Cerebral Activation Associated with Sexual Arousal in Response to a Pornographic Clip

13 Pages·2001·0.51 MB·English

NeuroImage14,105–117(2001)
doi:10.1006/nimg.2001.0794,availableonlineathttp://www.idealibrary.comon
Cerebral Activation Associated with Sexual Arousal in Response to a
Pornographic Clip: A 15O–H O PET Study in Heterosexual Men
2
M. Bocher,* R. Chisin,*,1 Y. Parag,† N. Freedman,* Y. Meir Weil,‡ H. Lester,* E. Mishani,* and O. Bonne‡
*DepartmentofMedicalBiophysicsandNuclearMedicine/HBRC,HadassahHebrewUniversityHospital,Jerusalem91120Israel;
†TheHebrewUniversity-HadassahSchoolofMedicine,Jerusalem,Israel;and‡DepartmentofPsychiatry,
HadassahHebrewUniversityHospital,Jerusalem,Israel
ReceivedOctober16,2000
intricatelyrelatedtothecoreofbeing.Tragicexamples
This study attempted to use PET and 15O–H O to ofthisbody–minddichotomyareobservedinmenwho
2
measure changes in regional cerebral blood flow have suffered injury to the spinal cord: mechanical
(rCBF)duringsexualarousalevokedin10younghet-
rubbing of the penis can induce erection and ejacula-
erosexual males while they watched a pornographic
tionevenwithoutthepatientbeingawareoftheoccur-
video clip, featuring heterosexual intercourse. This
rence. On the other hand, such patients may experi-
condition was compared with other mental setups
ence “phantom orgasms,” i.e., mental orgasmic
evoked by noisy, nature, and talkshow audiovisual
experience without any genital occurrence (Comarr,
clips.Immediatelyaftereachclip,theparticipantsan-
1970). Using biological methodologies, a large body of
sweredthreequestionspertainingtowhatextentthey
thought about sex, felt aroused, and sensed an erec- data related to the physiology of sexual behavior has
tion. They scored their answers using a 1 to 10 scale. been accumulated, mainly, but not exclusively, in ani-
SPM was used for data analysis. Sexual arousal was mals (Beach, 1952; Everitt, 1990; Pfaus, 1999). This
mainly associated with activation of bilateral, pre- data relates to hormonal and vascular mechanisms as
dominantly right, inferoposterior extrastriate corti- well as to neural modules, primarily at the following
ces,oftherightinferolateralprefrontalcortexandof sub cortical levels: spinal, midbrain, hypothalamus,
themidbrain.Thesignificanceofthosefindingsisdis-
ventral striatum, septal nuclei, and the amygdaloid
cussed in the light of current theories concerning se-
complex. Only scarce and rather crude data exist that
lectiveattention,“mindreading”andmirroring,rein-
are relevant to the cerebral and especially to the cor-
forcementofpleasurablestimuli,andpenileerection.
tical role in human sexuality. Most are related to neu-
©2001AcademicPress
ropathological or surgical case descriptions, epilepsy
manifestations,orEEGstudies.Sofar,theattemptsto
INTRODUCTION connect subjective human sexual experience with a
simultaneous whole brain, high resolution biological
“The most important sex organ is...the brain.” recording have been limited (Tiihonen et al., 1994;
Laymen and professional therapists alike frequently Rauch et al., 1999; Stoleru et al., 1999; Redoute´ et al.,
usethispopularaphorism.Inspiteofsuchanintuitive 2000). The last two authors, who belong to the same
notion that links human sexuality to emotional and group, also used PET, and the intent of both studies
cognitive brain processes, surprisingly little biological
was comparable to ours, although the details of the
evidence exists that explicitly describes cerebral and
study design differ.
especially cortical activation during sexual arousal.
The recent availability of fMRI and PET potentially
Phenomenologically,humansexuality,likesomeother
allows for such imaging and also for correlation be-
human behaviors, appears to have a dual nature: on
tween the imaged data and the reported experience.
the one hand, a physiological-genital activity and on
The aim of our study was to take one of the first steps
the other, a fundamental psychological process that is
into this essentially under-explored field. We at-
tempted to use PET and 15O–H O to measure changes
2
1To whom correspondence and reprint requests should be ad- in regional cerebral blood flow (rCBF) during sexual
dressedattheDepartmentofMedicalBiophysicsandNuclearMed-
arousalevokedinyoungheterosexualmaleswhilethey
icine/HBRC(Director:H.Atlan),HadassahHebrewUniversityHos-
watchedapornographicvideoclip.Wepresenthereour
pital, P.O.B. 12000, Jerusalem 91120, Israel. Fax: [phone].
