Distinct and distributed functional connectivity patterns across cortex
reflect the domain-specific constraints of object, face, scene, body, and
tool category-selective modules in the ventral visual pathway
R. Matthew Hutchison
a,
⁎, Jody C. Culham
b,c
, Stefan Everling
a,b
, J. Randall Flanagan
d,e
, Jason P. Gallivan
d,e,
⁎⁎
a
Robarts Research Institute, University of Western Ontario, London, Ontario, Canada
b
Brain and Mind Institute, University of Western Ontario, London, Ontario, Canada
c
Department of Psychology, University of Western Ontario, London, Ontario, Canada
d
Centre for Neuroscience Studies, Queen's University, Kingston, Ontario, Canada
e
Department of Psychology, Queen's University, Kingston, Ontario, Canada
abstract article info
Article history:
Accepted 20 March 2014
Available online 31 March 2014
Keywords:
fMRI
Functional connectivity
Faces
Scenes
Bodies
Tools
Primate occipitotemporal cortex (OTC) is composed of a mosaic of highly specialized brain regions each involved
in the high-level visual analysis and recognition of particular stimulus categories (e.g., objects, faces, scenes, bod-
ies and tools). Whereas theories attempting to account for this modular organization of category-selective re-
sponses in OTC have largely focused on visually driven, bottom-up inputs to OTC (e.g., dimensions related to
the visual structure of the world and how it is experienced), other proposals have instead focused on the connec-
tivity of OTC's outputs, emphasizing how the information processed by different OTC regions might be used by
the rest of the brain. The latter proposals underscore the importance of interpreting the activity (and selectivity)
of individual OTC areas within the greater context of the widely distributed network of areas in which they are
embedded and that use OTC information to support behavior. Here, using resting-state fMRI, we investigated
the functional connectivity (FC) patterns of OTC regions associated with object-, face-, scene-, body- and tool-
related processing defined from task-based localizers acquired in the same cohort of participants. We observed
notable differences in the whole-brain FC patterns, not only across OTC regions, but even between areas thought
to form part of the same category-selective network. Furthermore, we found that the neuroanatomical location of
OTC regions (e.g., adjacency) had little, if any, bearing on the FC networks observed. FC between certain OTC areas
and other regions traditionally implicated in sensory-, motor-, affective- and/or cognitive-related processing and
the associated theoretical implications is discussed.
© 2014 Elsevier Inc. All rights reserved.
Introduction
Convergent evidence from a wide variety of methodologies, ranging
from non-human primate (NHP) neurophysiology to human functional
MRI (fMRI), transcranial magnetic stimulation (TMS), and neuropsy-
chology, suggests that occipitotemporal cortex (OTC) contains a constel-
lation of highly specialized brain regions involved in the high-level
perceptual analysis of different categories of visual stimuli (see Grill-
Spector and Malach, 2004). For instance, human fMRI work has identi-
fied a number of regions – some of which have also been reported
in the NHP (see for example, Nasr et al., 2011; Tsao et al., 2003, 2006;
Wachsmuth et al., 1994) – that maximally respond to the viewing of
particular object categories. These areas include the lateral occipital
(LO) area and posterior fusiform sulcus (pFs) for basic objects (Malach
et al., 1995), the occipital face area (OFA) and fusiform face area (FFA)
for faces (Kanwisher et al., 1997), the retrosplenial cortex (RSC) and
parahippocampal area (PPA) for scenes (Epstein and Kanwisher, 1998;
Maguire et al., 1998), the extrastriate body area (EBA) and fusiform
body area (FBA) for bodies (Downing et al., 2001; Peelen and Downing,
2005a) and the posterior middle temporal gyrus (pMTG) for tools
(reviewed in Lewis, 2006). Consistent with this fMRI evidence, disruption
to the normal activity of these regions, either via brain lesions or stimula-
tion, selectively impairs the perceptual processing of specific object cate-
gories (e.g., Mahon et al., 2007; Moro et al., 2008; Parvizi et al., 2012;
Pitcher et al., 2009, 2012; Urgesi et al., 2004).
Several theories have been proposed to account for this highly mod-
ular arrangement of category-selective neural responses in OTC, with
the majority suggesting that this organization largely reflects the visual
NeuroImage 96 (2014) 216–236
⁎ Correspondence to: R.M. Hutchison, Center for Brain Science, Harvard University,
Cambridge, MA, USA.
⁎⁎ Correspondence to: J.P. Gallivan, Department of Psychology, Centre for Neuroscience
Studies, Queen's University, Kingston, Ontario K7L 3N6, Canada.
E-mail addresses: rhutchison@FAS.Harvard.edu (R.M. Hutchison),
jasongallivan@gmail.com (J.P. Gallivan).
http://dx.doi.org/10.1016/j.neuroimage.2014.03.068
1053-8119/© 2014 Elsevier Inc. All rights reserved.
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NeuroImage
journal homepage: www.elsevier.com/locate/ynimg