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A neurobiological enquiry into the origins of our experience of the sublime and beautiful

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Philosophies of aesthetics have posited that experience of the sublime—commonly but not exclusively derived from scenes of natural grandeur—is distinct from that of beauty and is a counterpoint to it. We wanted to chart the pattern of brain activity which correlates with the declared intensity of experience of the sublime, and to learn whether it differs from the pattern that correlates with the experience of beauty, reported in our previous studies (e.g., Ishizu and Zeki, 2011). 21 subjects participated in a functional magnetic resonance imaging experiment. Prior to the experiment, they viewed pictures of landscapes, which they rated on a scale of 1–5, with 5 being the most sublime and 1 being the least. This allowed us to select, for each subject, five sets of stimuli—from ones experienced as very sublime to those experienced as not at all sublime—which subjects viewed and re-rated in the scanner while their brain activity was imaged. The results revealed a distinctly different pattern of brain activity from that obtained with the experience of beauty, with none of the areas active with the latter experience also active during experience of the sublime. Sublime and beautiful experiences thus appear to engage separate and distinct brain systems.
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ORIGINAL RESEARCH ARTICLE
published: 11 November 2014
doi: 10.3389/fnhum.2014.00891
A neurobiological enquiry into the origins of our
experience of the sublime and beautiful
Tomohiro Ishizu*and Semir Zeki*
Wellcome Laboratory of Neurobiology, Division of Biosciences, Department of Cell and Developmental Biology, University College London, London, UK
Edited by:
Oshin Vartanian, Defence Research
and Development Canada, Canada
Reviewed by:
Evgeny Gutyrchik,
Ludwig-Maximilians-Universität,
Germany
Marcos Nadal, University of Vienna,
Austria
*Correspondence:
Tomohiro Ishizu and Semir Zeki,
Wellcome Laboratory of
Neurobiology, Division of
Biosciences, Department of Cell and
Developmental Biology, University
College London, Anatomy Building,
Gower Street, London WC1E
6BT, UK
e-mail: t.ishizu@ucl.ac.uk;
s.zeki@ucl.ac.uk
Tomohiro Ishizu is a Fellow of the
Japan Society for the Promotion of
Science (JSPS).
Philosophies of aesthetics have posited that experience of the sublime—commonly but
not exclusively derived from scenes of natural grandeur—is distinct from that of beauty and
is a counterpoint to it. We wanted to chart the pattern of brain activity which correlates with
the declared intensity of experience of the sublime, and to learn whether it differs from
the pattern that correlates with the experience of beauty, reported in our previous studies
(e.g., Ishizu and Zeki, 2011). 21 subjects participated in a functional magnetic resonance
imaging experiment. Prior to the experiment, they viewed pictures of landscapes, which
they rated on a scale of 1–5, with 5 being the most sublime and 1 being the least. This
allowed us to select, for each subject, five sets of stimuli—from ones experienced as very
sublime to those experienced as not at all sublime—which subjects viewed and re-rated
in the scanner while their brain activity was imaged. The results revealed a distinctly
different pattern of brain activity from that obtained with the experience of beauty, with
none of the areas active with the latter experience also active during experience of the
sublime. Sublime and beautiful experiences thus appear to engage separate and distinct
brain systems.
Keywords: beauty, emotion, fMRI, neuroesthetics, sublimity
INTRODUCTION
When Edmund Burke (1757) published A Philosophical Enquiry
into the Origin of Our Ideas of the Sublime and Beautiful,of
which our title is an imitation, he was removed by centuries
from early speculations on the origins of the sublime and its
experience. History traces those origins to Longinus, a Greek
philologist of doubtful existence also known as pseudo Longinus,
who thought of the sublime as “a certain loftiness and excellence
of language” (Havel, 2006). While acknowledging that “words
have as considerable a share in exciting ideas of beauty and of
the sublime” (Burke, 1757,5:I),forBurkeandothersduring
the Enlightenment, the trigger for the experience of the sub-
lime shifted toward a more sensory base. Now the sublime was
found in the experience of Nature and its uncontrollable forces:
the untameable power of oceans, the grandeur of mountains, the
terror of erupting volcanoes, and the vastness of deserts became
some of its principal sources. Yet a common theme across the
centuries dividing Longinus from Burke was that the source of
the experience was traceable to the workings of the mind, rather
than the objects of Nature exclusively. Critical to that experi-
ence was the involvement of the imagination and the process
of completion, since it posited a profound interaction between
the apprehended object and its completion by the recipient;
the sublimity lay beyond the power of the senses and there-
fore recruited the power of the imagination. Longinus wrote that
“sublime thoughts belong properly to the loftiest minds.Kant
(1790/1986), somewhat more emphatically, stated that sublimity
“is not contained in anything in nature, but only in our mind”
(§28, 264), giving an example from mathematics where, “to be
able to think the infinite as a whole indicates a mental power that
surpasses any standard of sense” (§26, 255). Here, then, was a
critical difference from the experience of beauty, for which there
was a more equitable division, especially in the Platonic tradition,
between sensory experience and the characteristics of the appre-
hended object. These objects and Ideas had, for Plato, an existence
independent of humans even though they could only be accessed
through a thought process.
A greater emphasis on the imagination is not the sole char-
acteristic separating the experience of the beautiful from that of
the sublime. While beauty came to be associated with feelings of
pleasure, reward, and satisfaction, the sublime was associated with
awe, fear and terror, because “Whatever therefore is terrible, with
regard to sight, is sublime too” (Burke, 1757,2:II).But,signi-
cantly, these feelings were read into scenes from a safe distance.
The sublime was associated, above all, with the obscure and the
uncertain, with “some sort of approach toward infinity” (Burke,
1757,2:IV).
These differences, listed by Burke, Kant, and Schopenhauer
among others, are impressive and compelling. In pursuing our
studies of the neurobiology of aesthetic experiences, we therefore
thought it interesting to enquire whether they are also mirrored
in the pattern of brain activity that correlates with the two expe-
riences. We naturally approached our experimental project with
diffidence. However, compelling the differences between the two
Frontiers in Human Neuroscience www.frontiersin.org November 2014 | Volume 8 | Article 891 |1
HUMAN NEUROSCIENCE
Ishizu and Zeki Experience of the sublime and the beautiful
experiences may be at the extremes, there remain many experi-
ences, of which the Pietà of Michelangelo at St Peter’s Basilica is
a supreme example, which are easy to characterize as both beau-
tiful and sublime. Indeed, Schopenhauer (1844, I: 289) resorted
to giving different categories of the sublime, in terms of inten-
sity of experience. Acknowledging these difficulties, we tailored
our experiment so that each subject characterized the inten-
sity of the experience of the sublime individually. Given the
dominance accorded by philosophers of aesthetics to natural
scenes in the experience of the sublime, we restricted ourselves
to studying the experience of the sublime when aroused by
such scenes. We then undertook a parametric imaging study of
the strength of activity in the implicated brain areas, in rela-
tion to the declared intensity of the experience of the sublime.
In light of the distinctions made in the philosophy of aesthet-
ics between the experience of the beautiful and that of the
sublime, we hypothesized that there would be a significant dif-
ference in the pattern of activation that correlates with the two
experiences.
MATERIALS AND METHODS
PARTICIPANTS
Twenty-one healthy right-handed volunteers (11 males; 10
females; mean age, 26.6 years) coming from different cultures
and ethnic backgrounds (3 Chinese, 4 Indian, 6 Japanese, 2
Pakistani, and 6 West Europeans) participated. All had normal
or corrected-to-normal vision, and none had a history of neu-
rological or psychiatric disorder. Written informed consent was
obtained from all participants. The study was approved by the
Ethics Committee of University College London. All data were
anonymized.
PRELIMINARY BEHAVIORAL TESTING AND POST-SCANNING RATINGS
Prior to the scanning sessions, psychophysical tests were con-
ducted to select stimuli which were subsequently used in the
scanning sessions; this allowed subjects to classify the visual stim-
uli into five groups according to the intensity with which they
experienced them- 5 corresponding to “very sublime,” 1 to “not
at all sublime” and the others falling in between. These ratings
allowed us to balance the sequence of stimuli for each partici-
pant in order to achieve an even distribution of visual stimuli
of all 5 ratings during the scanning sessions. During a first visit
to the laboratory, between 2–5 days prior to scanning, each sub-
ject was instructed about the experiment and rated the stimuli as
described above. Each viewed 232 photographs of natural scenes
from the National Geographic Magazine available on the inter-
net; these included pictures of mountains, falls, forests, volcanoes,
tornadoes, ocean waves, glaciers, clouds, and deserts, that is to
say the type of stimuli which have been considered in literature
to evoke feelings of the sublime. Stimuli remained on the screen
until participants responded, after which an inter-trial interval
of 1 s followed. Based on the responses of each participant dur-
ing the preliminary psychophysical testing, we selected—for each
participant—35 stimuli corresponding to each of the 5 categories,
making a total of 175 stimuli which each participant viewed in
the scanner. Immediately after scanning, each participant was
asked to report their affective feelings with regards to the “beauty,”
“pleasantness,” and “scale” of each stimulus that they had viewed
in the scanner, on a scale of 1 to 5 (ugly to beautiful for “beauty,”
fearful to pleasant for “pleasantness,” and 5 to 1 (small to grand
for “scale”). We chose a reverse rating for scale, because it has
been posited in philosophies of aesthetics that large scales (sizes)
are more characteristic of the sublime, while small ones are more
characteristic of the beautiful (Burke, 1757, 3: XXVII).