E-mail:[email protected]. resultsandproposeourinterpretationsofthefindings.
105 1053-8119/01$35.00
Copyright©2001byAcademicPress
Allrightsofreproductioninanyformreserved.
106 BOCHER ET AL.
METHODS The PET room was dimly lit and quiet, the partici-
pant’s head was restrained using a head holder, and
Subjects interference with his privacy was kept to a minimum
throughout the experiment. The video clips were
Thesubjectgroupconsistedoftenright-handed,het-
shown on a 14-inch TV monitor, set on a holder above
erosexual male students, aged 24–32 (average 27). All
the subject’s abdomen. Since the PET gantry limited
participantswerephysicallyhealthyanddidnotsuffer
the participants’ field of view, we provided them with
from any psychiatric illness. They did not use any
medications or mind affecting drugs. All volunteers prism eyeglasses that redirected the oncoming light
described themselves as being definitely heterosexual rays by 90°, enabling them to watch the video clips
and likely to be sexually aroused while watching a while looking straight ahead.
pornographic clip featuring heterosexual intercourse. Following a 15-min transmission scan, six 15O–H O
2
Personal information gathered during the study was emissionscanswereperformed,oneforeachcondition.
kept confidential. The ethical committees of Hadassah While the subject was engaged in watching the perti-
HospitalandtheMinistryofHealthinIsraelapproved nent clip, a 925–1110 MBq (25–30 mCi) bolus of 15O–
thestudyandparticipantssignedaninformedconsent. H Owasinjectedand20slateracquisitionwasstarted
2
for1min.Thetimeintervalbetweeninjectionswas10
Video Clips and Participants Observation Scores min.
Following the injection of 15O–H O, PET data were
2
acquired under four types of mental conditions, each Data Analysis
pertaining to a particular video clip that the partici-
pants were shown in the following order: (1) Baseline
The 1999 version of Statistical Parametric Mapping
clip (B-condition), presenting a white central cross,
(SPM)software(Fristonetal.,1995),implementedona
surrounded by randomly appearing dots with a white
Matlab platform, was used for data analysis. In order
noise auditory background. (2) Nature clip (N-condi-
toallowpixel-by-pixelintersubjectstatisticalanalysis,
tion), showing tropical fish swimming in an aquarium
with background music. (3) Talkshow clip (T-condi- allimageswererealignedwithageneric 15O–H2OPET
tion),featuringaconversationbetweentwopeople.(4) image that was stereotactically registered to the Mon-
Visual-auditory pornographic clip (S-condition), fea- treal Neurological Institute (MNI) brain atlas. Coordi-
turing heterosexual intercourse. PET acquisition was nates of interest on this atlas were transformed even-
performed once for each of the first three conditions tuallytotheTalairachatlas(TalairachandTournoux,
followed by three acquisitions during the S-condition 1988) coordinate system. Images were smoothed with
clip, which the participants watched continuously for an isotropic Gaussian kernel with a full width at half
half an hour. The same clip sequence was used for all maximumof10mmandwereresampledtoanewvoxel
subjects,sinceitwasthoughtthatthebrainactivation size of 2 3 2 3 2 mm. Each image was normalized to
associated with the S-condition might be long lasting the total activity within the brain. In order to avoid
andthereforecauseinterferenceifpresentedbeforethe analysisofregionsbelongingtowhitematter,allpixels
“sexually neutral” films. Immediately after each PET whose average counts across all subjects and all con-
acquisition,theparticipantswereaskedtoanswerthe ditionswerebelow80%ofthetotalaveragepixelcount,
following same three questions and to score their an- wereeliminatedandexcludedfromevaluation.Forall
swers in the range 1 to 10: (1) To what extent did you SPManalysis,weusedathresholdofp,0.001,equiv-
thinkaboutsexwhileyouwatchedtheclip?(2)Towhat alent to Z score .3.09, uncorrected for multiple sam-
degreedidyoufeelsexuallyaroused?(3)Didyousense pling, and a cluster size .50 pixels (400 mm3), as
any erection?
