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Ackno wledgments: We thank C. Perry and H. Swanson for technical
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is supported by the National Institute of Mental Health, the Simons
Foundation Autism Research Initiative, the National Institute on
Drug Abuse, the Defense Advanced Research Projects Agency,
the Gatsby Charitable Foundation, and the Wiegers Family Fund.
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(DAAD), and S. Y.L. received support from the Fidelity Foundation.
Optogenetic tools and methods reported in this paper are
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Materials and Methods
Figs. S1 to S3
18 February 2014; accepted 19 March 2014
Neural Mechanisms of
Daniel Baldauf* and Robert Desimone
How we attend to objects and their features that cannot be separated by location is not understood.
We presented two temporally and spatially overlapping streams of objects, faces versus houses, and used
magnetoencephalography and functional magnetic resonance imaging to separate neuronal responses
to attended and unattended objects. Attention to faces versus houses enhanced the sensory responses
in the fusiform face area (FFA) and parahippocampal place area (PPA), respectively. The increases in
sensory responses were accompanied by induced gamma synchrony between the inferior frontal junction,
IFJ, and either FFA or PPA, depending on which object was attended. The IFJ appeared to be the driver
of the synchrony, as gamma phases were advanced by 20 ms in IFJ compared to FFA or PPA. Thus, the
IFJ may direct the flow of visual processing during object-based attention, at least in part through
coupled oscillations with specialized areas such as FFA and PPA.
When covertly attending to a location in the periphery, visual processing is biased toward the attended location, and the
sources of top-down signals include the frontal
eye fields (FEF) (1, 2) and parietal cortex (PC).
FEF may modulate visual processing through a
combination of firing rates and gamma frequency
synchrony with visual cortex (2). For nonspatial
attention, the mechanisms of top-down attention
are much less clear. When people attend to a feature, such as a particular color (3–5), or to one of
several objects at the same location (6–8), activity
in the extrastriate areas representing properties of
the attended object is enhanced. But where do the
attentional biases (9) come from, and how do they
enhance object processing when the distractors are
not spatially separate?
We combined magnetoencephalography
(MEG), supplemented by functional magnetic
resonance imaging (fMRI) and diffusion tensor
imaging to optimize both spatial and temporal
resolution. In the MEG experiment, two spatially
overlapping streams of objects (faces and houses)
were tagged at different presentation frequencies
(1.5 and 2.0 Hz) (Fig. 1, A and B) (5, 10–12). The
stimuli went in and out of “phase coherence,” so
that they were modulated in visibility over time
but did not change in luminance or flash on and
off. When subjects were cued to attend to one of
the streams and to detect occasional targets with-
in the cued stream, frequency analyses allowed
identifying brain regions that followed the stim-
Using MEG data only (13), the strongest ac-
tivity evoked by the face tag was in the right fu-
siform gyrus, whereas the activity evoked by
the house tag was more medially in the inferior-
temporal cortex (IT) (Fig. 1C; figs. S1 and 2 for
individual subjects and alternative source recon-
struction approaches). These areas were roughly
consistent with the locations of fusiform face area
(FFA) and parahippocampal place area (PPA)
determined previously in fMRI (14–16). To in-
crease the accuracy of localization in each sub-
ject, we added high-resolution fMRI localizers
for FFA and PPA (Fig. 2, B and D, and fig. S3A),
which were focused at the expected spots (Fig. 2F).
To identify other areas important for non-
spatial attention, we contrasted the brain state
when attending to one of the two superimposed
object classes with a similarly demanding state
that did not require attending to either object
class. The attention-related fMRI localizers re-
vealed consistent activation in the inferior frontal
junction (IFJ) at the intersection of the inferior-
frontal and precentral sulcus (17–19) (Fig. 2, A,
C, and E), with weaker and less-consistent sig-
nals in posterior-parietal and in inferior-temporal
cortex (fig. S3C). A control experiment confirmed
that IFJ's activation was indeed related to non-
spatial attention, rather than simply memory
Each subject's individual fMRI localizers
were then used as regions of interest (ROIs) to
guide the analysis of the MEG signals (see sup-
plementary material for a description of the co-
registration of fMRI and MEG). The modulation
of sensory responses by attention in the tagging-
frequency range is shown in Fig. 2G (fig. S5B for
individual subjects). FFA and PPA had the stron-
gest responses, with FFA more responsive to the
attended face tag (t test, P < 0.001) and PPA more
responsive to the attended house tag (t test, P <
0.01). Thus, object-specific attention modulates
the sensory responses in FFA and PPA. Weaker
sensory responses were found in region V1.
Although weaker in amplitude, sensory re-
sponses were also found in IFJ, and the attention
effects were much stronger—there was a tagging
frequency response only to the attended object
(both t test, P < 0.001). Control regions in the
FEF (localized in separate fMRI runs, fig. S3D),
PC (localized in the attention-related fMRI experi-
ment in some participants) and the frontal pole
(anatomically defined) showed only minor and
less consistent responses. The general pattern of
McGovern Institute for Brain Research, Massachusetts
Institute of Technology, Cambridge, 02139 MA, USA.
*Corresponding author. E-mail: email@example.com