Download face-specific responses from the human inferior occipito

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Neuroscience Vol. 77, No. 1, pp. 49–55, 1997
Copyright ? 1997 IBRO. Published by Elsevier Science Ltd
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S0306-4522(96)00419-8
FACE-SPECIFIC RESPONSES FROM THE HUMAN
INFERIOR OCCIPITO-TEMPORAL CORTEX
M. SAMS,*† J. K. HIETANEN,‡§ R. HARI,* R. J. ILMONIEMI*¶ and
O. V. LOUNASMAA*
*Low Temperature Laboratory, Helsinki University of Technology, 02150 Espoo, Finland
‡Institute of Biomedicine, Department of Physiology, P.O. Box 9, 00014 University of Helsinki,
Helsinki, Finland
Abstract––Whole-head neuromagnetic responses were recorded from seven subjects to pictures of faces
and to various control stimuli. Four subjects displayed signals specific to faces. The combination of
functional information from magnetoencephalography and anatomical data from magnetic resonance
images suggests that the face-specific activity was generated in the inferior occipitotemporal cortex. All
four subjects showed the face-specific response in the right hemisphere, one of them also in the left.
Our results, together with recent positron emission tomography and lesion studies, suggest a
right-hemisphere preponderance of face processing in the inferior occipitotemporal cortex. Copyright ?
1997 IBRO. Published by Elsevier Science Ltd.
Key words: magnetoencephalography, face, visual cortex, evoked responses, perception, human.
Processing of facial images has been studied extensively during the past few years. Neuropsychological
models have emphasized the unique nature and
sequence of different stages in this process (e.g.,
Ref. 9), while neurophysiological recordings have
provided evidence for the existence of localized
brain areas related to facial perception and recognition.17,21,39 This multidisciplinary approach is hoped
to be successful in constructing anatomo-functional
models of cerebral face processing.
Many different experimental methods have been
employed: measurements of performance and
reaction time,8,13,42,43 tachistoscopic presentation of
face stimuli to divided visual fields,20,25,36 investigations of symptoms in patients having (prosopagnostic) difficulties in perceiving and recognizing faces
after local brain injuries,11,12,28 measurements of
visual evoked potentials6,21,22,23 and magnetic fields27
to face stimuli, and measurements of regional
cerebral blood flow with positron emission tomography (PET) during facial image processing.39 In
addition, single-unit recordings on monkeys have
revealed cell populations in the temporal cortex
responding selectively to faces.14,19,32,33
Magnetoencephalography (MEG), a method for
studying the neural basis of cognitive brain functions
non-invasively, is based on recordings of the weak
magnetic fields produced by electric currents flowing
in active neurons (for a comprehensive review of the
method, see Ref. 16). MEG differs from electroencephalography (EEG) in its selectivity to superficial, tangentially oriented neural currents. This
means that MEG ‘‘sees’’ mainly the fissural cortex
and, therefore, less neuronal activity than EEG.
MEG offers a temporal resolution in the millisecond
range which makes it useful in studying the timecourse of stimulus-evoked brain responses. In
addition, because the intervening cerebral and
extracerebral tissues are practically transparent to
magnetic fields, whereas electric recordings are
often smeared by inhomogeneities in them, it is often
easier to calculate the locus of the activated
brain area on the basis of MEG rather than EEG
recordings.16
In a previous study from this laboratory,27 MEG
was applied to identify face-responsive brain areas.
Three sites outside the occipital visual cortex were
observed to become active, two of them exclusively
by viewing faces: an area near the occipitotemporal
junction and another in the mid-temporal lobe. In
this early study, MEG signals were recorded with a
24-channel magnetometer that covered an area
12.5 cm in diameter. We decided to extend and
confirm the previous results with our 122-channel
neuromagnetometer. This device covers the whole
scalp and thus offers the possibility of studying interand intrahemispheric differences in the magnetic
fields during a single recording session.
†To whom correspondence should be addressed.
§Present address: Department of Psychology, University of
Tampere, Tampere, Finland.
¶Present address: BioMag Laboratory, Medical Engineering
Centre, Helsinki University Central Hospital, 00290
Helsinki, Finland.
Abbreviations: ECD, equivalent current dipole; EEG,
electroencephalography; MEG, magnetoencephalography; MRI, magnetic resonance imaging; PET, positron
emission tomography.
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50
M. Sams et al.
Fig. 1. Examples of pictures used in the experiment. From left to right: a face, the same face pointillized,
an everyday object and a sphere.