critical thresholds. Since a preliminary analysis
showednosignificantdifferencebetweentheimagesof
PET Acquisition the three S conditions, those images were treated as
one pool for all further subtractive analysis. The SPM
Images representing rCBF were acquired on a
subtractive approach was used, employing the PET
Positron Corporation HZL/R scanner, with a 16.6 cm
axial field of view (covering the whole brain), 6.2-mm “multisubjectconditionsandcovariates”model,tofind
in-plane resolution and 6.3-mm axial resolution. Ac- bothrelativeincreasesandrelativedecreasesinrCBF
quired counts were corrected for random coincidences, when the S condition was compared to the B, N, or T
measured tissue attenuation, scatter, detector sensi- conditions. Additionally, using the same SPM critical
tivity, dead-time, decay and gantry wobbling. Slices thresholds, we searched for significant regional corre-
were reconstructed by filtered back projection using a lationbetweenthechangesinrelativerCBFacrossthe
Butterworth filter (order 10, cutoff .07 mm21) with a sevenconditionsandthecorrespondingchangesinpar-
2.57-mm slice thickness. ticipants’ scoring, for each of the three questions.
CEREBRAL ACTIVITY WITH SEXUAL AROUSAL 107
TABLE 1 In general, the S condition was characterized by
bilateral widespread activation of the inferior lateral
Participants’ObservationScores
occipital and posterior temporal cortices, associated
Thinking with the extrastriate visual brain areas. This was ob-
Condition aboutsex Sexualarousal Erectionsensation servedwithminorvariationswhentheSconditionwas
compared to all three other mental conditions. The
B 2.00(1.89) 1.80(1.93) 1.00(0.00)
phenomenon was more prominent in the right hemi-
N 1.60(1.08) 1.10(0.32) 1.00(0.00)
T 2.00(1.56) 1.50(0.97) 1.10(0.32) sphere. Other activation areas were the right inferior
S 8.47(1.16) 7.53(1.67) 5.1(2.13) lateral prefrontal cortex (S 2 B), left superior post
central gyrus (S 2 B), right inferior parietal lobule
Note. Average and (standard deviation) of participants’ observa- (S2N),andleftsuperiorandinferiorparietallobules
tionscores.
(S 2 T). The correlation of rCBF and the scores of
sexualarousal(Table5andFig.3)pointedagaintothe
RESULTS extrastriate cortices and to the left postcentral gyrus
and in addition revealed significant activation in the
Table1summarizesthescoredanswersparticipants
midbrain (Figs. 3 and 4) and in the frontal pole (Brod-
gave to the three questions following each of the four
mann area 10) of the left prefrontal cortex (Fig. 3).
types of mental conditions. A paired t test analysis
RelativerCBFdecreasesduringtheSconditionwere
showed that the S condition scores were significantly
noted bilaterally in the medial prefrontal/anterior cin-
higher (p , 0.001) than the scores of any of the other
gulateareas,posteriorcingulate,andposterioraspects
three conditions B, N, and T.
of the superior prefrontal areas and in addition in the
Tables 2–4 highlight the significantly activated
right medial orbitofrontal area.
brainareasresultingfromthesubtractiveapproachof
SPM, comparing the S condition to the B, N, and T
conditions, respectively. Relative increases and de- DISCUSSION
creasesinrCBF,duringtheScondition,areportrayed
in Figs. 1 and 2, respectively. Table 5 and Fig. 3 dem- When we planned and launched the project, our ini-
onstratetheregionswithsignificantcorrelation,across tial objective was to perform groundwork, exploratory
