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					                                                                             Journal of medical ethics, I980, 6, 133-138



Biological aspects of homosexuality

Malcolm MacCulloch Park Lane Hospital, Maghull, Liverpool


Editor's note                                                    Table i The association between homosexual type (primary and
                                                                 secondary) and success at latestfollow up in response to avoidance
This paper is another of those prepared for a London             learning. Series and trial patients are combined
Medical Group symposium on homosexuality held in
October 1979. Dr MacCulloch describes a clinical trial                                 Primary          Secondary             Total
conducted on 73 patients, 30 ofwhom were selected. Early         Success                    5                36                41
calculations at the end of the trial confirmed an impression     Failure                   I2                10                22
that there were two categories of homosexuals primary            Total                     17                46                63
and secondary the former being those who reported that
they had never shown any heterosexual interest. A case           X2 = 12.2I
history of identical twins is highlighted in the control trial   p =   <O.OOI
between two kinds of aversion therapy and psychotherapy.         because he was finding the strain of maintaining a
   Dr MacCulloch offers evidence of a biochemical                heterosexual 'front' intolerable.
aetiology ofprimary homosexuality and suggests that ifthis
is upheld it will lead to markedly less hostility in the         Sexual history
attitudes of the puMlic and professions to homosexuals and       The patient's first sexual experience at the age of 13
to a different view of society by the homosexuals                was that of having another boy's naked body held
themselves.                                                      against his at a swimming baths. He was excited by
                                                                 this; on other similar occasions he later came to admire
                                                                 the physique of other boys. He began auto-
Introduction                                                     masturbation and phantasised males of his own age at
The origin of my argument that some homosexual                   the age of 17. He also bought physical culture books.
behaviour has a biological cause is clinical. In the             At the age of i8 he was picked up by a male in a public
course of treating 43 unselected patients presenting             convenience but declined to go with him for the pur-
complaining of homosexual behaviour and of treating a            pose of mutual masturbation. Later he regretted this
further 30 selected patients in a clinical trial, it was         decision and at the age of 23 he met a 35 year old man
noticed that patients who never had a history of                 under similar circumstances and practised intracrural
heterosexual interest throughout their lives appeared            sexual intercourse with pleasure mixed with some
to do rather less well than those patients who did give a        anxiety and nervousness. Within weeks he began to
positive heterosexual history. Preliminary calculations          make regular homosexual pick-ups and then began to
at the end of the trial confirmed this impression and the        go to another city specifically to make homosexual
patients are divided into two categories, primary and            pick-ups. He did so in order to avoid recognition in his
secondary homosexuals, the former being those cases              own town. He practised sodomy once at the age of 23
who, by their own report, had never at any time shown            following a heavy intake of alcohol. At the time of the
any heterosexual interest. Because the importance of             interview he was making homosexual pick-ups once
this primary secondary dichotomy was not appreci-
               -                                                 per week and practised intracrural sexual intercourse,
ated at the beginning of the trial, the random assigna-          kissing and petting. His auto-masturbatory phantasy
tion of patients to treatment was made without                   was of well-built males and various homosexual acts.
reference to this factor. Within that trial the small               He played with girls a good deal as a younger child,
group and sub-group numbers made statistical evalua-             preferring their company to that of boys and he did not
tion difficult but, however, it was possible to combine          play games. He was never attracted to females but
the total cohort of 30 trial patients and 36 of the series       commenced heterosexual dating at the age of I 5
patients for analysis and the association between                'because it was the thing to do'. He disliked holding
primary homosexuality and successful outcome at lat-             hands. Six months prior to presentation he tried kis-
est follow up was significant (p = <o.ooi).                      sing and petting but he said, 'I just can't bring myself
                                                                 to put on a normal act. I dislike girls'. (His sister-in-law
During the   course of our control trial between two              did not attract him in any sense).
kinds of aversion therapy and psychotherapy we saw a
24 year old man who was one of a pair of identical                Personal history
twins. His twin was exclusively heterosexual. The                 The twin birth was uncomplicated and his upbringing
patient referred himself via his general practitioner             unexceptional. He was described by the heterosexual
134 Malcolm MacCulloch


