A Common Cortical
A Common Cortical
A Common Cortical
Behavioral/Cognitive
Distance describes more than physical space: we speak of close friends and distant relatives, and of the near future and distant past. Did
these ubiquitous spatial metaphors arise in language coincidentally or did they arise because they are rooted in a common neural
computation? To address this question, we used statistical pattern recognition techniques to analyze human fMRI data. First, a machine
learning algorithm was trained to discriminate patterns of fMRI responses based on relative egocentric distance within trials from one
distance domain (e.g., photographs of objects relatively close to or far away from the viewer in spatial distance trials). Next, we tested
whether the decision boundary generated from this training could distinguish brain responses according to relative egocentric distance
within each of two separate distance domains (e.g., phrases referring to the immediate or more remote future within temporal distance
trials; photographs of participants’ friends or acquaintances within social distance trials). This procedure was repeated using all possible
combinations of distance domains for training and testing the classifier. In all cases, above-chance decoding across distance domains was
possible in the right inferior parietal lobule (IPL). Furthermore, the representational similarity structure within this brain area reflected
participants’ own judgments of spatial distance, temporal soon-ness, and social familiarity. Thus, the right IPL may contain a parsimo-
nious encoding of proximity to self in spatial, temporal, and social frames of reference.
Key words: egocentric distance; inferior parietal lobule; multivoxel pattern analysis; psychological distance; social cognition; temporo-
parietal junction
Figure 1. Experimental paradigm. A–C, Examples of each trial type. Within each trial, stimulus change over time was analogous to “movement” either toward or away from the observer in a
spatial, temporal, or social frame of reference. A, Spatial distance trials consisted of household objects photographed at different egocentric distances. B, Temporal distance trials consisted of phrases
referring to the immediate or more remote future. C, Social distance stimuli consisted of the names and photographs of four friends and four acquaintances of each participant. Experimental stimuli
contained individuals’ actual first and last names rather than the words “friend” and “acquaintance.” D, Generic trial schematic. Within each domain, two possible probes varied randomly across trials
(e.g., either “Sooner?” or “Later?” for temporal distance trials). Participants responded “Yes” or “No” with a button press. Each trial was followed by an additional 6 s of fixation before the beginning
of the next trial.
Both a shared encoding mechanism and nearby but distinct codes distance domain (e.g., spatial distance). Thus, in effect, the progression
would yield overlapping results (Peelen and Downing, 2007). of stimuli over time within each trial was analogous to “movement” by an
To determine whether different domains of egocentric dis- equivalent amount either toward or away from the participant in a spa-
tance are represented by a common code, we used information- tial, temporal, or social frame of reference.
based searchlight mapping (Kriegeskorte et al., 2006), which Trials were presented according to a slow event-related design. Each
trial was followed by 6 s of fixation and then a probe (e.g., “Later?”) that
provides a data-driven method of continuously mapping local
was intended to ensure that participants were comparing the anchor and
information content throughout the brain using multivoxel pat- target stimuli in the intended manner (i.e., in terms of relative egocentric
tern analysis (MVPA; Norman et al., 2006). Cross-domain distance and not other aspects of the stimuli). Participants responded
searchlights tested whether decision boundaries that distinguish “Yes” or “No” to the probe with a Lumina response pad regarding, in this
local response patterns based on distance within one domain example (“Later?”), whether the target phrase referred to a point in time
generalize to other domains. Additionally, we combined repre- later in the future than the anchor phrase. All probes were presented in
sentational similarity analysis (RSA; Kriegeskorte et al., 2008) black 96-point font. Each probe was followed by an additional 6 s of
with searchlight mapping to search for regions whose repre- fixation before the beginning of the next trial. Participants used the left
sentational content reflect subjective ratings of psychological response button to indicate “Yes” and the right response button to indi-
distance. cate “No.” Within each domain, there were two possible probes that
could follow each trial (i.e., either “Sooner?” or “Later?” for temporal
Materials and Methods distance trials; either “More familiar?” or “Less familiar?” for social dis-
Participants. Fifteen participants (10 females; aged 20 –28 years; mean tance trials; either “Closer?” or “Farther?” for spatial distance trials).