the 10 subjects, between the changes in relative rCBF study with only a vague prior conjecture, regarding
across the six conditions and the corresponding brain areas that we expected to see activated. This
changes in participants’ scoring for questions 1 to 3. reflected our overall impression regarding the paucity
TABLE 2
ChangesinrCBFbetweenSandBConditions
Brainregion X Y Z Zscore Clustersize
SminusB
Leftoccipitotemporalgyrus 238 274 210 6.61 984
Leftinferiortemporalgyrus 247 268 0 5.53
Leftmedialoccipitalgyrus 232 280 10 3.5
Leftinferioroccipitalgyrus 224 297 25 4.75 398
Leftsuperiorpostcentralgyrus 229 237 42 4.95 234
Rightmedialoccipitalgyrus 45 274 26 7.87 2021
Rightsuperiorparietallobule 34 260 47 3.51 53
Rightinferolateralprefrontalcortex 36 21 8 4.24 77
BminusS
Leftposteriorcingulategyrus 210 250 30 4.20 300
Leftmiddlefrontalgyrus 232 16 46 4.23 59
Rightposteriorcingulategyrus 10 254 6 4.5 522
Rightcuneus 15 268 0 3.5
Rightmiddlefrontalgyrus 19 29 47 4.05 59
Rightmedialprefrontal/A.Cingulate 6 37 10 3.94 238
Leftmedialprefrontal/A.Cingulate 21 43 21 3.82
Rightmedialorbitofrontalcortex 1 12 212 3.46 84
Note.BrainclusterswithabovethresholdsignificantchangeinrelativerCBFduringthepornographicclip(S)comparedtothebaseline
condition(B).Clustersizeisgiveninpixels.Foreachcluster,theanatomicalregions,Zscore,andtheTalairachcoordinates(X,Y,Z)ofthe
pixelswiththehighestZscorearegiven.ThepositivedirectionofXistotherightofmidline,ofYisanteriortotheanteriorcommisure,and
ofZissuperiortothebicommissuralplane.Locationsprintedinitalicsrefertoadditionalmaximawithinthesameclusterthatisprinted
abovethem.ThetabledescribesbothrelativerCBFincreases(“sexminusbaseline”)aswellasdecreases(“baselineminussex”).
108 BOCHER ET AL.
TABLE 3
ChangesinrCBFbetweenSandNConditions
Brainregion X Y Z Zscore Clustersize
SminusN
Leftoccipitaltemporalgyrus 240 276 210 4.80 461
Leftoccipitaltemporalgyrus 250 266 24 4.78
Rightoccipitalgyrus 26 285 25 3.83 97
Rightmedialtemporalgyrus 47 258 2 5.86 1528
Rightmedialoccipitalgyrus 48 274 210 4.85
Rightoccipitaltemporalgyrus 45 266 214 4.82
Rightsuperiorparietallobule 34 256 41 3.58 56
NminusS
Leftmedialtemporalgyrus 248 4 220 3.96 50
Leftsuperiortemporalgyrus 245 28 23 3.77 85
Leftlateralsulcus 250 28 10 3.20
Rightposteriorcingulategyrus 12 256 7 3.95 61
Rightposteriorsuperiorfrontalgyrus 13 23 52 4.00 183
Rightsuperiortemporalgyrus 52 24 24 4.08 86
Rightmedialaspectfrontallobe 1 52 20 3.95 187
Rightanteriorsuperiorfrontalgyrus 4 56 25 3.73
Note.BrainclusterswithabovethresholdsignificantchangeinrelativerCBFduringthepornographicclip(S)comparedtothenatureclip
condition(N).SeeTable2fordetails.
ofunambiguousknowledgerelatingdirectlytothesub- PET scanner, three-dimensional acquisition, an older
ject. patient cohort and stimuli that included both still pic-
ThesimilaritiesbetweenthefindingsofStoleruetal. tures of women as well as clips of heterosexual inter-
(1999)andourresultssupporttheexistenceofdefinite course. The most significant cognitive difference is
patterns of brain activation related to sexual arousal probablythetimethatelapsedbetweenthestartofthe
elicited by a pornographic clip. A major difference be- sexual clip presentation and acquisition: 60 s in Red-
tween our study and theirs was the more than twice oute´ et al. (2000), 6 min in Stoleru et al. (1990), and
larger (16.6 vs 7.2 cm) axial field of view of our PET threeacquisitionsduring30mincontinuouswatching,
scanner,enablingustoseebrainregionshigherthan4 with scans at 10, 20, and 30 min in our study.