twin as doing 'girlish type things' as a child. There is a                                                                                         during the early years tended to smother the patient.
clear difference in their temperaments, the heterosex-                                                                                             On presentation he was tending to go out in the even-
ual twin being more outgoing and aggressive; the latter                                                                                            ings in order to avoid listening to his mother's health
felt that the patient was more close to their mother and                                                                                           complaints. She was, no doubt, the dominant parent.
was shown more physical affection.
                                                                                                                                                   TREATMENT
PERSONALITY                                                                                                                                        The patient received 24 sessions of anticipatory avoid-
There was evidence of life long self insecure personal-                                                                                            ance" followed by 24 sessions of classical condition-
ity abnormality showing sensitive features and at times                                                                                            ing and showed no shift either clinically or by the
ideas of reference. The homosexuality was beginning                                                                                                sexual orientation method.'
to have a developmental effect. He showed obsessional
features also. There was no hint of previous illness and                                                                                           FOLLOW UP
on examination his mental state was normal. His twin                                                                                               No change in sexual orientation had occurred at final
was interviewed using the same initial questionnaire                                                                                               follow up at 66 weeks post-treatment. His final Kinsey
and the common parental history was confirmed. The                                                                                                 rating was 6.
twin was entirely heterosexual and had always been so.
Family history                                                                                                                                     Discussion
His father was a foreman concreter and was a strict                                                                                                Perhaps the most striking feature of this case was the
parent with sensitive personality features. The patient                                                                                            complete discordance for sexual object choice. The
had little or no emotional contact with his father. His                                                                                            avoidance latencies are extremely irregular and do not
                                                                                                                                                                                              I



mother tended to complain of bodily ailments and                                                                                                   show any evidence of learning.

PATIENT 17                                                                                 AVOIDANCE                                           LATENCIES




            ,
                *2                f-       2 ez                ei
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                                                                 6
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                                                                                                                                                      6                 e       x                                                 us




                                  e11
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                                        A;i 7.         750              Z   I
                                                                                12
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                                                                                                                             5*                I          2        I                      ;6 *                          a *   A   *    v*




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                                                       a       is       6       12.        16    co,                     IZ           kk              ; . 1. ;3         z       ;A        4       4       Z,        i    a        ;6    ib   6   #a   a   m

                                                                                24            SESSIONS
                                                                                24            TRIALS PRECEDED                                                          BY       ESCAPE                         TRIALS

 Fig.   i   Twenty-four sessions of aversion therapy avoidance latencies with 24 trials in each session                                                                                                             -
                                                                                           Biological aspects of homosexuality 135


                        SEXUAL       ATTITUDE        SCORE

              PRE TREATMENT                   WITHIN TREATMENT               POST TREATMENT              FOLLQW UP
     -    .         -                                                    i
                                                                         *
                                                                                                     I


   48                        -X           $k
                                           ) X             x         "       X   -It
              1-7
   42                                                                                                                    I~~HOM
   36


   30


    24


    18


    12

     6.
         tI     ..IN
                5        4   3
                                 ..
                                 2
                                          4     12    24   36   48
                                                                         41 +i----,--w-r
                                                                             i    2 4 53
                                                                                                              ,
                                                                                                         Latesf
                                                                                                                     i


                                                                                                         Follow-up
                        MONTH                        SESSIONS                MONTHS

Fig. 2 The male andfemale sexual orientation method scores for a monozygotic twin patient 4 months prior to anticipatory avoidance
averson therapy treatment.


During 72 sessions of treatment, for 3 months after                      theory. It therefore seemed to us that an explanation
treatment, and at latest follow up 66 weeks post-                        must be sought which superposes change on an embryo
treatment the scores show no deviation from the pre-                     before learning takes place and which does not depend
treatment levels. I have not seen another case where the                 directly on heritable mechanisms. We have previously
sexually orientated method figures totally fail to vary                  postulated' that there may be hormonally sensitive
in response to treatment.                                                areas in the human fetal brain which 'are critically
   We were able to interview both his twin who had a                     susceptible to circulating levels of male and female
totally discordant early history and later sexual history                hormones' (p i69). We therefore turned to the animal
and his mother who confirmed the histories given by                      literature on sexual dimorphism which is extensive and
both twins. They had been reared together under                          which by the early I970s had generally concluded that
apparently normal conditions and their monozygocity                      for the inherent programme of sexual differentiation in
was established beyond doubt. The combined evi-                          both sexes, man was as female.
dence of the primaries'resistance to treatment, their                       The presence of androgens during the critical
markedly different histories from the secondary                          periods of sexual differentiation in animals has been
homosexuals and this pair of discordant monozygotic                      found to organise both genetic males and females to
twins led my colleagues and myself to begin to think                     possess masculine reproductive organs,2 masculinise
about an explanation for homosexual behaviour which                      hepatic steroidogenic enzymes,3 cause tonic (male pat-
would account for learned patterns of homosexual                         tern) hypothalamic control of gonadotrophic secre-
behaviour occurring in relatively normal people and                      tion4- and produce male sexual behaviour.7 At that
the existence of those in whom there has never been                      time it was thought that an absence of either gonad
any heterosexual interest or arousal and who appear                      during the critical developmental period allowed the
'different'. The monozygotic discordant twins                            expression of female characteristics which were
appeared to me to disallow a learning theory for the                     thought to be inborn.8 t
homosexual twin's condition and the heterosexual                            Experiments by Phoenix et al° showed how a gen-
twin's 'normality' would seem to disallow a genetic                      etic female could be masculinised by androgens and,
 136 Malcolm MacCulloch