STIMULI
Stimuli were generated with Cogent 2000 (http://www.vislab.
ucl.ac.uk/cogent_2000.php) running in MATLAB (MathWorks,
Natick, MA, USA). They were back-projected onto a screen, by
useofanLCDprojector,throughanangledmirror.Thereso-
lution of the screen was 1400 ×1050 pixels; the height of each
stimulus was 19,andthewidthvaried.
The session began with subjects viewing a flat black screen
for 20 s to allow for T1 equilibration effects to subside (the cor-
responding first six brain volumes were discarded). After this
20 s blank period, an instruction about the sublimity judgment
appeared on the screen, to inform participants that a session had
started. A fixation point was then presented at the center of the
screen for 1 s against a black background, following which visual
stimuli were presented in a pseudorandom order for 5 s. This was
followed by an interval of 5–7 s, during which the participants
responded.
Following each stimulus presentation, participants were asked
to rate them on a five Likert scale as in the preliminary testing,
by pressing one of five buttons with their right five fingers. The
response period lasted 5–7 s and participants could make their
rating at any time during that period. The session ended with
a blank period of 20 s, during which the scanner continued to
acquire blood-oxygen-level dependent (BOLD) signals. The stim-
uli were presented in 7 sessions. Each session consisted of 22
stimuli, presented in pseudorandom order, with a 20 s resting
period between first and last 11 trials, during which participants
were instructed not to close their eyes. Prior to the scanning, par-
ticipants had a short practice session with different visual stimuli
to those used in the scanning session.
FUNCTIONAL MAGNETIC RESONANCE IMAGING (fMRI) SCANNING
Scanning data were acquired in a 3-T Siemens Magnetom
Trio magnetic resonance imaging scanner (Siemens, Erlangen,
Germany) fitted with a 12-channel head-coil. An echo-planar
imaging (EPI) sequence was applied for functional scans to obtain
BOLD signals (echo time, 30 ms; repeat time, 3.36 s), using 48
slices to cover the whole brain. The voxel resolution was 3 ×3-
mm in-plane resolution, with a 2 mm slice thickness and 1-mm
inter-slice gap. Magnetic resonance imaging signal losses in the
orbitofrontal cortex (OFC) and amygdala were reduced by apply-
ing a z shim gradient moment and slice tilt (Weiskopf et al.,
2006). T1-weighted anatomical images were acquired at the end
of experimental sessions for each subject (176 slices; resolution,
1×1×1 mm; echo time, 2.48 ms; repeat time, 7.92 ms). Field
maps were also acquired with Siemens standard gradient-echo
field map sequence to correct geometric distortion of EPI images
(Hutton et al., 2002). We also recorded the heart and respiration
rates for each subject.
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Ishizu and Zeki Experience of the sublime and the beautiful
fMRI DATA ANALYSIS
All data were analyzed with SPM8 (Statistical Parametric
Mapping, http://www.fil.ion.ucl.ac.uk/spm/software/spm8/).
The EPI images for each subject were realigned and normalized
into Montreal Neurological Institute (MNI) space, smoothed
with a Gaussian smoothing kernel of 9 ×9×9 mm, and filtered
with a high-pass cut-off (128 s) to remove drift terms. The stimu-
lus for each subject was modeled as a set of regressors in a general
linear model first-level (within subject) analysis. The stimulus
was a block design, and boxcar functions were used to define
stimulus functions; these modeled the onsets and durations of
the visual stimuli. Head movement parameters calculated from
the realignment pre-processing step, physiological recordings,
and the response periods were included as regressors of no
interest. Stimulus functions were convolved with a canonical
haemodynamic response function.
To analyze the data for parametric modulation according to
intensity of experience, sublimity rated stimuli were used as
regressors, with sublimity rating as the parametric modulator.
Ratings were coded as 1, 2, 3, 4, and 5 for “not at all sublime”
to “very sublime,” and a 1st order polynomial expansion was
included. Contrast images for visual presentations and sublim-
ity ratings were taken to second-level (random effects) analysis
to produce summary statistical t-maps at the group level. In
order to study de-activations produced by viewing the stimuli,
we classified the latter as follows: stimuli given ratings of 1–2 as
“Not sublime,” 3 as “Mid sublime,” and 4–5 as “Very sublime,
which allowed us to examine the de-activations produced by these
three groupings relative to baseline. We carried out a categorical
analysis of sublime rating, by coding contrasts for Very sublime,
Mid sublime, Not at all sublime vs. Baseline for each subject at
the first-level and taking these to a second-level, random effects,
analysis.
We report cluster level activations that were significant at
p<0.05 FWE (family wise error) corrected, although some of
these were also significant at the voxel level.
RESULTS
BEHAVIORAL DATA
The percentage distribution of rating during the scanning exper-
iment averaged over all participants for each of the five ratings of
sublimity is 17.3% for 1 (SD =7.81), 19.3% for 2 (SD =9.28),
20.7% for 3 (SD =7.21), 23.3% for 4 (SD =9.00), and 19.5%
for 5 (SD =10.32). Thought not perfect, the distribution nev-
ertheless provided a reasonable ratio between categories for the
analyses.
Rating according to experienced sublimity carries with it cer-
tain confounds, since “In the infinite variety of natural combi-
nations we must expect to find the qualities of things the most
remote imaginable from each other united in the same object”
(Burke, 1757, 3: XXVII). Chief among these is beauty, since stim-
uli experienced as sublime can also be experienced as beautiful
or sometimes even ugly. In addition, sublimity often has fear
and grandeur (magnitude or scale) attached to it. We therefore
thought it wise to ask participants, after the scanning sessions,
to rate the stimuli that they had viewed in the scanner along
the three axes of beautiful—ugly, pleasant—unpleasant (fearful)
and small—grand, each on a scale of 1 to 5 (but note that, as
mentioned under Methods, we used a reverse rating for scale,
compared to those sublime, beautiful, and pleasant). The fre-
quency distribution of post-scan ratings for experiences besides
sublimity (that is, those of beauty, pleasantness, and scale), pro-
duced by viewing the same stimuli as the ones in the scanner, are
presented in Figure 1 and Ta bl e 1. Correlation analyses between
ratings according to sublimity and each of the three post-scan rat-
ings (Tab l e 1 ) shows that sublimity ratings correlated positively
with beauty (Pearson correlation, r=0.520, p<0.001, 2-tailed),
weakly with pleasantness ratings (r=0.136, p<0.001), and
had a significant negative correlation with scale (r=−0.534,
p<0.001).
BRAIN ACTIVATIONS CORRELATING WITH EXPERIENCE OF THE
SUBLIME
Our primary interest was to determine the brain activity that
correlates with the declared intensity of experiences qualified as
sublime. A number of brain areas, cortical and subcortical, were
found to have been parametrically active when sublime ratings
were used as modulators (see Tab le 2 and Figure 2). The corti-
cal areas were the inferior temporal cortex (encroaching upon
fusiform gyrus and the lateral occipital complex (LOC), the pos-
terior hippocampus, and the inferior/middle frontal gyri. The
sub-cortical cortical areas were the basal ganglia (head of caudate
and putamen). There was, in addition, prominent involvement of
the cerebellum.
DEACTIVATIONS
Next, we investigated which brain areas were deactivated rela-
tive to baseline, using the following contrasts: very sublime <
baseline, mid sublime <baseline, and not sublime <base-
line. The results, summarized in Tab l e 2 and Figure 2, show
that all contrasts give significant deactivations in a number of
areas. These include the anterior part of cingulate cortex/medial
prefrontal cortex, anterior superior temporal sulcus, parts of
the cerebellum, and the caudate (tail and body). The signifi-
cant deactivations in posterior cingulate cortex/precuneus and
superior frontal gyrus were only obtained with stimuli rated as
very sublime.
Deactivations in the cerebellum could be dissociated from the
activations in it (peak voxels for deactivation, 24 82 32/
21 76 35; for activation, 30 61 47/27 64 44,
Figure 3).
COMPARISON OF BRAIN AREAS WHOSE ACTIVITY CORRELATES WITH
THE EXPERIENCE OF THE SUBLIME AND THAT OF THE BEAUTIFUL
Another of our aims was to learn about differences between the
neural correlates of the experience of the beautiful and the sub-
lime. We therefore compared the regions engaged during the
experience of beauty in our previous study (Ishizu and Zeki,
2011) with the regions engaged in the present one, by superim-
posing the pattern obtained in the former study onto the one
obtained in the latter (Figure 4). A glance at this figure shows the
profound difference in neural activity that correlates with the two
experiences. In particular, field A1 of mOFC, in which activity
correlates parametrically with the declared experience of beauty
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Ishizu and Zeki Experience of the sublime and the beautiful
FIGURE 1 | Behavioral data summed over 21 subjects. (Upper left) Frequency distribution of sublimity rating over post-scan beauty rating, (upper right) over
post-scan pleasantness rating, (bottom) over post-scan scale rating, with a fitted linear regression. Size of each circle is proportional to the number for that rating.