Fig. 2. Whole-head 122-channel neuromagnetic responses to faces (continuous lines) and pointillized faces
from subject S3. The head is viewed form the top (the nose is pointing up), and in each response pair the
upper trace illustrates the field derivative along the latitude and the lower trace along the longitude. The
face-specific response is best seen in the channel pair over the right occipital cortex (framed). The thin
vertical line is drawn at the peak of the face-specific response. (Insert) The channel pair showing the
face-specific response is depicted on an expanded scale in the center. The occipital dipolar magnetic field
pattern at the peak of the face-specific response is illustrated in the upper part; the center of the white
arrow indicates the approximate location of the source for this response; the head is viewed from the right
and slightly behind. The isocontours are separated by 30 fT. The lower part shows the field pattern at the
same latency for pointillized faces. In this case there is very weak indication of activity in the right visual
cortex.
EXPERIMENTAL PROCEDURES
Seven subjects with normal vision were studied (one
left-handed, three females, four males, 22–35 years old).
During the recordings, the subject sat in a magnetically
shielded room with the head supported against the helmetshaped magnetometer.
Four different stimulus categories were presented (see
Fig. 1): (i) 23 faces of persons working in the laboratory; (ii)
‘‘pointillized’’ (Adobe Photoshop=) versions of these 23
faces; the altered figures did not look like faces at all, but
their mean luminance was preserved; (iii) 23 images of
everyday objects such as a watering can, a watch, scissors
etc.; and (iv) a white sphere on a grey background. All
Face-specific response
stimulus categories were equiprobable (P=0.25) and they
were presented in random order within one sequence. The
subjects were instructed to fixate on a cross in the center of
the image, avoid eye movements during stimuli and concentrate on looking at the pictures without any other specific
task. The pictures, 3.1) in height and 2.6) in width, were
presented against grey background for 500 ms, once per
second, on a computer screen located outside the darkened
magnetically shielded room. The subjects viewed them
through a hole via a mirror system.
The magnetic brain signals were recorded with the
Neuromag-122 system,1 which has 122 planar first-order
SQUID (Superconducting QUantum Interference Device)
gradiometers covering the whole head. Each sensor block
contains a pair of independent units that measure two
orthogonal tangential derivatives of the magnetic field component Bz, normal to the helmet surface at the sensor
location. With this instrument, brain activity produces the
largest signal just above the source, where the field gradient
has its maximum. The two derivatives measured at each site
also give the direction of the source current.
The signals were analogically bandpass-filtered (0.03–
100 Hz), digitized at 0.4 kHz and averaged on-line. The
900-ms analysis period included a 100-ms prestimulus baseline. A minimum of 120 responses were averaged for each
stimulus category. To check the replicability of the data, the
experiment was performed twice for each subject. A vertical
electro-oculogram was used to reject data contaminated by
eye movements or blinks.
Three marker coils were attached to the scalp, and their
positions in the head coordinate frame were measured with
a three-dimensional digitizer. The coordinate system was
specified by the two periauricular points and the nasion.
The head position with respect to the sensor array was then
determined by feeding current to the marker coils when the
subject was seated under the magnetometer.
To identify neural sources underlying the evoked
magnetic responses, equivalent current dipoles (ECDs),
each best describing the measured field pattern at a given
time instant, were extracted by a least-squares search. After
digital low-pass filtering at 30 Hz, single ECDs were found
using a subset of channels around the one showing the
largest signal. The goodness-of-fit (g) of the source model
was also calculated.24 Only ECDs explaining more than
80% of the field variance during the face-specific response
were accepted.
In one subject (S3), the ECD locations were related to
brain anatomy obtained from magnetic resonance images.
The magnetic resonance imaging (MRI) coordinate system
was aligned with the help of oil capsules attached to the
nasion and to the two preauricular points before MRI
acquisition. These marker locations were picked from the
images. The volume conductor sphere was fitted on
the basis of the magnetic resonance images to the local
curvature of the surface of the brain over the source area.