age, 24.6 years) completed the study. All participants were right-handed, Probes were randomized across trials so that participants could not an-
fluent in English, and had normal or corrected-to-normal vision. Partic- ticipate the correct response or formulate an appropriate motor plan
ipants provided informed consent, and the experiment was approved by until after each trial had ended. More specifically, for trials from each
the Dartmouth College Committee for the Protection of Human distance domain, because participants did not know which of the two
Subjects. possible probes would appear until several seconds after the trial had
fMRI paradigm. While being scanned in a 3 T Philips scanner, partic- ended, they could not anticipate the correct button response (i.e., a left
ipants saw spatial, temporal, and social distance trials, consisting of ob- button press for “Yes” or a right button press for “No”) during trials. This
jects photographed at different egocentric distances (Berryhill and approach also ensured that left and right response buttons were equally
Olson, 2009; Fig. 1A), words referring to the immediate or more remote likely to signify relatively near and far egocentric distances within each
future (Fig. 1B), and names and photographs of familiar others and tested distance domain throughout the experiment.
acquaintances (Fig. 1C), respectively. To make distances meaningfully Each participant’s stimulus set consisted of pictures of four friends,
comparable across domains, participants were asked to compare each four acquaintances, four relatively close objects and four relatively dis-
stimulus with a reference point or anchor from the same distance do- tant objects, as well as four verbal phrases referring to the immediate
main. More specifically, each trial began with a briefly presented (500 future and four verbal phrases referring to the more remote future. All
ms) anchor from the same stimulus domain as a target stimulus that was four friend pictures preceded and followed all four acquaintance pictures
presented for the majority of the trial (1500 ms). Participants were asked an equal number of times during social distance trials, all four photo-
to think about how much closer or farther, more or less familiar, or graphs of close objects preceded and followed all four photographs of
sooner or later the target was relative to the anchor during spatial, social, distant objects an equal number of times during spatial distance trials,
and temporal distance trials, respectively. Different trial types within a and all four phrases referring to the immediate future preceded and
domain (e.g., closer and farther spatial distance trials) contained the followed all four phrases referring to the remote future an equal number
same stimuli in reverse order such that the direction (i.e., either toward of times during temporal distance trials. This yielded a total of 96 unique
or away from the self) of relative egocentric distance changes over time, trials per participant. Each run consisted of 36 trials (six instances of each
but not the magnitude of these changes (e.g., 250 cm for spatial distance of six trial types: closer, farther, sooner, later, more familiar, less famil-
trials), differed between trial types (e.g., closer vs farther) within each iar). Within runs, trials were presented in a pseudorandom order to
Parkinson et al. • Spatial, Temporal, and Social Distance J. Neurosci., January 29, 2014 • 34(5):1979 –1987 • 1981
approximate second-order counterbalancing of trial type (i.e., closer, and 7 (the image/phrase on the left is a great deal sooner/closer/more
farther, sooner, later, more familiar or less familiar). Counterbalanced familiar). Distance ratings for trials containing the same stimulus pairs in
trial type orders were filled with specific trials by drawing randomly reverse order were assigned the same numerical ratings multiplied by ⫺1.
without replacement from lists of all trials belonging to each trial type, One participant completed both this questionnaire and a questionnaire
with each trial repeated three times. Thus, each unique trial was repeated with stimuli presented in reverse order that asked for ratings between 1
three times over the course of eight functional runs. (equally late/far/familiar) and 7 (the image/phrase on the left is a great
Spatial distance stimuli. All stimuli and probes were presented against deal later/farther/less familiar). Ratings did not differ between the two
a light gray 1280 ⫻ 600 pixel background (Fig. 1A). Spatial distance versions of the questionnaire.
stimuli came from a preexisting stimulus set depicting common house- Image acquisition. Participants were scanned at the Dartmouth Brain
hold objects either 50 or 300 cm away amid a naturalistic background Imaging Center using a 3 T Philips Achieva Intera scanner with a 32-
containing strong monocular depth cues (Berryhill and Olson, 2009). channel head coil. An echo-planar sequence (35 ms TE; 2000 ms TR;
These stimuli were tested previously to ensure that viewers perceive them 3.0 ⫻ 3 0.0 ⫻ 3.0 mm resolution) was used to acquire functional images,
to be at the intended egocentric distances and have been demonstrated with 291 dynamic scans per run, for a total acquisition time of 582 s per
previously to automatically elicit egocentric distance processing (Berry- run. A high-resolution T1-weighted anatomical scan (8200 ms TR; 3.7
hill and Olson, 2009). Retinal subtense was approximately consistent ms TE; 0.938 ⫻ 0.938 ⫻ 1.0 mm resolution) was acquired at the end of
across near and far pictures, because stimuli were drawn from four image the scanning session. Foam padding was placed around subjects’ heads to
pairs that depicted similar objects of different sizes (e.g., circular breads: minimize motion.