Table 1 | The results of correlation analyses derived from the
behavioral data over 21 subjects.
Sublime Beautiful Pleasant Scale
Sublime Pearson Correlation 1 0.520** 0.136** 0.534**
Sig. (2-tailed) 0.000 0.000 0.000
N2618 2618 2618 2618
Beautiful Pearson Correlation 0.520** 1 0.452** 0.545**
Sig. (2-tailed) 0.000 0.000 0.000
N2618 2618 2618 2618
Pleasant Pearson Correlation 0.136** 0.452** 10.174**
Sig. (2-tailed) 0.000 0.000 0.000
N2618 2618 2618 2618
Scale Pearson Correlation 0.534** 0.545** 0.174** 1
Sig. (2-tailed) 0.000 0.000 0.000
N2618 2618 2618 2618
**p<0.001.
derived from different sources (Ishizu and Zeki, 2011, 2013; Zeki
et al., 2014,inter alia) was not active in the current study, while
other regions, notably the head of the caudate, the putamen, and
the posterior hippocampus, in which activity has been recorded
as correlating with experiences of pleasure, hate, and memory,
respectively, were also active with the experience of sublimity.
Taken together, these results indicate that aesthetic (beauty)
experiences and experience of the sublime engage separate and
distinct brain systems.
DISCUSSION
The sublime and its experience occupy a prominent place in
philosophical discourse on aesthetics and are often considered
as constituting a counterpoint to beauty and its experience. It
seems natural, then, that a study of the neural correlates of the
experience of beauty should lead ineluctably to a study of its
counterpart, the experience of the sublime. Both are topics that
are fraught with difficulty and hence our diffidence in approach-
ing the subject and undertaking this study. Any exhaustive study
of the sublime would have to consider fields as diverse as rhetorics,
tragedy, mathematics, nature, and divinity, all of which have been
considered to lead to that sense of elevation [Erhebung ]that
Schopenhauer (1844) wrote of. We tried to render our study more
manageable by concentrating on natural scenes, partly because
they have occupied such a paramount place in discussions of the
sublime and partly because they enabled us to restrict the range
of stimuli that we employed in our study. The experience of the
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Ishizu and Zeki Experience of the sublime and the beautiful
Table 2 | Location, MNI coordinates, cluster size and values for the activations produced by the parametric modulation with sublimity ratings
and deactivations produced by the contrasts sublime <baseline.
Activations Cluster Peak
L/R p(FEW) kE p(unc) p(FWE) TZp(unc) XYZ
Posterior hippocampus L 0.000 1369 0.000 0.000 11.97 6.51 0.000 24 31 1
Inferior temporal cortex/fusiform gyrus R 0.000 8.98 5.69 0.000 45 58 5
0.060 5.98 4.52 0.000 30 22 28
Inferior termporal cortex/fusiform gyrus L 0.000 1648 0.000 0.000 9.14 5.74 0.000 48 55 8
Caudate(head) R 0.002 7.96 5.35 0.000 9 23 16
Putamen R 0.003 7.72 5.26 0.000 18 75
Cerebellum L 0.001 272 0.000 0.005 7.40 5.14 0.000 30 61 47
Celebellum L 0.031 6.36 4.70 0.000 21 70 44
0.074 5.86 4.46 0.000 12 55 50
Inferior/midd1e fronta1 gyrus L 0.015 146 0.003 0.038 6.24 4.64 0.000 39 35 10
0.111 5.62 4.34 0.000 54 35 13
0.660 4.39 3.65 0.000 42 50 19
Cerebellum R 0.057 97 0.013 0.045 6.14 4.60 0.000 27 64 44
Deactivations Cluster Peak
p(FWE) kE p(unc) p(FEW) TZp(unc) XYZ
Caudate (tall) R 0.000 235 0.000 0.000 10.49 65535 0.000 21 43 19
0.004 5.60 5.00 0.000 33 43 4
0.007 5.42 4.87 0.000 27 25 31
Anterior cingulate cortex R 0.000 874 0.000 0.000 9.49 7.39 0.000 12 41 4
0.000 8.16 6.67 0.000 15 32 7
Anterior ungulate cortex/medial
prefrontal cortex
R 0.000 6.85 5.87 0.000 9 62 1
Anterior superio tempora1 sulcus R 0.000 236 0.000 0.000 8.31 6.75 0.000 54 10 8
0.001 5.99 5.28 0.000 63 25 8
0.001 5.97 5.26 0.000 54 14 29
Anterior superio tempora1 cortex L 0.000 148 0.000 0.000 7.53 6.29 0.000 51 16 8
0.000 7.09 6.02 0.000 54 711
Cerebellum L 0.000 103 0.000 0.000 7.46 6.25 0.000 24 82 32
0.000 167 0.000 0.000 7.19 6.08 0.000 27 43 10
Caudate (tail) L 0.000 6.83 5.85 0.000 18 46 22
0.000 6.25 5.47 0.000 12 34 22
Cerebellum R 0.000 78 0.002 0.000 7.10 6.03 0.000 21 76 35
0.000 6.98 5.95 0.000 18 85 32
Caudate (body) L 0.000 66 0.003 0.000 6.34 5.53 0.000 24 13 34
0.001 6.11 5.37 0.000 21 431
0.005 5.57 4.98 0.000 24 25 34
(Continued)
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Ishizu and Zeki Experience of the sublime and the beautiful
Table 2 | Continued
Deactivations Cluster Peak
p(FWE) kE p(unc) p(FEW) TZp(unc) XYZ
Caudate (body) R 0.002 27 0.042 0.009 5.34 4.81 0.000 21 128
0.012 5.28 4.76 0.000 21 8 25
0.031 4.96 4.53 0.000 21 13 31
DEACTIVATIONS UNIQUE TO VERY SUBLIME
Posterior cingulate cortex/precuenus 0.001 42 0.014 0.003 5.71 5.08 0.000 0 52 40
Superior frontal gyrus R 0.006 15 0.117 0.06 5.51 4.94 0.000 30 32 55
FIGURE 2 | (A) Parametric activations with sublimity. Statistical parametric
maps rendered onto canonical anatomical sections showing t-statistics.
Random effects analysis with 21 participants. Display threshold at
p<0.001 (uncorrected). I/MFG, inferior/middle frontal gyrus (39 35 10);
pHipp, posterior hippocampus (24 31 1); Fusi/ITC, fusiform
gyrus/inferior temporal cortex (48 55 8, 45 58 5); caudate (head)
(9 23 16); cerebellum (9 64 44). (B) Sites deactivated during the
experience of sublimity relative to baseline activity. Display threshold at
p<0.05 (corrected). Light blue indicates common deactivations for all
contrasts, very sublime <baseline, mid sublime <baseline, and not
sublime <baseline, and dark blue indicates sites deactivated uniquely
during the presentation of the stimuli experienced as “very sublime.
aSTS, anterior superior temporal sulcus (54 10 8/51 16 8); SFG,
superior frontal gyrus (30 32 55); ACC/mPFC, anterior cingulate
cortex/medial prefrontal cortex; (9 62 1); PCC, posterior cingulate cortex
(0 52 40); caudate (tail) (18 46 22).
sublime has a contradictory element within it, combining the
noble with horror. It was indeed the experience of the unfath-
omable grandeur of the Alps by Dennis (1693),whoexperienced
the sublime there as “mingled with Horrours, and sometimes
almost with despair,” the Earl of Shaftesbury (1709) who thought
ofitas“a wastedmountain...[appearing]...as anobleruin,and
Joseph Addison (1712) forwhomthe“Alps...fillthemindwithan
agreeable kind of horror” that were the trigger for discussions of
the sublime among those who brought the subject to prominence
in the 18th century.
“SUBLIME” AS AN INCLUSIVE TERM
One of the difficulties in addressing the neurobiology of the
sublime is that the word itself unites under a single umbrella
many different, even opposed, emotions—“fear,” “horror,” “awe,
“pleasure-pain,” and “pleasure that is only possible by means
of a displeasure” (Kant, 1790/1986, §27; 260) are some of the
characteristics ascribed to the experience of the sublime. This
is compounded by another difficulty, namely that each of these
wordscan,inaddition,describeorconveyamultitudeoffeel-
ings. “Fear,” for example, is flexible enough to apply to a variety
of emotions and yet imprecise in not specifying the more specific
emotion. Fear on viewing a face and the more detached and cog-
nitive fear experienced when viewing natural scenes of immensity
differ significantly, yet the word itself subsumes them under the
same term. The flexibility is an asset in linguistic discourse but the
imprecision is a disadvantage for scientific communication. We
here assume that the “sublime” is a distinct cognitive-emotional
complex, which involves many components but is distinct from
each individually, i.e., that the whole is other than the parts.
We emphasize this because a straightforward comparison of our
present results with past studies that have explored brain activa-
tion with various emotions, such as those of fearful human faces,
or of pain, or of pleasure, is neither straightforward nor easy.
Frontiers in Human Neuroscience www.frontiersin.org November 2014 | Volume 8 | Article 891 |6
Ishizu and Zeki Experience of the sublime and the beautiful
FIGURE 3 | Activations and deactivations in the cerebellum; yellow
shows activations (30 61 47/27 64 44) and green shows
deactivations (24 82 32/21 76 35), when an inclusive mask
covering the whole cerebellum was applied.