RESULTS
Figure 2 shows the neuromagnetic responses of
subject S3 to faces (continuous lines) and pointillized
faces (dashed lines). The largest signals to both
stimuli, as also to everyday objects and spheres, were
recorded over the occipital cortex; the frontal and
frontotemporal areas showed only negligible responses. Responses to faces and pointillized faces
differed systematically over the right occipital cortex
(framed channel pair and inset) from 120 ms onwards; the difference was largest around 160 ms. The
occipital magnetic field pattern at the peak of the face
51
Fig. 3. Neuromagnetic signals of four subjects over the
posterior part of the left and right hemispheres. Traces from
two consecutive recordings are superimposed. The responses to face stimuli are presented with thick continuous
lines. The thinner continuous curves indicate responses to
pointillized faces, the thinnest short dashed lines responses
to everyday objects and longer dashed lines responses to
spheres.
response is shown in the upper part of the inset. The
arrow depicts the surface projection of the ECD.
The field pattern drawn at the same latency for the
pointillized faces (lower part of the inset) suggested
very weak activity over the occipital cortex.
Responses to the two stimulus categories also
differed at the posterior channels (Fig. 2). It is
suggested that this difference reflects the differential
processing of simple visual features. Response differences were also found between faces and other
control stimuli. These differences were not, however, systematic but were different for various
control–stimulus categories.
Of the seven subjects studied, four showed clear
and replicable face-specific responses. The responses
from these subjects are depicted in Fig. 3. Subject S1,
who is right handed, had a face-specific response over
both hemispheres but the signal was clearly larger
over the left hemisphere. The other three subjects
produced a face-specific signal only over the right
hemisphere; the responses peaked at 150–170 ms. The
other stimulus categories elicited only small signals at
about the same latency. Note the good replicability
of the face-specific responses.
Figure 4 (upper part) shows the source location
for the face-specific response of subject S3, projected
on her MRI surface rendering. This ECD, pointing towards the occipitoparietal area, accounted
for 84% of the field variance. MRI slices cut
through the source are illustrated in the bottom row.
The Talairach41 coordinates of the source are
9-c-G, agreeing with the location of the fusiform
gyrus.
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M. Sams et al.
Fig. 4. (Top, from left to right) Right, back and top views of MRI surface renderings of subject S3. The
source area (white dot) of the face-specific response is projected on to the surface of the brain along
the viewing direction. (Bottom) MRI slices at the source level of the face-specific response. The line in the
sagittal section shows the direction of the ECD.
Figure 5 illustrates the calculated source locations
and directions for the face-specific responses for
subjects S1–S4. The corresponding goodness-of-fits
were 89, 87, 84 and 83%. The right-hemisphere
response of subject S1 (Fig. 3) was not adequately
explained by a single ECD. In all subjects, ECDs
point towards the centroparietal or occipitoparietal
scalp. The sources were in the occipital regions, but
clearly outside the primary projection areas. We did
not find face-specific responses in more anterior parts
of the brain.
Faces, pointillized faces (Fig. 2) and the other
picture categories elicited many other MEG deflections at 80–400 ms. These responses were predominantly recorded over the back of the head, evidently
arising from occipitoparietal areas. Because the
fixation point was at the center of the images, stimuli
activated the visual cortex in a very complex way.
Therefore, it was not possible to determine the
location of the ECDs for these different signals,
which certainly reflect the mixed activation of several
cytoarchitectonic areas.
DISCUSSION
The present study reports replicable face-specific
neuromagnetic responses in four of seven normal
human subjects. The combination of functional
information from MEG and anatomical data from
MRI suggests that the face-specific activity is
generated in the inferior occipitotemporal cortex.
Very similar responses occurring at approximately
the same latency have been reported in intracranial
recordings,3 evoked-potential recordings21 and in a
separate MEG experiment conducted in our laboratory.15 The source location of the response agrees
with that found in other recent studies.3,10,15,18,34,39
Face-specific responses peaked at 150–170 ms, in
accordance with evoked potential data21 and subdural recordings.3 Single units in the temporal lobe of
the macaque monkey (STPa) reach their maximum
firing rate on average 180 ms after face stimuli,30
whereas the responses from V1 have a mean latency
of about 50 ms.37 The first human MEG responses,
probably originating from the striatal and extra-
Face-specific response
Fig. 5. Horizontal (xy), sagittal (yz) and coronal (xz) views
illustrating the sources of face-specific responses in four
subjects. The schematic head (radius=7 cm) is shown to give
an impression of the approximate source locations in the
brain.
striatal areas, peak at 80–100 ms.2 The rather long
peak latency and the source location suggest that
the face-specific signal reflects activation of brain
mechanisms involved in complex visuoperceptual
processing of the facial image.