a mini pita and a pizza shell), with the larger and smaller objects photo- Image preprocessing. Functional data were preprocessed, and parame-
graphed at distances of 300 and 50 cm, respectively. The images used in ter estimates ( values) were obtained for each of the six trial types in
the current study depicted spoons, round breads, beverage pitchers, and each run using AFNI (Cox, 1996). Data were time shifted to correct for
round yellow fruits. interleaved slice order, and each volume was spatially registered to the
Temporal distance stimuli. Temporal distance stimuli consisted of ver- volume immediately preceding the high-resolution anatomical scan.
bal phrases referring to the immediate or more remote future. Previous Next, data were despiked to remove transient, extreme values in the
work suggests that words describing relatively proximal and distal tem- signal not attributable to biological phenomena and were spatially
poral entities are automatically processed in terms of egocentric psycho- smoothed using a 4 mm full-width at half-maximum Gaussian kernel.
logical distance (Bar-Anan et al., 2006, 2007). To ensure readability of Each voxel time series was scaled to a mean amplitude of 100. Next,
these quickly transitioning stimuli, the anchor and target phrases were parameter estimates were extracted for each voxel using the general linear
presented in different font colors: the anchor phrase was always pre- model (GLM). Stimulus events were defined as the 2 s trial period begin-
sented in orange text, and the target phrase was always presented in blue ning with the onset of the 0.5 s presentation of the anchor and ending at
text (Fig. 1B). Phrases were presented in 96-point font. Remote future the conclusion of the 1.5 s presentation of the target and were convolved
phrases were: “A YEAR FROM NOW”; “DECADES FROM NOW”; “A with the standard hemodynamic response function. The GLM included
MONTH FROM NOW”; “IN A FEW YEARS.” Immediate future phrases six predictors, one for each trial type, and six regressors of no interest
were: “IN A FEW SECONDS”; “MOMENTS FROM NOW”; “IN AN (motion parameters), resulting in an estimate of the response of each
INSTANT”; “A MINUTE FROM NOW.” Wilcoxon’s rank-sum tests voxel to each trial type within each run for use in classification analyses.
(function wilcox.test in R; R Core Team, 2013) indicated that word For RSA and univariate analyses, deconvolution was performed on con-
counts in immediate (median, 3.50) and remote (median, 4.00) future catenated data from all eight runs. Gray matter segmentation of each
phrases did not significantly differ (W ⫽ 10, p ⫽ 0.61, r ⫽ 0.18). Letter participant’s anatomical image was performed using FreeSurfer (Fischl et
counts also did not significantly differ between immediate (median, al., 2004). Gray-matter masks were aligned to anatomical images after the
13.50) and remote (median, 12.50) future phrases (W ⫽ 6, p ⫽ 0.65, r ⫽ alignment of the anatomical images to functional data and then resa-
0.16). Additionally, the number of plural nouns was exactly matched mpled to the resolution of the functional data.
between the two trial types (i.e., exactly two of the immediate future Classification analyses. The spatial variability of response patterns can
phrases and two of the remote future phrases contained one plural reveal information that distinguishes between experimental conditions,
noun). The frequency of all phrases and their constituent words were even in the absence of overall mean activation differences (Peelen and
obtained from the Corpus of Contemporary American English (Davies, Downing, 2007). Thus, compared with univariate analyses, MVPA can
2010), a 450 million-word corpus of spoken English, fiction, newspapers, be more sensitive to differences between trial types within domains (e.g.,
popular magazines, and academic journals from 1990 to 2012. The fre- closer vs farther trials). Additionally, MVPA can provide a more stringent
quencies of words used in the immediate (median, 1,106,896) and re- test of whether common cortical mechanisms encode egocentric distance
mote (median, 718,023) future phrases did not significantly differ (W ⫽ across domains, because overlapping univariate contrasts could result
116.5, p ⫽ 0.61, r ⫽ 0.09), nor did the frequencies of the exact immediate from a shared computational process or from the elicitation of overlap-
(median, 102) and remote (median, 291.5) future phrases used (W ⫽ 10, ping but functionally independent population responses (Peelen and
p ⫽ 0.69, r ⫽ 0.14). Downing, 2007). Thus, cross-domain distance decoding based on dis-
Social distance stimuli. Before scanning, participants provided names tributed patterns of fMRI responses provides a useful means of testing
and front-facing photographs of four people whom they know well and whether or not response patterns within a given brain region similarly
with whom they have a strong personal relationship, and of four people distinguish between relatively near and relatively far egocentric distances
whom they know well but with whom they do not have a strong friend- across distance domains.