cm above the bicommissural line, not covered by their Weshallnowreviewthemostprominentbrainareas
scanner.Recently,anotherstudywaspublishedbythe associated with sexual arousal in our study and try to
same group (Redoute´ et al., 2000) that differed signif- elucidate their neurocognitive significance. It should
icantly both from their original work and from ours. be noted that in this study relative and not absolute
Major differences were the higher resolution of the changes in rCBF are discussed throughout. In a situ-
TABLE 4
ChangesinrCBFbetweenSandTConditions
Brainregion X Y Z Zscore Clustersize
SminusT
Leftinferioroccipitalgyrus 241 280 26 4.97 420
Leftinferiortemporalgyrus 245 266 0 3.80
Leftsuperiorparietallobule 227 256 48 4.36 232
Leftinferiorparietallobule 231 243 43 3.45
Rightmedialoccipitalgyrus 27 280 3 4.09 181
Rightinferioroccipitalgyrus 40 281 210 4.08 297
TminusS
Leftsuperiortemporalgyrus 255 223 2 5.57 2387
Leftmedialtemporalgyrus 248 4 220 5.14
Leftmedialaspectfrontallobe 21 54 27 4.26 184
Rightsuperiortemporalgyrus 52 26 23 6.06 3024
Rightmedialtemporalgyrus 59 227 2 5.73 52
Rightinferiortemporalgyrus 48 28 220 5.85
Note.BrainclusterswithabovethresholdsignificantchangeinrelativerCBFduringthepornographicclip(S)comparedtothetalkshow
condition(T).SeeTable2fordetails.
CEREBRAL ACTIVITY WITH SEXUAL AROUSAL 109
ation where there may be changes in global CBF, e.g., limitations of our preliminary study, but the relative
inresponsetosexualarousal,interpretationofchanges lack of activation in central classical limbic structures
inrelativerCBFmaynotbesimple,sinceifglobalCBF in our study may tilt the balance slightly towards the
increases, areas with less increase in rCBF may be secondinterpretation.Itisalsopossiblethattheextra-
classified as areas with decreases. striateactivationobservedresultsfrombothtop-down
andbottom-upmechanisms.Theactivationwe,aswell
Extrastriate visual cortices and left postcentral gy-
asRedoute´ (2000),foundintheposteriorpartoftheleft
rus. During the S condition, after which subjects re-
postcentral gyrus can be explained in a similar way.
ported having been sexually aroused, wide regions of
We should also consider the possibility that the
significantbrainactivationweredetectedbilaterallyin
strong signal received in the extrastriate visual cortex
the extrastriate visual cortices. The wide activation
is related to a difference in visual processing between
seen included and tended to circumscribe the human
the S condition and each of the other three conditions
visual motion area, human area V5 (Watson, 2000).
and not to sexual arousal. Perhaps a clip of human
OurfindingsreplicatethoseofStoleruetal.(1999).The
dyads engaged in non-sexual manner like dancing,
entirety of the activated regions is known to consist of
fencing or wrestling could have provided a better con-
modules associated with several aspects of visual pro-
trol for the S condition in our study. Such a view is
cessing.
supportedtosomeextentbytheconclusionsofRedoute´
Phenomenologically, arousal in response to a sexu-
et al. (2000). They reported similar activation of the
ally explicit clip implies concentration on the clip and
same area during both sexual arousal and humorous
attention to the inner emotional response experienced
conditions.
usuallyasapleasurablereinforcingoccurrence.Within
Ourresultsindicatethattherightexstrastriatecor-
thisphenomenologicalcontext,itisinterestingtocom-
texshowedstrongeractivationcomparedtotheleft,in
pare our findings to numerous neuroimaging studies
termsofbothsignalintensityandclustersize.Stoleru
that have shown that the degree of activational re-
et al. (1999) also found the same asymmetry. In an
sponse of the extrastriate system, to apparently simi-
EEGstudybyTuckerandDawson(1984),professional
lar visual inputs, may vary according to the context.
actorsrecalledexperiencesinordertocreateemotional
The level of attention is one of the best-described fac-
states of sexual arousal or depression. Greater right
tors influencing the response (Corbetta et al., 1990,
hemisphericactivationwasobservedforsexualarousal
1991; Heinze et al., 1994; Woodruff et al., 1996;
and analysis of coherence topography showed greater
O’Craven et al., 1997). Corbetta et al. (1990, 1991)
coherenceinrightcentralandposteriorregionsforthe
showedthatneuralactivityasmeasuredbyrCBFPET
sexual arousal condition. Similar EEG right hemi-
wasincreasedintheextrastriateareasasafunctionof
spheric preponderance was noted during self-stimula-
focused attention toward specific features of visual
tion orgasm provoked in healthy volunteers (Cohen et
stimuli. The areas identified in this top-down activa-
al.,1976).Ithasbeenproposed(WeintraubandMesu-
tion were in concordance with the results of earlier
lam,1987),thattherighthemisphereisequippedwith
bottom-up PET paradigms that used simple visual
neural mechanisms to attend to both visual fields,
stimuli without attentive anticipation. Recently, the
whilethelefthemisphereattendspredominantlytothe
same group reviewed evidence from a number of stud-
right visual field. Moreover, studies of split-brain pa-
ies for top-down effects on sensory cortex (Shulman et tients (Sperry, 1996; Bogen, 1969; and Gazzaniga,
al., 1997). One way to interpret such findings, as well 1970) suggest the possible coexistence of two indepen-
as ours and that of Stoleru, would be to assume that dent consciousness systems, one in each hemisphere.