FIGURE 4 | Superimposed functional maps to show brain areas whose
activity correlates with the experience of visual beauty (Ishizu and
Zeki, 2011) (green) and the ones in which activity correlates with
experience of the sublime (this study, red). Activity in the body of the
caudate nucleus (91 25) and in the medial obito-frontal cortex (mOFC)
(64111) correlates with the experience of visual beauty whereas
activity in the head of the caudate, encroaching on anterior cingulate cortex,
correlates with experience of the sublime (9 23 16). Both activations are
presented using p<0.001 uncorrected threshold.
Moreover, our results did not show any activity in brain areas
such as the amygdala and the insula, which have been associated
with the experience of fear and threat (Mattavelli et al., 2013; Aube
et al., 2014) (although the great majority addressing this question
have concentrated on faces) or perceived pain (Cheon et al., 2013;
Ellingsen et al., 2013; Favilla et al., 2014), which engages the ante-
rior cingulate cortex, de-activated in our study. Hence the overall
pattern of activation in this study is significantly different from
the overall activity observed in studies dealing with pain, threat,
or fear, each one of which qualifies—at least lexically—as consti-
tuting an element in the experience of the sublime. It is therefore
perhapsfutiletogivetoorigidaninterpretationofthefunctions
of regions that were activated and de-activated in our study in
relation to past imaging study that have addressed the individ-
ual components (such as fear or surprise) which are subsumed
under the term (and experience of) of sublime. This is even more
so because, although the regions themselves can be fairly accu-
rately demarcated, a search of the literature reveals that there is
no unanimity of views on the overall functions of each of these
active regions, beyond the somewhat general statement that they
are involved in some kind of emotional experience, with some
having cognitive functions as well.
There are further difficulties even within such confines. Both
the Earl of Shaftesbury (1709) and Arthur Schopenhauer (1844),
among others, regarded the transition from the beautiful to the
sublime as graded and gradual. We circumvented this difficulty by
asking our subjects to rate the sublimity of the stimuli for them-
selves and undertook a parametric study of the relationship of
the intensity of experience of the sublime to the intensity of cere-
bral flow. We acknowledge at once that there remains another,
presently insurmountable, difficulty even when we restrict our-
selves to natural scenes, which is that subjects were asked about
their experience of the sublime in images of natural scenes within
the confines of a scanner. This inevitably limits the grandeur
and depth of the experience and of course limits our conclu-
sions too. Yet, in spite of these restrictions and difficulties, we
believe that our results give interesting insights—no more—into
the neural mechanisms that are engaged during the experience of
the sublime and how they differ from those engaged during the
experience of its counterpart, namely beauty.
CORTICAL AREAS IN WHICH ACTIVITY CORRELATES PARAMETRICALLY
WITH THE DECLARED INTENSITY OF EXPERIENCE OF THE SUBLIME
The posterior hippocampus
The hippocampus has been divided into two broad sub-divisions,
an anterior (ventral) one and a posterior one (Fanselow and
Dong, 2010 for a review). It has been hypothesized that the poste-
rior division is more engaged by cognitive tasks while the anterior
one is more so during emotional experiences. Although a strong
cognitive element has also been imputed to experience of the
sublime, particularly as regards mathematical sublimity and the
role of the imagination (Kant, 1790/1986), characteristics which
may properly be called “cognitive,” the great majority of those
who have written on the topic of sublimity have also invoked as
strong, if not stronger, emotional elements, summarized in terms
such as “awe,” “fear,” and “horror.” By this measure, one would
have expected some activity in both hypothetical subdivisions
of the hippocampus. That the activity was restricted to poste-
rior hippocampus, where activity also correlates with romantic
experiences (Bartels and Zeki, 2004; Zeki and Romaya, 2010),
leads us to suspect that the proposed subdivisions of the hip-
pocampus along cognitive—emotional lines is inadequate or does
not take into account experiences that involve both emotional
and cognitive components. At any rate, the activity reported here
and elsewhere about positive emotions (Bartels and Zeki, 2004;
Zeki and Romaya, 2010) and negative ones (Lang et al., 2009;
Pohlack et al., 2012; Shafer and Dolcos, 2012; Poppenk et al.,
2013 for a review) does not sit easily within such a subdivision.
Interesting to note in this context is a recent report of a difference
in the response of anterior and posterior hippocampus to anxiety
Frontiers in Human Neuroscience www.frontiersin.org November 2014 | Volume 8 | Article 891 |7
Ishizu and Zeki Experience of the sublime and the beautiful
related to receiving a shock and anxiety related to interpreting the
environment as posing a threat (Satpute et al., 2012), which could
as well include the threat perceived at a safe distance; the former
appears to correlate with activity in anterior hippocampus while
the latter with activity in posterior hippocampus, although both
can be qualified as emotional experiences.
Fusiform gyrus/inferior temporal cortex/ lateral occipital complex
The activity observed in our study extended posteriorly to include
visual areas in the inferior temporal cortex and fusiform gyrus,
encroaching onto the lateral occipital cortex (LOC), areas that
would be expected to be activated by viewing natural scenes.
This is consistent with previous results which have shown that
the fusiform gyrus and LOC are active when subjects view emo-
tional scenes (Bradley et al., 2003; Sabatinelli et al., 2011). What
our results show in addition is that activity in both is paramet-
rically modulated with the declared intensity of experience of
the sublime. This has echoes in a previous study which showed
that activity in V5, a visual sensory area, is parametrically related
to the declared preference for kinetic stimuli (Zeki and Stutters,
2012). Collectively these results thus indicate that activity that is
parametrically modulated with subjective, including emotional,
experiences is not restricted to “higher” cortical areas but may
involve as well visual sensory areas, possibly by feedback from
other centers. We also note that we did not observe such paramet-
rically modulated activity in the primary visual cortex (V1) and
the adjacent visual areas V2/V3. This suggests that the sublimity
modulation in fusiform gyrus and LOC cannot be accounted for
by a visual attentional effect.
Inferior/middle frontal gyrus
The inferior frontal gyrus activity in this study extended to the
middle frontal gyrus, which is not surprising given that previ-
ous studies of emotional states have led to activity in both gyri,
but the exact role that each gyrus plays remains uncertain. A
variety of studies have shown that the inferior frontal gyrus is
activated by emotional stimuli (Yamasaki et al., 2002), including
emotional imagery and emotional scenes (Sabatinelli et al., 2006,
2011). Interestingly, it has also been found to be active when sub-
jects imagine future events (Viard et al., 2011), hence emphasizing
the importance of the imagination in neural terms, just as it has
been emphasized in hypothetical terms in past discussions of the
sublime.
Basal ganglia
The role traditionally ascribed to the basal ganglia, of an impor-
tant motor center, is undergoing a profound change, to include
activity related to emotions as well (see Arsalidou et al., 2013 for
a meta-analysis). Previous studies have shown the body of the
caudate nucleus to be involved in the experience of beauty while
our present one shows that there was parametrically related activ-
ity in the head of the right caudate, which is reportedly involved
in both emotional and cognitive functions, though more promi-
nently in the latter (Arsalidou et al., 2013). We also observed
activity in the right putamen, which also has cognitive and emo-
tional functions of an indeterminate nature, in addition to being
involved in emotional motor planning (Monchi et al., 2006;
Boecker et al., 2008; Zeki and Romaya, 2008; Ishizu and Zeki,
2013).
Cerebellum
As with the basal ganglia, there has been increasing emphasis on
the importance of the cerebellum in both emotional and cogni-
tive experiences (Baumann and Mattingley, 2012). An especially
interesting example in the present context is the activity in it that
correlates with the experience of mathematical beauty (Zeki et al.,
2014), an experience that has both emotional and cognitive com-
ponents and that has been given a special status within the context
of the sublime, by both Kant and Schopenhauer. The active area
in our study was located in Crus II, and was peak level significant
for both hemispheres while it was only cluster level significant in
the left hemisphere. Crus II is the cerebellar locus which previ-
ous studies have found to be activated with fear (Baumann and
Mattingley, 2012).
COMBINED EMOTIONAL AND COGNITIVE FUNCTIONS WITHIN
INDIVIDUAL AREAS
The areas in our study whose activity was parametrically modu-
lated with the intensity of sublime experiences, as well as evidence
from previous studies, raises interesting questions as to the extent
to which, even areas that have been traditionally regarded as being
primarily sensory in function, combine the experiential, sensory
and cognitive element with the emotional one.
Taken together with previous results, the results given here
lead us to conclude that (i) there is no easy separation between
cognitive and emotional components insofar as the functions of
these areas are concerned, since all the areas enumerated above
have been found in past studies to have been active during tasks
belonging to both categories (see also Cromheeke and Mueller,
2014). This is interesting to emphasize in the context of this study
because, as our Introduction points out, a review of the history
of discussion on the sublime reveals, likewise, that both cognitive
and emotional elements of the experience have been emphasized
in the past.