ship or interpersonal connection. Familiar and unfamiliar others were Six spherical searchlights (radius, 3 voxels) were moved throughout
matched for gender, race, age, and facial expression (which was either each subject’s gray matter-masked data that iteratively performed cross-
neutral or slightly positive). These photographs were cropped to include domain distance decoding (Fig. 2A–C) on local fMRI response patterns
only the shoulders, neck, and head and were grayscaled. Photographs using PyMVPA (Hanke et al., 2009). At each searchlight center (i.e., at
were presented at a size of 400 ⫻ 400 pixels directly above the individual’s each voxel), a linear support vector machine (SVM) learning algorithm
full name in black 72-point font (Fig. 1C). was trained to discriminate local distributed patterns of fMRI responses
Postscan questionnaire. After scanning, 12 participants completed a to trials from one domain (e.g., social distance) in terms of relative psy-
paper-and-pencil questionnaire consisting of behavioral ratings of psy- chological distance (e.g., more vs less familiar) within data from seven of
chological distance between stimuli. Stimuli were grouped by domain the eight functional runs and was tested on local response patterns cor-
(social, spatial, temporal); domain order was counterbalanced across responding to trials from another distance domain (e.g., temporal dis-
participants. All stimulus pairs were presented with the psychologically tance) from the left-out run. In the aforementioned example,
“closer” stimulus on the left of the psychologically “farther” stimulus. classification would be considered correct if sooner and later trials were
Participants rated the difference in psychological distance between the classified as more familiar and less familiar trials, respectively. For each
two stimuli on a 7-point scale between 1 (equally soon/close/familiar) searchlight, this procedure was repeated eight times using the data of
1982 • J. Neurosci., January 29, 2014 • 34(5):1979 –1987 Parkinson et al. • Spatial, Temporal, and Social Distance
Figure 3. RSA and results. A–C, Analysis steps. A, At each voxel, a neural RDM was generated based on pairwise correlation distances between local neural response patterns to each condition.
Behavioral RDMs were constructed for each subject using Euclidean distances between postscan distance ratings (B) and correlated with local neural RDMs at each voxel (C). D, Results. The largest
cluster in which local neural and behavioral RDMs were significantly related was in the right IPL (R IPL). Behavioral and neural RDMs were also related in the right IFG (R IFG) and left SMA (L SMA).
responding to the null hypothesis that no relationship exists between the Table 1. Regions where relative psychological distance could be decoded from local
neural and behavioral RDMs was obtained by randomly shuffling the patterns of voxel responses across all distance domains
domain labels on the behavioral RDM 1000 times and then computing Average
the correlation between the neural RDM and each of the 1000 randomly Number COG COG COG peak %
generated permutations of the behavioral RDM. Next, the inverse of the Hemisphere Location BA of voxels x y z accuracy
cumulative normal distribution was calculated to convert the resultant p
values into z scores (Connolly et al., 2012). Z-statistic maps describing R IPL (AG), STG 39, 22 273 61 ⫺39 9 62.33
the relationship between the similarity structure of each participant’s L, R LG, CUN 18 200 0 ⫺77 5 66.12
behavioral ratings of distance for each trial type and the similarity struc- R IPL (SMG) 40 70 59 ⫺46 21 65.18
ture of local distributed fMRI response patterns corresponding to each R IPL (SMG) 40 29 62 ⫺35 31 61.30
trial type were aligned to standard space (Talairach and Tournoux, 1988) R IPL (AG) 39 24 54 ⫺59 26 62.19
and submitted to a group analysis (one-sample t test against a z score of 0) R IPL (SMG) 40 21 60 ⫺38 26 66.01
in AFNI (Cox, 1996). R STG, IPL (SMG) 42, 40 15 61 ⫺28 16 60.49
Conventional univariate analyses. A standard univariate analysis using All presented results are significant at an FDR-corrected threshold of p ⬍ 0.05 (two-tailed) for each of six statistical
the GLM was performed in AFNI (Cox, 1996) to determine whether the tests (corresponding to significance tests for accuracy maps derived from using all possible pairs of the three tested
distance domains for training and testing data). To obtain average peak accuracy values, a mask of each of these
MVPA results merely reflected differences in the overall average magni- clusters was applied to average accuracy maps for each of the six tests, and peak percentage accuracies were
tude of responses to closer, sooner, and more familiar trials compared averaged across tests for each cluster. BA, Brodmann’s area; COG, center of gravity; R, right; L, left; LG, lingual gyrus;
with farther, later, and less familiar trials, respectively. Voxelwise param- CUN, cuneus. All coordinates are in Talairach space.