perception is recruited by a hierarchically separate Inrespecttovisualprocessing,itissuggestedthatthe
cognition system, working through a dedicated atten- right hemisphere preferentially processes the global
tionmoduleactivatingvisualprocessing.Inthecontext aspectofcomplexvisualscenes,whilelocalaspectsare
of sexual arousal, this would imply the recruitment of preferentially processed by the left hemisphere (Rafal
a dedicated attentional subsystem by a supervising andRobertson,1995;Finketal.,1996).Interestingly,a
network (e.g., the limbic–paralimbic system) that as- later study by Fink et al. (1997) suggests that this
sessestherelevanceofstimuliandprovidesemotional global/locallateralityeffectcouldchangesidesdepend-
responses. An alternative way to interpret this prefer- ing on stimulus category. Kosslyn (1987) made a dis-
ential increase in rCBF in the extrastriate cortex is tinction between categorical and self-referential spa-
that the activation emerges in a bottom-up fashion, as tial coordinate representations of objects and
a result of the cooperativity of multiple, single, pre- successfully tested the hypothesis that the left and
dominantly local, visual modules. The same network right hemispheres respectively preferentially con-
might be utilized also in situations of sexual inter- tribute to each representation mode (Kosslyn et al.,
courseorinvolvingvisualmemoryandimageryofsex- 1989). It may be inferred from all of the above that
ual events. Deciding which of the two approaches is the preferential right hemispheric activation we ob-
closer to the neurobiological truth is far beyond the served reflects a relative bias of attention towards
FIG. 1. Clusters with significant, above threshold, relative increases of rCBF during the S conditions, compared to the B, N, and T
conditions(columns1,2,and3,respectively).TheupperthreerowsshowtheareasprojectedintoanMNIatlascoordinatediagram.Topto
bottom:sagittal,coronal,andtransaxialplanes.Thelowerfiverowsshowtheareasprojectedintoathreedimensionalsurfacerenderingof
thesameatlas.Toptobottom:anterior,rightlateral,posterior,leftlateral,andtopviews.
110
CEREBRAL ACTIVITY WITH SEXUAL AROUSAL 111
FIG. 2. Clusters with significant, above threshold, relative decreases of rCBF during the S conditions, compared to the B, N, and T
conditions(columns1,2,and3,respectively).FordetailsseethelegendtoFig.1.
112 BOCHER ET AL.
TABLE 5
CorrelationbetweenrCBFIncreasesandParticipants’Scoring
Brainregion X Y Z Zscore Clustersize
Thinkingaboutsex
Leftmedialoccipitalgyrus 240 276 26 5.11 887
Leftinferiortemporalgyrus 248 266 1 4.36
Leftpostcentralgyrus 254 227 21 4.08 125
Rightmedialoccipitalgyrus 47 260 25 6.03 2173
Sexualarousal
Leftinferioroccipitalgyrus 238 276 23 5.07 721
Leftinferiortemporalgyrus 248 264 0 4.24
Leftoccipitotemporalgyrus 240 264 216 3.33
Leftpostcentralgyrus 254 227 21 3.74 98
Rightmedialoccipitalgyrus 47 258 23 5.67 2071
Rightinferioroccipitalgyrus 34 283 23 4.52
Middlemidbrain 3 221 219 4.02 71
Sensationoferection
Leftmedialfrontalgyrus 231 58 15 5.17 88
Leftpostcentralgyrus 254 225 21 4.46 231
Leftmedialoccipitalgyrus 248 258 25 4.26 229
Leftinferiortemporalgyrus 224 287 0 3.74 129
Leftcuneus 227 291 5 3.66
Rightinferiortemporalgyrus 47 260 29 4.40 680
Rightoccipitotemporalgyrus 36 262 211 4.09
Midbrain 3 219 219 4.28 108
Rightinferioroccipitalgyrus 31 281 21 4.02 174
Note.BrainclusterswithabovethresholdsignificantcorrelationbetweenincreasesinrelativerCBFandparticipants’scoring.SeeTable
2fordetails.