The results also lead us to conclude that (ii) the activity in
all the above areas, even ones considered to have mainly sensory
functions, such as the fusiform gyrus, infero-temporal cortex and
LOC, can be modulated by experiences such as that of the sub-
lime, which have a strong emotional component in addition to
the cognitive. Whether an emotional modulation of such sensory
areas is “top-down” and dependent upon input from “higher”
areas or whether it is “bottom-up,” or whether both, is an unre-
solved question. The parametric modulation of sensory areas with
experiences that have an emotional component, as in this study, is
interesting to compare with the parametric modulation of activ-
ity in an area such as V5 with kinetic stimuli that are preferred
but have no strong emotional component (Zeki and Stutters,
2013). This suggests that “bottom-up” processes which are not
strictly sensory may also play an important, if not exclusive, role
in modulating activity within sensory areas.
DEACTIVATIONS
The general comments we make about cortical activations apply
as well to the de-activations that we have observed. Of these, the
following deserve special comment:
Frontiers in Human Neuroscience www.frontiersin.org November 2014 | Volume 8 | Article 891 |8
Ishizu and Zeki Experience of the sublime and the beautiful
Superior frontal gyrus
The most prominently deactivated area, unique to the highest lev-
els of the sublime experience, was the superior frontal gyrus, a
zone that was previously found to be de-activated during sensori-
motor processing, and interpreted to signify a suppression of
self-awareness during such processing (Goldberg et al., 2006).
Suppression of self awareness would not be expected during expe-
rience of the sublime, which has been written of as leading to an
awareness of one’s insignificance in relation to the immensity and
grandeur of the Nature. This would imply that one is aware of
one’s existence and insignificance during such experiences.
Posterior cingulate cortex/precuneus
Another prominent deactivation, produced by experience of the
highest sublimity alone, was found in the PCC/precuneus, which
discerns emotional and self-related information (Buckner et al.,
2008 for a review). Together with mPFC, which allows for self-
reflection and the regulation of emotions (Raichle et al., 2001;
Buckner et al., 2008 for a review), and which was deactivated with
sublimity in this study, PCC/precuneus have been regarded as
key structures of resting-state functional connectivity (or default
state network), which has been thought to reflect introspection
and self-referential thought (Raichle et al., 2001). Deactivations
within those self-referential regions, again, may suggest a linkage
between the feeling of awareness of one’s insignificance and the
experience of sublimity.
Cerebellum
The bilateral de-activation observed in Crus I of the cerebellum
highlights again the strong cerebellar involvement in emotional
and cognitive processing. This particular part of the cerebellum
has been previously reported to be activated during the experi-
ence of fear (Baumann and Mattingley, 2012), emphasizing well
our point above. The term sublime includes the component of
fear, but with a very different nuance and emphasis. Hence it
may not be surprising to find that areas mediating what is more
traditionally understood by fear are suppressed during the expe-
rience of fear associated with the sublime, which is an altogether
different kind of experience.
Here it is interesting to point out that the deactivation in
right cerebellum was significant at both peak and cluster levels
while the activation in Crus I (see above) was only significant
at peak level. In spite of this difference in statistical significance
between activation and de-activation, the proximity and symmet-
rical distribution of active cerebellar regions, compared to ones
that were de-activated, may be of potential interest for future
studies exploring similar affective states as this one.
Anterior cingulate/medial prefrontal cortex
The above point is made emphatic as well with the observation of
a de-activation in the anterior cingulate/medial prefrontal cortex.
The latter has been posited to be important during the experience
of negative emotions. It is not at all surprising that the experience
of the sublime, which has generally been written of as a positive
experience, should lead to de-activation in regions which previ-
ous studies have implicated in negative experiences (Etkin et al.,
2011; Doty et al., 2014).
CONCLUSION
We undertook this work to learn whether there is any difference
in the neural mechanisms that correlate with two complex experi-
ences that are nevertheless easily distinguishable at the extremes,
even if what is beautiful can sometimes also be regarded as sub-
lime and vice versa. We were surprised to find that the neural
activity that correlates with experience of the beautiful is very dif-
ferent from that which correlates with experience of the sublime.
None of the areas active in studies of visual beauty (Kawabata
and Zeki, 2004; Vartanian and Goel, 2004,inter alia;reviewed
in Ishizu and Zeki, 2011), and not even beauty derived from a
highly cognitive source such as mathematics (Zeki et al., 2014)
were active in this study, and vice versa.
Burke terminated his book which, among other works,
inspired our experiments, thus: “on a review of all that has been
said of the effects, as well as the causes of both; it will appear,
that the sublime and beautiful are built on principles very dif-
ferent, and that their affections are as different: the great has
terror as its basis... the beautiful is founded on mere positive
pleasure” (Burke, 1757, 4: XXV). Our experiments, while leaving
many details unsettled and many questions unanswered, nev-
ertheless show that the profound distinction between the two
experiences emphasized in the past is reflected neurobiologically
in the engagement of radically different mechanisms during the
two experiences.
ACKNOWLEDGMENT
This work was supported by the Wellcome Trust, London.
REFERENCES
Addison, J. (1712). The Miscellaneous Works of Joseph Addison,Vol.4.Oxford:
Talb o y s .
Arsalidou, M., Duerden, E. G., and Taylor, M. J. (2013). The centre of the
brain: topographical model of motor, cognitive, affective, and somatosen-
sory functions of the basal ganglia. Hum. Brain Mapp. 34, 3031–3054. doi:
10.1002/hbm.22124
Aube, W., Angulo-Perkins, A., Peretz, I., Concha, L., and Armony, J. L. (2014). Fear
across the senses: brain responses to music, vocalizations and facial expressions.
Soc. Cogn. Affect. Neurosci. doi: 10.1093/scan/nsu067. [Epub ahead of print].
Bartels, A., and Zeki, S. (2004). The neural correlates of maternal and
romantic love. Neuroimage 21, 1155–1166. doi: 10.1016/j.neuroimage.2003.
11.003
Baumann, O., and Mattingley, J. B. (2012). Functional topography of primary
emotion processing in the human cerebellum. Neuroimage 61, 805–811. doi:
10.1016/j.neuroimage.2012.03.044
Boecker, H., Jankowski, J., Ditter, P., and Scheef, L. (2008). A role of the basal
ganglia and midbrain nuclei for initiation of motor sequences. Neuro image 39,
1356–1369. doi: 10.1016/j.neuroimage.2007.09.069
Bradley, M. M., Sabatinelli, D., Lang, P. J., Fitzsimmons, J. R., King, W., and Desai,
P. (2003). Activation of the visual cortex in motivated attention. Behav.Neurosci.
117, 369–380. doi: 10.1037/0735-7044.117.2.369
Buckner, R. L., Andrews-Hanna, J. R., and Schacter,D. L. (2008). The brain’s default
network: anatomy, function, and relevance to disease. Ann. N.Y. Acad. Sci. 1124,
1–38. doi: 10.1196/annals.1440.011
Burke, E. (1757). A Philosophical Enquiry into the Origin of our Ideas of the Sublime
and Beautiful. London: R. and J. Dodsley.
Cheon, B. K., Im, D. M., Harada, T., Kim, J. S., Mathur, V. A., Scimeca, J. M.,
et al. (2013). Cultural modulation of the neural correlates of emotional pain
perception: the role of other-focusedness. Neuropsycholog ia 51, 1177–1186. doi:
10.1016/j.neuropsychologia.2013.03.018
Cromheeke, S., and Mueller, S. C. (2014). Probing emotional influences on cog-
nitive control: an ALE meta-analysis of cognition emotion interactions. Brain
Struct. Funct. 219, 995–1008. doi: 10.1007/s00429-013-0549-z
Frontiers in Human Neuroscience www.frontiersin.org November 2014 | Volume 8 | Article 891 |9
Ishizu and Zeki Experience of the sublime and the beautiful
Dennis, J. (1693). “From the critical works of John Dennis,” in The Sublime: a
Reader in British Eighteenth-Century Aesthetic Theory, ed E. N. Hooker (1996)
(Quoted by A. Ashfield and P. de Bolla) (Cambridge: Cambridge University
Press), 59.
Doty, T. J., Japee, S., Ingvar, M., and Ungerleider, L. G. (2014). Intersubject variabil-
ity in fearful face processing: the link between behavior and neural activation.
Cogn. Affect. Behav. Neurosci. doi: 10.3758/s13415-014-0290-y. [Epub ahead of
print].
Earl of Shaftesbury (Cooper, Anthony Ashley, 3rd Earl of ). (1709). Characteristics of
Men, Manners, Opinions, Times, ed L. E. Klein (1999) (Cambridge: Cambridge
University Press), 316.
Ellingsen, D. M., Wessberg, J., Eikemo, M., Liljencrantz, J., Endestad, T., Olausson,
H., et al. (2013). Placebo improves pleasure and pain through opposite modula-
tion of sensory processing. Proc. Natl. Acad. Sci. U.S.A. 110, 17993–17998. doi:
10.1073/pnas.1305050110
Etkin, A., Egner, T., and Kalisch, R. (2011). Emotional processing in anterior
cingulate and medial prefrontal cortex. Trend s Cog n . Sc i . 15, 85–93. doi:
10.1016/j.tics.2010.11.004
Fanselow, M. S., and Dong, H. W. (2010). Are the dorsal and ven-
tral hippocampus functionally distinct structures? Neuron 65, 7–19. doi:
10.1016/j.neuron.2009.11.031
Favilla, S., Huber, A., Pagnoni, G., Lui, F., Facchin, P., Cocchi, M., et al. (2014).