The source locations of the face-specific responses
varied across the subjects. The common feature was
that all ECDs point towards the centroparietal or
occipitoparietal scalp and that the sources were in the
posterior brain regions, outside the primary projection areas. In S3, whose magnetic resonance images
were available, the ECD was located in the area of
the fusiform gyrus, in the occipitotemporal sulcus.
However, as suggested by previous studies, rather
extensive areas in the gyral and sulcal cortices are
activated by face stimuli.34 When this activity is
53
modeled by a single dipole, its location denotes a
center of gravity of the activated area.
In the other subjects, the right-hemisphere sources
were more superior and located rather anteriorly (S4)
or posteriorly (S2). This variability might be due to
individual differences in the locations of the facespecific cortical areas.3 Additional variability might
be caused by simultaneous activity of more than
one adjacent face-specific area, whose relative
contributions might vary (cf. Ref. 39).
Meaningful control stimuli, comparable in their
complexity to faces, typically elicit smaller and later
electrical evoked responses than faces.21–23 Similarly,
our control stimuli weakly activated the right
occipital cortex at 150–170 ms (Fig. 2, Fig. 3). These
findings suggest that even non-face stimuli can
activate the face neurons, although less intensively.
However, recent subdural recordings3 imply that the
inferior occipital cortex contains areas which are very
specific to faces and that other stimulus types may
elicit responses at the same latency, but at different
cortical locations.
One possible explanation for the absence of facespecific responses in three of our seven subjects is
source orientation. If the source is close to radial, the
signal cannot be recorded by MEG. In addition,
face-specific neurons may be located rather deeply,3
resulting in signals too weak to be picked up.
Jeffreys21 identified an evoked potential to faces in
eight of nine subjects, but because the responses were
small, the conclusions were based on recordings on
only three subjects. Jeffreys and Tukmachi23 screened
each new volunteer in order to obtain subjects with
distinct ‘‘vertex positive peaks’’, which they have
demonstrated to be sensitive to faces.
A previous face study from this laboratory27
suggested two face-specific areas, one near the
occipitotemporal junction and another in the middle
temporal lobe. The response in the occipitotemporal
junction peaked at 95–160 ms and was on average
38 mm beneath the skull. The signal is probably
analogous to the face-specific response of the present
study, which actually suggests an origin in the
inferior occipitotemporal cortex. The present study
did not reveal face-specific responses in the midtemporal areas. Neuronal activity in the middle
temporal gyrus may be modulated during identification of facial emotions.29 It is possible that the
subjects in our previous study paid attention to the
emotionality of the faces.
The polarity of the face-specific response in subdural recordings3 suggests source currents oriented
towards the parietal lobe and vertex. A similar direction was obtained for the present ECDs. This kind of
current source appears as a scalp positivity close to
the vertex, as was found in EEG recordings.21–23
Lateralization of functions involved in face
processing is still a controversial issue.4,5 In subdural
recordings, Allison et al.3 found face-specific signals
from the fusiform and inferior temporal gyri of both
54
M. Sams et al.
hemispheres. Similarly, cortical volumes activated by
face stimuli in a recent functional MRI study were
not different in the two hemispheres.34 On the other
hand, prosopagnostic patients studied recently with
MRI and PET showed no involvement of the left
hemisphere.40 Sergent et al.39 suggested that three
areas of the right hemisphere play a crucial role in
face processing: (i) the ventral part of the right
occipital cortex is involved in perceptual operations,
(ii) the more anterior ventral regions of the right
hemisphere relate perceptual information to stored
biographical memories, and (iii) the anterior temporal cortex of both hemispheres acts as a depository
of biographical memories. The authors emphasized
the role of the right hemisphere in face recognition
and considered the role of the left hemisphere as
complementary.
In the present study, three subjects demonstrating
the face-specific response showed it unilaterally in the
right hemisphere and in only one was the signal
bilateral. Our subjects were looking at the faces
with no particular task. In studies reporting bilateral
activation during face recognition, the subjects
have performed some type of stimulus discrimination.3,17,39 We suggest that the present type of
‘‘passive’’ viewing task favors the global, configurational processing of facial features, suggested to be a
function of the right hemisphere.7,26,31,35,38 Our
conclusion is that the present results, together with
lesion data and PET studies, suggest a dominance
of the right inferior temporal cortex in global
visuoperceptual face processing.
Acknowledgements—This study was supported by the
Academy of Finland. We thank Veikko Jousmäki and Satu
Tissari for help in the analysis of MRI data.
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(Accepted 16 July 1996)