processingglobalfeaturesinaselfreferentialspatial compatible with the possibility that the neural corre-
coordinate representation of a moving, complex, vi- late for modeling other minds is located in the frontal
sual scene. However, such a conjecture is only spec- cortex. However, Gallese and Goldman (1998) have
ulative. Specific, carefully designed paradigms are suggested that the second hypothesis may predict the
needed to test it. participationoftheinferiorfrontalcortexastheneural
Rightinferolateralprefrontalcortex. Afurtherphe- substrateofmindreading.SPECT(Baron-Cohenetal.,
nomenological analysis of the specific nature of sexual 1994)andPET(Fletcheretal.,1995)studies,basedon
arousalassociatedwithourScondition,leadustolook mind reading paradigms, have shown specific activa-
for neuro-functional correlates of two facets of cogni- tion in areas adjacent to the inferior frontal cortex. In
tionthatmaybepresentinourstudydesign:Theoryof our study, sexual arousal is happening during the S
mind and Mirroring. Our participants’ sexual arousal conditionwithoutdirecttactilestimulation,butrather
was provoked by watching movie actors engaged in throughaffiliationwiththeallegedmentalstateofthe
sexual intercourse and not through direct sexual en- clip actors. Therefore, it is interesting to note the tan-
counter with a real partner. Theory of mind or “mind dem activation of the bilateral extrastriate visual cor-
reading” is an attribute of consciousness that enables tex with the right lateral inferior frontal cortex (Table
humans(andalsoanimals,seePremackandWoodraff, 2 and Fig. 1). The significance of our finding is
1978; Premack, 1988; Brothers, 1995) to ascribe to strengthened by the fact that it is a replication of that
othersmentalstatessuchasemotions,thoughts,goals foundbyStoleruetal.(1999)andsimilarfindingswere
or beliefs. It is often used to explain the presumed alsoreportedbyRedoute´ etal.(2000).Thisobservation
deficitinautism(Frithetal.,1991;Baron-Cohenetal., isinagreementwiththesecondhypothesisoftheoryof
1993).Essentially,twonotmutuallyexclusivetheories mind and also with the prediction of lateral inferior
wereproposedtoexplainsuchphenomena.Onetheory frontal activation based on neurobiological data con-
assumes that people use implicitly known causal cerned with Mirroring. Mirroring is a neurobiological
and/or explanatory laws to infer the relationship be- conceptpredictingtheexistenceofneuralmodulesthat
tween observed stimuli, mental states and behavior are based on a direct link between perception and
(Astington et al., 1988). The other asserts that people action and provides a common substrate for mapping
attribute mental states to others by using their own betweenobservedmovementandmovementexecution.
mental mechanism to simulate another’s mental state Such a system may support abilities such as theory of
(Carruthers and Smith, 1996). Both hypotheses are mind (Gallese and Goldman, 1998) and imitation
CEREBRAL ACTIVITY WITH SEXUAL AROUSAL 113
(MeltzoffandMoore,1997),bothessentialforlearning showspreponderancetowardrighthemisphericactiva-
and social interactions (Piaget, 1962). “Mirror neu- tion.