Ranking brain areas encoding the perceived level of pain from fMRI data.
Neuro image 90, 153–162. doi: 10.1016/j.neuroimage.2014.01.001
Goldberg, I. I., Harel, M., and Malach, R. (2006). When the brain loses its self:
prefrontal inactivation during sensorimotor processing. Neuron 50, 329–339.
doi: 10.1016/j.neuron.2006.03.015
Havel, H. L. (2006). Longinus,On the Sublime.(Transl.byH.L.Havel
with commentaries by A. Lang). Available online at: http://www.gutenberg.
org/files/17957/17957-h/17957-h.htm
Hutton, C., Bork, A., Josephs, O., Deichmann, R., Ashburner, J., and Turner,
R. (2002). Image distortion correction in fMRI: a quantitative evaluation.
Neuro image 16, 217–240. doi: 10.1006/nimg.2001.1054
Ishizu, T., and Zeki, S. (2011). Toward a brain-based theory of beauty. PLoS ONE
6:e21852. doi: 10.1371/journal.pone.0021852
Ishizu, T., and Zeki, S. (2013). The brain’s specialized systems for aesthetic and
perceptual judgment. Eur. J. Neurosci. 37, 1413–1420. doi: 10.1111/ejn.12135
Kant, I. (1790/1986). Kritik der Urteilskraft, translated as Critique of Judgment,
Pluhar (1986). Indianapolis, IN: Hackett Publishing Co.
Kawabata, H., and Zeki, S. (2004). Neural correlates of beauty. J. Neurophysiol. 91,
1699–1705. doi: 10.1152/jn.00696.2003
Lang, S., Kroll, A., Lipinski, S. J., Wessa, M., Ridder, S., Christmann, C., et al. (2009).
Context conditioning and extinction in humans: differential contribution of the
hippocampus, amygdala and prefrontal cortex. Eur. J. Neurosci. 29, 823–832.
doi: 10.1111/j.1460-9568.2009.06624.x
Mattavelli, G., Sormaz, M., Flack, T., Asghar, A. U., Fan, S., Frey, J., et al. (2013).
Neural responses to facial expressions support the role of the amygdala in
processing threat. Soc. Cogn. Affect. Neurosci. doi: 10.1093/scan/nst162. [Epub
ahead of print].
Monchi, O., Petrides, M., Strafella, A. P., Worsley, K. J., and Doyon, J. (2006).
Functional role of the basal ganglia in the planning and execution of actions.
Ann. Neurol. 59, 257–264. doi: 10.1002/ana.20742
Pohlack, S. T., Nees, F., Liebscher, C., Cacciaglia, R., Diener, S. J., Ridder, S., et al.
(2012). Hippocampal but not amygdalar volume affects contextual fear condi-
tioning in humans. Hum. Brain Mapp. 33, 478–488. doi: 10.1002/hbm.21224
Poppenk, J., Evensmoen, H. R., Moscovitch, M., and Nadel, L. (2013). Long-axis
specialization of the human hippocampus. Tre n ds Cog n . Sc i . 17, 230–240. doi:
10.1016/j.tics.2013.03.005
Raichle, M. E., MacLeod, A. M., Snyder, A. Z., Powers, W. J., Gusnard, D. A., and
Shulman, G. L. (2001). A default mode of brain function. Proc. Natl. Acad. Sci.
U.S.A. 98, 676–682. doi: 10.1073/pnas.98.2.676
Sabatinelli, D., Fortune, E. E., Li, Q., Siddiqui, A., Krafft, C., Oliver, W.
T., et al. (2011). Emotional perception: meta-analyses of face and natural
scene processing. Neuroimage 54, 2524–2533. doi: 10.1016/j.neuroimage.2010.
10.011
Sabatinelli, D., Lang, P. J., Bradley, M. M., and Flaisch, T. (2006). The neural basis
of narrative imagery: emotion and action. Prog. Brain Res. 156, 93–103. doi:
10.1016/S0079-6123(06)56005-4
Satpute, A. B., Mumford, J. A., Naliboff, B. D., and Poldrack, R. A. (2012). Human
anterior and posterior hippocampus respond distinctly to state and trait anxiety.
Emotion 12, 58–68. doi: 10.1037/a0026517
Schopenhauer, A. (1844). Die Welt als Wille und Ausstellung, translated as The World
as Will and Representation, Vol. I. Transl. E. F. J. Payne (1969). New York, NY:
Dover Publications.
Shafer, A. T., and Dolcos, F. (2012). Neural correlates of opposing effects of
emotional distraction on perception and episodic memory: an event-related
FMRI investigation. Front. Integr. Neurosci. 6:70. doi: 10.3389/fnint.2012.
00070
Vartanian, O., and Goel, V. (2004). Neuroanatomical correlates of aesthetic
preference for paintings. Neuroreport 15, 893–897. doi: 10.1097/00001756-
200404090-00032
Viard, A., Chetelat, G., Lebreton, K., Desgranges, B., Landeau, B., de La Sayette,
V., et al. (2011). Mental time travel into the past and the future in healthy
aged adults: an fMRI study. Brain Cogn. 75, 1–9. doi: 10.1016/j.bandc.2010.
10.009
Weiskopf, N., Hutton, C., Josephs, O., and Deichmann, R. (2006). Optimal EPI
parameters for reduction of susceptibility-induced BOLD sensitivity losses:
a whole-brain analysis at 3 T and 1.5 T. Neuroim age 33, 493–504. doi:
10.1016/j.neuroimage.2006.07.029
Yamasaki, H., LaBar, K. S., and McCarthy, G. (2002). Dissociable prefrontal
brain systems for attention and emotion. Proc. Natl. Acad. Sci. U.S.A. 99,
11447–11451. doi: 10.1073/pnas.182176499
Zeki, S., and Romaya, J. P. (2008). Neural correlates of hate. PLoS ONE 3:e3556.
doi: 10.1371/journal.pone.0003556
Zeki, S., and Romaya, J. P. (2010). The brain reaction to viewing faces of opposite-
and same-sex romantic partners. PLoS ONE 5:e15802. doi: 10.1371/jour-
nal.pone.0015802
Zeki, S., Romaya, J. P., Benincasa, D. M., and Atiyah, M. F. (2014). The experience
of mathematical beauty and its neural correlates. Front. Hum. Neurosci. 8:68.
doi: 10.3389/fnhum.2014.00068
Zeki, S., and Stutters, J. (2012). A brain-derived metric for preferred kinetic stimuli.
Open Biol. 2:120001. doi: 10.1098/rsob.120001
Zeki, S., and Stutters, J. (2013). Functional specialization and generalization for
grouping of stimuli based on colour and motion. Neuroimage 73, 156–166. doi:
10.1016/j.neuroimage.2007.09.069
Conflict of Interest Statement: The authors declare that the research was con-
ducted in the absence of any commercial or financial relationships that could be
construed as a potential conflict of interest.
Received: 04 August 2014; accepted: 16 October 2014; published online: 11 November
2014.
Citation: Ishizu T and Zeki S (2014) A neurobiological enquiry into the origins of our
experience of the sublime and beautiful. Front. Hum. Neurosci. 8:891. doi: 10.3389/
fnhum.2014.00891
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... Yue et al. (2007) reported greater activity for preferred vs. non-preferred scenes (a mixture of indoor and outdoor) in right, but not left PPA. A study of 'sublime' natural landscapes found increased activity in an extensive portion of the ventral occipitotemporal cortex (VOT) stretching from fusiform gyrus to PHG and underlying posterior hippocampus (Ishizu and Zeki, 2014); yet as no scene-selective localizer was performed, the location of activation relative to PPA was unclear. Another study reported that attractiveness ratings of natural landscapes were correlated with subthreshold activity changes in PHG and CoS, but that only activity in the object-selective lateral occipital complex (LO), and not place-selective PPA, was significantly correlated with place attractiveness (Pegors et al., 2015). ...
... Studies investigating reward prediction at different time scales have found that a number of areas in the limbic loop, including the ventral striatum, are involved in the prediction of immediate rewards; dorsal striatum, a part of the motor loop, was found to be involved in future reward prediction (Tanaka et al., 2004). The activation of dorsal striatum in response to aesthetically appealing landscape movies (this study) and images (Yue et al., 2007;Ishizu and Zeki, 2014) might relate to the fact that many of the pleasing features of landscapes relate to potential reward such as the potential for habitat, for exploration, for resource availability, or for monitoring one's surroundings -environmental conditions favorable to survival (Rostrup, 2014). ...
