-evoked potentials (MEPs) recorded from both left and right
hands. Inhibition was not found with MEPs evoked using unconditioned pulses of TMS. These results
demonstrate a sensorimotor response to observed non-noxious stimulation and suggest an empathic
matching system for the tactile experiences of others.
© 2010 Published by Elsevier Ireland Ltd.
Intersubjectivity requires shared experience and the capacity to 23
take others’ perspectives. A number of studies have demonstrated 24
that the neural structures underlying sensation processing are 25
recruited when observing the sensory experiences of others. fMRI 26
studies of the effects of touch observation [3,9,11] found activation 27
of secondary or primary somatosensory cortex when participants 28
experienced touch and when they observed another person or 29
object being touched. These findings support the notion of shared 30
neural circuits for first and third person experiences of touch. This 31
direct matching mechanism bears strong analogies with the mir- 32
ror systems, where observation of an action automatically activates 33
parts of corresponding neural circuits in the observer, neural cir- 34
cuits that would be recruited if she were performing the action 35
herself [7,10]. 36
Visual activation of somatosensory cortical circuits for touch 37
observation occurs regardless of the animacy of the entity being 38
touched (i.e. object or person), is independent of the observer’s 39
perspective (i.e. ego- or allo-centric) and is not restricted to the 40
domain of intentional touch [9]. This suggests that the observation 41
of any touch can activate shared somatosensory circuits, although 42
intentional touches appear to elicit a greater response in SI (BA 43
2) than accidental touches. Visuotactile mirroring may thus pro- 44
vide an embodied mechanism to support the interpretation of any 45
∗
Corresponding author.
E-mail address: luigi.cattaneo@unitn.it (L. Cattaneo).
touch (regardless of animacy or intentionality) via processes of 46
multimodal integration. 47
Aside from empathy for touch, some studies have addressed 48
the issue of empathy for somatosensory sensation that carries a 49
much stronger affective implication: cutaneous pain. Avenanti et 50
al. [1] were able to demonstrate modulation of sensorimotor activ- 51
ity in response to pain observation using a single-pulse transcranial 52
magnetic stimulation (TMS) paradigm. Motor-evoked potentials in 53
the muscle participants saw being subjected to painful stimulation 54
were significantly reduced. Inhibition was correlated to the inten- 55
sity of the pain observed but not to task instructions, indicating that 56
the sensorimotor component of empathy for pain may be stimulus 57
driven, i.e., predicated on the perceived intensity of the aversive 58
stimulation received by the observed other [1]. 59
Observation of touch is known to elicit both perceptual and neu- 60
rophysiological changes in the observer [4,14–16]. The observation 61
of painful stimulation has been shown to produce a motor response 62
in the observer, however this effect has not previously been found 63
for non-painful stimuli. Thus, we used a short-latency afferent inhi- 64
bition (SAI) paradigm [17] to test the primary sensory and motor 65
cortices for an effect analogous with that found for noxious touch 66
during the observation of non-noxious touch. 67
The SAI technique tests the effects of an afferent somatosen- 68
sory stimulus on the excitability of the motor cortex. TMS alone 69
at stimulation intensities just above motor threshold is capable of 70
probing the excitability state of the motor cortex by depolarizing 71
cortical interneurons and ultimately exciting corticospinal neurons 72
0304-3940/$ – see front matter © 2010 Published by Elsevier Ireland Ltd.
doi:10.1016/j.neulet.2010.02.012