Primary somatosensory contribution to action observation brain activity—combining fMRI and cTBS
Social Cognitive and Affective Neuroscience, 2016, 1205–1217
doi: 10.1093/scan/nsw029
Advance Access Publication Date: 15 March 2016
Original article
Primary somatosensory contribution to action
observation brain activity—combining fMRI and cTBS
1
Department of Neuroscience, University of Groningen, University Medical Center Groningen, Antonius
Deusinglaan 2, 9713 AW Groningen, The Netherlands, 2The Netherlands Institute for Neuroscience, Royal
Netherlands Academy of Arts and Sciences (KNAW), Meibergdreef 47, 1105 BA Amsterdam, The Netherlands,
3
Department of Psychology, University of Amsterdam, Weesperplein 4, 1018 XA Amsterdam, The
Netherlands, 4Department of Psychology and Centro studi e ricerche in Neuroscienze Cognitive, University of
Bologna, Cesena Campus, Cesena 47521, Italy, and and 5Istituto di Ricerca e Cura a Carattere Scientifico
Fondazione Santa Lucia Rome 00179, Italy
Correspondence should be addressed to Valeria Gazzola, The Netherlands Institute for Neuroscience, Royal Netherlands Academy of Arts and Sciences
(KNAW), Meibergdreef 47, 1105 BA Amsterdam, The Netherlands. E-mail:
Present address: Nikola Valchev, Department of Psychiatry, Yale University, CMHC S110, 34 Park Street, New Haven, CT, 06519, USA
*The first two authors contributed equally to this work.
Abstract
Traditionally the mirror neuron system (MNS) only includes premotor and posterior parietal cortices. However,
somatosensory cortices, BA1/2 in particular, are also activated during action execution and observation. Here, we examine
whether BA1/2 and the parietofrontal MNS integrate information by using functional magnetic resonance imaging (fMRI)guided continuous theta-burst stimulation (cTBS) to perturb BA1/2. Measuring brain activity using fMRI while participants
are under the influence of cTBS shows local cTBS effects in BA1/2 varied, with some participants showing decreases and
others increases in the BOLD response to viewing actions vs control stimuli. We show how measuring cTBS effects using
fMRI can harness this variance using a whole-brain regression. This analysis identifies brain regions exchanging actionspecific information with BA1/2 by mapping voxels away from the coil with cTBS-induced, action-observation-specific BOLD
contrast changes that mirror those under the coil. This reveals BA1/2 exchanges action-specific information with premotor,
posterior parietal and temporal nodes of the MNS during action observation. Although anatomical connections between
BA1/2 and these regions are well known, this is the first demonstration that these connections carry action-specific signals
during observation and hence, that BA1/2 plays a causal role in the human MNS.
Key words: SI; BA1/2; TMS; action observation; mirror neuron system
Introduction
Functional magnetic resonance imaging (fMRI) evidences a network of regions, agnostically dubbed ‘shared circuits’, activated
both during action perception (observation or listening) and
execution. [e.g. Grezes et al., 2003; Gazzola et al., 2006, 2007;
Dinstein et al., 2007; Filimon et al., 2007; Gazzola and Keysers,
2009; Ricciardi et al., 2009; Turella et al., 2009; see Caspers et al.
(2010) and Molenberghs et al. (2012) for meta-analyses]. Shared
Received: 31 July 2015; Revised: 22 January 2016; Accepted: 8 March 2016
C The Author (2016). Published by Oxford University Press.
V
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/),
which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
1205
Downloaded from http://scan.oxfordjournals.org/ at University of Pennsylvania on December 31, 2016
Nikola Valchev,1 Valeria Gazzola,1,2,3 Alessio Avenanti,4,5 and
Christian Keysers1,2,3
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| Social Cognitive and Affective Neuroscience, 2016, Vol. 11, No. 8
Table 1. Group shared circuits: ActionObs–CtrlObs and ActionExe–CtrlExe (both at P 0.001, T(16) 3.69, qFDR 0.05).
T
x
y
z
Hem
2886
15.18
13.49
12.96
10.85
10.22
9.42
8.12
12.65
9.04
6.66
15.30
6.07
10.59
7.00
6.40
5.83
7.20
4.87
8.75
5.03
4.54
5.90
5.36
50
30
36
58
52
42
28
26
6
2
38
52
28
54
40
40
32
28
50
12
24
6
54
26
42
46
26
28
32
48
6
0
8
6
4
2
8
4
4
58
62
70
20
10
78
62
44
58
60
34
48
40
58
58
48
30
8
28
62
24
12
2
26
20
8
2
2
4
10
L
L
L
L
R
R
R
L
L
L
L
L
R
R
R
R
R
L
L
L
L
L
R
2198
1500
646
457
333
217
159
99
82
74
69
49
Anatomical
description
Cytoarchitectonic
description
Inferior parietal lobule
Postcentral gyrus
Superior parietal lobule
Supramarginal gyrus
Postcentral gyrus
Supramarginal gyrus
Superior parietal lobule
Superior frontal gyrus
SMA
Anterior cingulate cortex
Insula lobe
Precentral gyrus
Superior frontal gyrus
Inferior frontal gyrus (pars opercularis)
Rolandic operculum
Insula lobe
Cerebellum (VI)
Cerebellum (VI)
Inferior occipital gyrus
Thalamus
Putamen
Linual gyrus
Inferior temporal gyrus
Area 2
Area 2
SPL
IPC
IPC
IPC
Area 2
Area 6
Area 6
Area 44
Area 6
Area 44
OP 3
Area 17
hOC5
From left to right: the cluster size in number of voxels; the T values, the MNI coordinates in mm, the hemisphere, the anatomical description and, when available, the
cytoarchitectonic description (as given by the Anatomy toolbox) of the local maxima within the cluster.
circuits include, in addition to occipital and temporal regions
associated with vision and audition, two additional groups of
areas. One, associated with the motor system, includes dorsal
and ventral premotor cortices and the inferior parietal lobe.
Because mirror neurons were recorded in these regions (Gallese
et al., 2001; Kohler et al., 2002; Keysers et al.,
et al., 1996; Umilta
2003; Cisek and Kalaska, 2004; Fogassi et al., 2005; Fujii et al.,
2008; Rozzi et al., 2008; Mukamel et al., 2010), this group has been
called the (putative) mirror neuron system (pMNS). The other
group, mainly associated with the somatosensory system, includes posterior regions of the primary (Brodmann Area 1 and 2
in particular, BA1/2) and secondary somatosensory cortex (SII).
Somatosensory cortices may therefore contribute to perceiving
others in general (Adolphs et al., 2000; Bufalari et al., 2007;
Valeriani et al., 2008; Keysers et al., 2010; Bolognini et al., 2011;
Bolognini et al., 2013; Bolognini et al., 2014), and their actions in
particular (Avenanti et al., 2007; Gazzola and Keysers, 2009;
Caspers et al., 2010; Keysers et al., 2010; Jacquet and Avenanti,
2015). As neuroscience embraces that cognition results from the
interplay of multiple regions, the challenge becomes to understand the interplay between the components of the shared circuits. BA1/2 has strong direct anatomical connections with
posterior parietal regions of the pMNS and strong indirect connections with premotor regions of the pMNS (Keysers et al.,
2010). The connections between BA1/2 and dorsal premotor cortex are mainly mediated via pos (...truncated)