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During aesthetically appealing visual experiences, visual content provides a basis for computation of affectively tinged representations of aesthetic value. How this happens in the brain is largely unexplored. Using engaging video clips of natural landscapes, we tested whether cortical regions that respond to perceptual aspects of an environment (e.g., spatial layout, object content and motion) were directly modulated by rated aesthetic appeal. Twenty-four participants watched a series of videos of natural landscapes while being scanned using functional magnetic resonance imaging (fMRI) and reported both continuous ratings of enjoyment (during the videos) and overall aesthetic judgments (after each video). Although landscape videos engaged a greater expanse of high-level visual cortex compared to that observed for images of landscapes, independently localized category-selective visual regions (e.g., scene-selective parahippocampal place area and motion-selective hMT+) were not significantly modulated by aesthetic appeal. Rather, a whole-brain analysis revealed modulations by aesthetic appeal in ventral (collateral sulcus) and lateral (middle occipital sulcus, posterior middle temporal gyrus) clusters that were adjacent to scene and motion selective regions. These findings suggest that aesthetic appeal per se is not represented in well-characterized feature- and category-selective regions of visual cortex. Rather, we propose that the observed activations reflect a local transformation from a feature-based visual representation to a representation of “elemental affect,” computed through information-processing mechanisms that detect deviations from an observer’s expectations. Furthermore, we found modulation by aesthetic appeal in subcortical reward structures but not in regions of the default-mode network (DMN) nor orbitofrontal cortex, and only weak evidence for associated changes in functional connectivity. In contrast to other visual aesthetic domains, aesthetically appealing interactions with natural landscapes may rely more heavily on comparisons between ongoing stimulation and well-formed representations of the natural world, and less on top-down processes for resolving ambiguities or assessing self-relevance.
... Sacred spaces have the potential of creating lasting and meaningful experiences for human beings. Recent studies in neuroaesthetics and neurotheology reveal the important role of human-environment interactions and spirituality on the cognitive, emotional, and behavioral aspects of human health and well-being (Bermudez et al. 2017;Chatterjee and Vartanian 2014;Coburn et al. 2017Coburn et al. , 2020Ishizu and Zeki 2014;Miller et al. 2019;Wang et al. 2011). Throughout the history of architecture, or at least the histories written by architectural historians, certain notable sacred buildings are repeatedly discussed due to the important role they have played in society or to the discipline of architecture. ...
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This paper seeks to create a comparative framework for evaluating transformative experiences for different types of ritual contexts found in sacred architecture by bridging the gap between the phenomenology of human experience and architecture’s built conditions. The methodology creates a framework for statistical analysis, whereby evidence of people’s actual (i.e., real, lived) “subjective” experiences can be evaluated against the “objective” architectural conditions. The comparative framework is put to the test by comparing the experiential and environmental conditions found at the Pantheon in Rome. Experiential data for the Pantheon is extracted from Julio Bermudez’s large survey database (N = 2872) of “extraordinary architectural experiences” for this study. This data is compared against “objective” graphical architecture analysis using Lindsay Jones’ “morphology of ritual-architectural priorities” with a specific focus on ritual contexts. The quantitative and qualitative data reveals that the Pantheon produces transformative experiences for visitors that are related to the expected outcomes of specific design features. The percentages from the “objective” and “subjective” analysis both rank the priorities of theatre, contemplation, and sanctuary in the same order. This study concludes that built environments possessing a higher presence and quality of “ritual-architectural priorities” are more likely to be perceived as sacred and produce transformative experiences.
... Aesthetic judgment shares its neural correlates in the reward system with moral decision-making, thus pointing in the direction of a common ground for aesthetic and moral judgments [186,187]. Activity in the medial orbito-frontal cortex occurs regardless of whether the source of the experience was visual, musical or mathematical [188][189][190]. These findings were a major starting point for later neuroimaging studies that revealed activity in the reward circuit as a whole as being a key component of the aesthetic experience. ...
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This paper argues for a biological conception of music listening as an evolutionary achievement that is related to a long history of cognitive and affective-emotional functions, which are grounded in basic homeostatic regulation. Starting from the three levels of description, the acoustic description of sounds, the neurological level of processing, and the psychological correlates of neural stimulation, it conceives of listeners as open systems that are in continuous interaction with the sonic world. By monitoring and altering their current state, they can try to stay within the limits of operating set points in the pursuit of a controlled state of dynamic equilibrium, which is fueled by interoceptive and exteroceptive sources of information. Listening, in this homeostatic view, can be adaptive and goal-directed with the aim of maintaining the internal physiology and directing behavior towards conditions that make it possible to thrive by seeking out stimuli that are valued as beneficial and worthy, or by attempting to avoid those that are annoying and harmful. This calls forth the mechanisms of pleasure and reward, the distinction between pleasure and enjoyment, the twin notions of valence and arousal, the affect-related consequences of music listening, the role of affective regulation and visceral reactions to the sounds, and the distinction between adaptive and maladaptive listening.
... We speculate that this response may reflect the different attentional demands that the control task required compared with the aesthetic task (Simmons et al., 2011). Furthermore, our results did not show sensitivity to aesthetic judgements in mOFC, even though previous research has linked mOFC engagement to processing artistic beauty (Ishizu et al., 2014;Kawabata & Zeki, 2004;Zhang et al., 2017). We speculate this lack of response in mOFC might be due to the homogeneity of the stimuli used, which were all portraits of a particular kind, rather than a more varied stimulus set. ...
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Although there is growing interest in the neural foundations of aesthetic experience, it remains unclear how particular mental sub‐systems (e.g., perceptual, affective, cognitive) are involved in different types of aesthetic judgments. Here we use fMRI to investigate the involvement of different neural networks during aesthetic judgments of visual artworks with implied motion cues. First, a behavioural experiment (N=45) confirmed a preference for paintings with implied motion over static cues. Subsequently, in a pre‐registered fMRI experiment (N=27), participants made aesthetic and motion judgments towards paintings representing human bodies in dynamic and static postures. Using functional region‐of‐interest and Bayesian multilevel modelling approaches, we provide no compelling evidence for unique sensitivity within or between neural systems associated with body perception, motion and affective processing during the aesthetic evaluation of paintings with implied motion. However, we show suggestive evidence that motion and body‐selective systems may integrate signals via functional connections with a separate neural network in dorsal parietal cortex, which may act as a relay or integration site. Our findings clarify the roles of basic visual and affective brain circuitry in evaluating a central aesthetic feature – implied motion – whilst also pointing towards promising future research directions, which involve modelling aesthetic preferences as hierarchical interplay between visual and affective circuits and integration processes in frontoparietal cortex.
... The experience of the sublime involves different neural mechanisms than that of beauty. It activates the inferior temporal cortex, the frontal gyrus and the posterior hippocampus, as well as the basal ganglia and most importantly, the cerebellum, which is associated with spatial cognition and the experience of extended space (Ishizu and Zeki, 2014). In contrast, the experience of beauty involves the medial orbito-frontal cortex (mOFC) and the anterior cingulate cortex (ACC) (Yeh et al., 2015). ...
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This paper contributes to a deepening of the knowledge about how architectural experience can be described in neuro-phenomenological terms, through the development of a cognitive-phenomenological approach to examining architectural experience through text-based analysis. It aims to develop an assessment tool to produce knowledge about one’s personal experience and perception of the built environment by exploring the impact of its spatial properties on an individual, taking as a case study Le Corbusier’s experience of the Kasbah of Algiers. The results demonstrate that this city has the power to stir emotional engagement that arises from: a high cognitive-affective reaction towards the dynamic interactions between the curved contours of its streets; the harmony of its colours; the magnitude and vastness generated by its panoramic views towards the sea; its proportions in relation to the dimensions of the human body in different postures; the contrasts of the height, light, dimensions and ambiances; and the spatial navigation that favours the act of walking to discover the Kasbah and unveil its mysteries. These properties exist as complex networks of interconnected physical and atmospheric elements, and they involve integrated perception under the influence of previous knowledge, beliefs and aspirations to shape Le Corbusier’s architectural experience of the Kasbah.
... In this field, seminal functional studies investigated the neural correlates of aesthetic experience, trying to localize cerebral regions sensible to beauty. The faculty of beauty seems to recruit the medial orbitofrontal (Ishizu and Zeki, 2011;Ishizu, 2014;Zeki et al., 2014) and the dorsolateral prefrontal cortices (Cela-Conde et al., 2004;Cattaneo et al., 2014). This brain-based approach to the study of aesthetics suggests that all works of art that appear beautiful to a subject affect the activity of specific brain regions (Ishizu and Zeki, 2011). ...
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Empathy for pain involves sensory and visceromotor brain regions relevant also in the first-person pain experience. Focusing on brain activations associated to vicarious experiences of pain triggered by artistic or non-artistic images, the present study aims to investigate common and distinct brain activation patterns associated to these two vicarious experiences of pain and to assess whether empathy for pain brain regions contribute to the formation of an aesthetic judgment in non-art expert observers. Artistic and non-artistic facial expressions (painful and neutral) were shown to participants inside the scanner and then aesthetically rated in a subsequent behavioural session. Results showed that empathy for pain brain regions (i.e., bilateral insular cortex, posterior sector of the anterior cingulate cortex and the anterior portion of the middle cingulate cortex) and bilateral inferior frontal gyrus are commonly activated by artistic and non-artistic painful facial expressions. For the artistic representation of pain, the activity recorded in these regions directly correlated with participants' aesthetic judgment. Results also showed the distinct activation of a large cluster located in the PCC/precuneus for non-artistic stimuli. This study suggests that non-beauty specific mechanisms such as empathy for pain are crucial components of the aesthetic experience of artworks.