eter estimates generated from concatenated data from all eight runs were
submitted to three paired t tests (sooner vs later; closer vs farther; more Table 2. Regions where behavioral and local neural RDMs were significantly
familiar vs less familiar) using the AFNI program 3dttest⫹⫹. To deter- correlated
mine whether any brain areas could distinguish between closer and far- Number COG COG COG Peak Peak Peak
ther trials, sooner and later trials, and more familiar and less familiar Hemisphere Location BA of voxels x y z x y z
trials based solely on the overall magnitude of local voxel responses, a
conjunction analysis was performed on the statistical maps resulting R IPL (AG, SMG) 39, 40 113 47 ⫺54 36 48 ⫺55 36
from each of these three t tests, using a threshold of p ⬍ 0.05, FDR L SMA 6 43 ⫺17 ⫺3 60 ⫺18 ⫺2 59
corrected, for each test. R IFG 47 35 23 15 ⫺11 23 16 ⫺11
L SMA 6 16 ⫺7 13 60 ⫺8 12 59
L SMA 6 13 ⫺17 2 63 ⫺17 1 63
Results All presented results are significant at an FDR-corrected threshold of p ⬍ 0.05 (two-tailed). BA, Brodmann’s area;
Behavioral results COG, center of gravity; R, right; L, left. All coordinates are in Talairach space.
Results of postscan written questionnaires confirmed that partic-
ipants perceived stimuli pairs from trials in all domains to differ
substantially in terms of relative egocentric psychological dis-
tance. Mean ⫾ SD ratings of perceived egocentric distance differ- RSA results
ences on a scale from 1 (equally soon/close/familiar) to 7 (one Representational content within a large cluster in the right IPL
image/phrase is a great deal sooner/closer/more familiar) were was significantly related to behavioral distance ratings, suggesting
6.21 ⫾ 0.70, 6.29 ⫾ 0.82, and 6.52 ⫾ 0.62 for closer, sooner, and that population codes within searchlights centered in this area
more familiar trials, respectively. One-sample t tests indicated contain representations that reflect subjective perceptions of ego-
that distance ratings for stimulus pairs from each domain signif- centric distance. As summarized in Table 2, the local neural sim-
icantly differed from 1 (equally soon/close/familiar; all p values ilarity structure in smaller clusters within the right inferior
⬍0.00001). A one-way ANOVA indicated that perceived relative frontal gyrus (IFG) and throughout the left supplementary motor
psychological distance did not significantly differ across the three area (SMA) were also significantly related to the similarity struc-
tested domains of psychological distance (F(2,22) ⫽ 1.94, p ⫽ 0.17, tures evinced in participants’ behavioral ratings of distance, sug-
G2 ⫽ 0.09). Additionally, response accuracies to probes during gesting that information contained in local population codes
scanning were high, suggesting that participants were able to at- within these regions may also be related to judgments of rela-
tend to and compare the anchors and targets in the intended tive egocentric social, spatial, and temporal distance. Addi-
manner during scanning. Run accuracies ranged from 95.83 to tional details regarding all significant clusters ( p ⬍ 0.05, FDR
100% (mean ⫾ SD, 97.97 ⫾ 1.34%). corrected; cluster size ⬎10 voxels) from this analysis are de-
scribed in Table 2.
Classification results
Clusters (cluster size ⬎10 voxels) in which relative egocentric Univariate results
distance could be decoded across all possible pairwise combina- No voxels survived an FDR-corrected threshold of p ⬍ 0.05 in
tions of distance domains are presented in Table 1. All voxels in any of the three t tests comparing trials based on distance within
each of these clusters were associated with significantly above- each distance domain (i.e., sooner vs later; more familiar vs less
chance classification across participants for each of the six group familiar; closer vs farther). Even using a dramatically reduced
analyses ( p ⬍ 0.05, FDR corrected, each test). Specifically, rela- voxelwise threshold of p ⬍ 0.01, uncorrected, for each test, no
tive egocentric distance could be decoded across all distance do- regions emerged as significant in the conjunction analysis, sug-
mains above chance across participants in searchlight spheres gesting that no regions could distinguish distances in all three
centered on voxels in a large (273-voxel) cluster in the right distance domains tested here in terms of average activity level.
inferior parietal lobule (IPL) extending into the posterior su- This suggests, at least at the current level of observation, using the
perior temporal gyrus (STG; Fig. 2D). Cross-domain distance current experimental paradigm, that the local distributed pat-
decoding was also possible in smaller clusters throughout the terns, rather than average magnitude, of fMRI responses con-
right IPL, spanning both the supramarginal (SMG) and angu- tain information that distinguishes between different relative
lar (AG) gyri, as well as in one cluster in medial occipital egocentric distances across social, spatial, and temporal dis-
cortex, as summarized in Table 1. tance domains.
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