rons,” found in the inferolateral frontal cortex of the Midbrain. Correlation analysis, across the 10 sub-
monkey, fire similarly, both when the monkey grasps jects, between the changes in relative rCBF across
anobjectandwhenitseesthesameactionexecutedby conditions and the corresponding changes in partici-
another. Those neurons are not activated when the pants’ scoring, revealed additional activation in the
monkey simply sees the object without an action per- midbrain particularly in respect to erection sensation
formed (Gallese et al., 1996; Rizzolatti et al., 1996a, (Table 5, Figs. 3 and 4). The midbrain is a relatively
1998). Evidently, these neurons seem to play a role in small region, surrounded by CSF and contains a large
a system that matches the observation and the execu- proportion of white matter. Moreover, cardiac related
tion of behavior. It has been suggested (Gallese and pulsatile brainstem motion might introduce further
Goldman, 1998), that some of the neural components difficulty in mapping this structure (Guimaraes et al.,
subservienttothecapacityofmindreadinginhumans 1998).Theveryfactthatasignificantsignalisdetected
are phylogenetically evolved from the mirror neurons in spite of all those limitations and the SPM filtering
found in the monkey. PET studies (Rizzolatti et al., mechanisms, indicates that the original signal related
1996b; Grafton et al., 1996), using execution and ob- to sexual arousal and erection sensation in the mid-
servation of object grasping, showed the activation of brainwasprobablyverystrong.Thismayberelatedto
theleftinferolateralfrontalcortex(inadditiontoother three types of neural connections:
areas) during observation of grasping but not during
execution. It is interesting that imagery of grasping 1. The midbrain is the storehouse of dopaminergic
alsocausedactivationofthesamearea(Graftonetal., (DA) neurons, located in the substantia nigra and in
1996). Phenomenologically speaking, sexual arousal theventraltegmentalarea,theiraxonsdividingexten-
provoked by watching actors perform sexual inter- sively, thus exerting their influence throughout the
course resembles a mirroring phenomenon. Mirroring, striatum,thelimbicsystemandthecerebralcortex.In
most likely, implies that the subject’s sexual arousal particular, the mesolimbic DA system appears to acti-
while watching the dyadic interaction happens vate behavior in response to sensory cues that signal
throughtheperspectiveofthemalefigure,althoughin theavailabilityofincentivesorreinforcers.Thetermi-
theory a male may also have the neural capacity to nal buttons of the mesolimbic DA neurons are located
mirrorfemaleactionsandstateofmind.However,one in the forebrain: nucleus accumbens (ventral stria-
should also consider an alternative mechanism of tum),amygdala,lateralseptum,hippocampus,andthe
arousal through a response to the female figure as a bed nucleus of stria terminalis. Midbrain DA neurons
powerfulstimulusinitsownright.Suchmechanismof fire bursts of activity, brought about by cortically reg-
arousal may be similar to the “cephalic phase” of ap- ulated afferents in response to sensory stimuli. The
petitive response to food stimulus, i.e., without “read- activity bursts give rise to a supra-additive release of
ing the mind” of the food...Interestingly, Redoute´ et dopamine and thus convey motivationally relevant in-
al. (2000), presenting both intercourse clips as well as formation to the forebrain. In this respect, it is note-
motionless female figures of graded sexual intensity, worthy that a variety of DA manipulations in the ven-
foundstrongactivationoftherightorbitofrontalcortex tralstriatumprofoundlyaffectthedisplayofappetitive
during clip watching but not during watching the elements of male sexual behavior in animals, yet, in-
highly arousing but motionless female. Nevertheless, terestingly, they do not affect copulatory behavior
theydidobservedactivationinthesameareawhenthe (Everitt,1990).Forexample,amarkedincreaseinDA
female figures were only moderately arousing. On the levelswasdetectedinthenucleusaccumbensofamale
other hand, evidence suggests that the orbitofrontal rat, when a female was introduced to him behind a
cortexisactivatedinresponsetothreetypesofprimary wirescreen.Thiselevatedlevelwasmaintainedduring
reinforcers: smell, taste, and pleasant touch (Francis, intromissionbutwasreducedsubstantiallyonejacula-
1999). It seems that future studies with meticulously tion, rising again immediately before the next copula-
designed paradigms are needed in order to estimate tory act (Phillips, 1989).
the neurocognitive significance of the difference be- 2. TheDAafferentsfromthemidbraintothemedial
tween stimuli that have “automated” appetitive quali- preoptic nucleus (MPA) of the hypothalamus were
ties, similar to food, and stimuli that possibly invoke shown to be essential for consummatory behavior of
“mind reading” through some form of mirroring. The intromission and ejaculation (Hull, 1995).
activation of the right inferolateral frontal cortex in 3. The midbrain is also a station between the hypo-
ourstudyasopposedtotheleft,reportedintheabove- thalamus and the peripheral and autonomic nervous
mentionedmirroringPETexperiments,isnoteworthy. systems.Ittransmitssomatosensoryinformationfrom
This could be explained by the fact that right hand thegenitalstotheMPAviaitsreticularformationcells
grasping is likely to preferentially activate the left and connects the hypothalamus with autonomic cen-
hemisphere,whilesexualarousal,asdiscussedbefore, ters via the periaqueductal gray matter.
114 BOCHER ET AL.
FIG.3. ClusterswithabovethresholdsignificantcorrelationbetweenincreasesinrelativerCBFandparticipants’scoring.Columns1,
2,and3pertaintoquestions1,2,and3,respectively.FordetailsseethelegendtoFig.1.