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L'attivazione corporea ed emotiva di fronte al dolore è stata collegata al desiderio di aiutare l'altro. Basandosi su precedenti ricerche di neuroestetica, e sul concetto di Conoscenza Relazionale Estetica nel quadro della terapia della Gestalt, la ricerca ha indagato le reazioni di 29 individui di fronte a immagini di dolore e sentimenti neutri, in rappresentazioni artistiche e in foto di attori. Gli individui sono stati testati con SCL-90-R, MAIA e IRI. I risultati confermano l'ipotesi che il desiderio di aiutare è connesso con l'attivazione corporea-emozionale, con la capacità di sentire il proprio corpo e tuttavia tenere l'emozione dell'altro. L'attivazione corporeo-emotiva è stata mostrata solo nella rappresentazione artistica del dolore. Una possibile spiegazione è che il "movimento" che attiva una persona di fronte al dolore è meglio espresso nelle immagini artistiche.
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There is growing interest in the cerebellum's contributions to higher order functions of the human brain. When considering specific activities of the human cerebellum related to art, we differentiate two broad areas. Neural activity within different locations of the cerebellum is involved in art perception and in artistic creativity. The cerebellum plays an underappreciated role in neuroaesthetics, including the perception and evaluation of art objects, their appreciation and affective aesthetic experience. Certain areas of the cerebellum presumably are of particular relevance, incorporating cognitive and affective issues within large-scaled neural networks in perceiving and appraising artworks. For art creativity, many investigations report cerebellar implementations. Important areas in these domains are evolutionary younger parts of the cerebellar hemispheres, in particular the lobule VII with its Crus I and II, influencing crucial networks such as the Default Mode Network in optimizing creativity. These structures help guide pattern recognition and in art appreciation as they may play a role in predicting ongoing neural network activities through a crucial frontoparietal axis. In this chapter, we consider how our current neuroscientific understanding of cerebellar functions point to a likely role of the cerebellum in art appreciation and creativity.
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According to recent accounts, we experience the emotion of “being moved” when a situation brings into play our core values. What are the core values evoked by nonhuman landscapes, however, particularly as the distinction between man-made and natural environments becomes increasingly blurry in the so-called Anthropocene? That is the central question tackled by this article. I start by rethinking the sublime as an affect that, since Romanticism, has shaped Western attitudes toward nature. I argue that today's climate crisis calls for an expansion of our affective engagement with the nonhuman: the sublime can be part of our emotional repertoire, but only if it is complicated by feelings that point to constitutive human–nonhuman entanglement.
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This article focuses on the conceptual relationship between awe and the experience of the sublime. I argue that the experience of the sublime is best conceived as a species of awe, namely, as aesthetic awe. I support this conclusion by considering the prominent conceptual relations between awe and the experience of the sublime, showing that all of the options except the proposed one suffer from serious shortcomings. In maintaining that the experience of the sublime is best conceived as aesthetic awe, I draw from historical theories of the sublime as well as recent work in empirical psychology.
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Stimuli that signal threat show considerable variability in the extents to which they enhance behavior, even among healthy individuals. However, the neural underpinning of this behavioral variability is not well understood. By manipulating expectation of threat in an fMRI study of fearful versus neutral face categorization, we uncovered a network of areas underlying variability in threat processing in healthy adults. We explicitly altered expectations by presenting face images at three different expectation levels: 80 %, 50 %, and 20 %. Subjects were instructed to report as quickly and accurately as possible whether the face was fearful (signaled threat) or not. An uninformative cue preceded each face by 4 s. By taking the difference between reaction times (RTs) to fearful and neutral faces, we quantified an overall fear RT bias (i.e., faster to fearful than to neutral faces) for each subject. This bias correlated positively with late-trial fMRI activation (8 s after the face) during unexpected-fearful-face trials in bilateral ventromedial prefrontal cortex, the left subgenual cingulate cortex, and the right caudate nucleus, and correlated negatively with early-trial fMRI activation (4 s after the cue) during expected-neutral-face trials in bilateral dorsal striatum and the right ventral striatum. These results demonstrate that the variability in threat processing among healthy adults is reflected not only in behavior, but also in the magnitude of activation in medial prefrontal and striatal regions that appear to encode affective value.
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Intrinsic emotional expressions such as those communicated by faces and vocalizations have been shown to engage specific brain regions, such as the amygdala. Although music constitutes another powerful means to express emotions, the neural substrates involved in its processing remain poorly understood. In particular, it is unknown whether brain regions typically associated with processing "biologically-relevant" emotional expressions are also recruited by emotional music. To address this question, we conducted an event-related fMRI study in 47 healthy volunteers in which we directly compared responses to basic emotions (fear, sadness and happiness, as well as neutral) expressed through faces, nonlinguistic vocalizations and short, novel musical excerpts. Our results confirmed the importance of fear in emotional communication, as revealed by significant BOLD signal increased in a cluster within the posterior amygdala and anterior hippocampus, as well as in the posterior insula across all three domains. Moreover, subject-specific amygdala responses to fearful music and vocalizations were correlated, consistent with the proposal that the brain circuitry involved in the processing of musical emotions might be shared with the one that have evolved for vocalizations. Overall, our results show that processing of fear expressed through music, engages some of the same brain areas known to be crucial for detecting and evaluating threat-related information.
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Many have written of the experience of mathematical beauty as being comparable to that derived from the greatest art. This makes it interesting to learn whether the experience of beauty derived from such a highly intellectual and abstract source as mathematics correlates with activity in the same part of the emotional brain as that derived from more sensory, perceptually based, sources. To determine this, we used functional magnetic resonance imaging (fMRI) to image the activity in the brains of 15 mathematicians when they viewed mathematical formulae which they had individually rated as beautiful, indifferent or ugly. Results showed that the experience of mathematical beauty correlates parametrically with activity in the same part of the emotional brain, namely field A1 of the medial orbito-frontal cortex (mOFC), as the experience of beauty derived from other sources.
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Placebo analgesia is often conceptualized as a reward mechanism. However, by targeting only negative experiences, such as pain, placebo research may tell only half the story. We compared placebo improvement of painful touch (analgesia) with placebo improvement of pleasant touch (hyperhedonia) using functional MRI and a crossover design. Somatosensory processing was decreased during placebo analgesia and increased during placebo hyperhedonia. Both placebo responses were associated with similar patterns of activation increase in circuitry involved in emotion appraisal, including the pregenual anterior cingulate, medial orbitofrontal cortex, amygdala, accumbens, and midbrain structures. Importantly, placebo-induced coupling between the ventromedial prefrontal cortex and periaqueductal gray correlated with somatosensory decreases to painful touch and somatosensory increases to pleasant touch. These findings suggest that placebo analgesia and hyperhedonia are mediated by activation of shared emotion appraisal neurocircuitry, which down- or up-regulates early sensory processing, depending on whether the expectation is reduced pain or increased pleasure.
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The amygdala is known to play an important role in the response to facial expressions that convey fear. However, it remains unclear whether the amygdala’s response to fear reflects its role in the interpretation of danger and threat, or whether it is to some extent activated by all facial expressions of emotion. Previous attempts to address this issue using neuroimaging have been confounded by differences in the use of control stimuli across studies. Here, we address this issue using a block design functional magnetic resonance imaging paradigm, in which we compared the response to face images posing expressions of fear, anger, happiness, disgust and sadness with a range of control conditions. The responses in the amygdala to different facial expressions were compared with the responses to a non-face condition (buildings), to mildly happy faces and to neutral faces. Results showed that only fear and anger elicited significantly greater responses compared with the control conditions involving faces. Overall, these findings are consistent with the role of the amygdala in processing threat, rather than in the processing of all facial expressions of emotion, and demonstrate the critical importance of the choice of comparison condition to the pattern of results.
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A fundamental question in the emotional memory literature is why emotion enhances memory in some conditions but disrupts memory in other conditions. For example, separate studies have shown that emotional stimuli tend to be better remembered in long-term episodic memory (EM), whereas emotional distracters tend to impair working memory (WM) maintenance. The first goal of this study was to directly compare the neural correlates of EM enhancement (EME) and WM impairing (WMI) effects, and the second goal was to explore individual differences in these mechanisms. During event-related functional magnetic resonance imaging (fMRI), participants maintained faces in WM while being distracted by emotional or neutral pictures presented during the delay period. EM for the distracting pictures was tested after scanning and was used to identify successful encoding activity for the picture distracters. The first goal yielded two findings: (1) emotional pictures that disrupted face WM but enhanced subsequent EM were associated with increased amygdala (AMY) and hippocampal activity (ventral system) coupled with reduced dorsolateral PFC (dlPFC) activity (dorsal system); (2) trials in which emotion enhanced EM without disrupting WM were associated with increased ventrolateral PFC activity. The ventral-dorsal switch can explain EME and WMI, while the ventrolateral PFC effect suggests a coping mechanism. The second goal yielded two additional findings: (3) participants who were more susceptible to WMI showed greater amygdala increases and PFC reductions; (4) AMY activity increased and dlPFC activity decreased with measures of attentional impulsivity. Taken together, these results clarify the mechanisms linking the enhancing and impairing effects of emotion on memory, and provide insights into the role of individual differences in the impact of emotional distraction.