paradoxically, by oestrogen. They left unsolved the            describe the occasional incidence of male external
problem of why fetal female brins were not mascu-              genitalia in girls born to mothers treated prenatally
linised by normal levels of endogenous fetal                   with male hormones. These females have almost
oestrogen. This problem was resolved by the critical           always been raised as boys and have themselves pre-
experiments of Shapiro et all who concluded that               ferred to continue in this way even when increased
raised serum progesterone in the female rat neonate            ovarian activity at puberty has begun to induce secon-
could function both to cause feminisation ofthe brain          dary feminine characteristics. This syndrome is sug-
and as a hormone antagonist to protect the develop-            gestive of male brain differentiation in the human
ing female brain from the masculinising effect of              female following prenatal exposure to abnormally high
both androgen and oestrogen.                                   levels of male sex hormones that are sufficient to over-
   To date there is little direct evidence that the brain is   come the normal protective effect of progesterone
sexually dimorphic in humans although there is one             against normally occurring amounts of androgen and is
striking experiment in humans that is very closely             entirely consistent with our theory of female homosex-
analogous to that of Phoenix et al. 10 Wilkins et al"2         uality.


                                Androgen/Progesterone          mixture produced
                                by the feto placental Unit




                        A>P                                                X       P>A
                                                                                   P

                  Androgen effect                                       Progesterone effect




Genetic                                                                                               Genetic
Male Brain                                                                                            Female Brain




              Male Differentiated Brain                              Female Differentiated Brain
                   Male Identity                                           Fej e Identity




                     Male Behaviour                                         Female Behaviour
Fig. 3 Summary ofparts of the mechanism responsible for normal sexual dimorphism in man.
                                                                               Biological aspects of homosexuality 137

Under production                            Over production                             Ant ibody absorpt ion
of androgen                                 of progesterone                             of androgen




                                           Abnormal A < P ratio




                                                                                               Normal A:P ratio



                                                                           14                    Target cell
                                                                                                 insensitivity
                                                                                                 to androgen




                                           Feminised hypothalamic neurone

Fig. 4 Some possible mechanisms which would lead to a female sexual differentiation in a male brain.

A biochemical theory for the aetiology of male and             human, hormones control brain differentiation and the
female homosexuality                                           direction of subsequent sexual object choice in adult
                                                               life.
The            of androgens during critical periods in
        presence                                                  Co-workers have suggested that the behaviour of
utero organises masculinisation of offspring and their         primary male homosexuals has as its essential cause a
absence allows the expression of female characteristics;       female differentiated brain. We see this mis-
the limited available evidence in the human male is in         differentiation as resulting from the absence of an
support of this concept. Additionally, in animals, brain       androgen effect in the hypothalamus during the critical
feminisation itself may in fact be hormonally con-             period for brain sex differentiation.
trolled by the in utero conditions. It may be that in the         As regards female homosexuals the findings of
138 Malcolm MacCulloch

Shapiro et allI relating to brain feminisation and to the   ety at large feels free to take a hostile view if the
protection of the brain from the masculinising effect of    behaviour in question is one which has been pro-
both androgens and oestrogens by progesterone pro-          scribed. In the case of homosexual behaviour there
vides a new theoretical basis for an explanation of         remains much hostility and disapprobation towards
primary lesbianism. We suggest that this behaviour          homosexuals even amongst the supposedly more
arises from a male differentiated brain in a genetic        enlightened members of society such as doctors,
female. As with male homosexuals, we suggest that           lawyers and judges. It seems clear to me that a
primary lesbians could comprise aetiologically              biochemical view of the aetiology of primary homo-
heterogenous groups consisting of subjects whose            sexuality, if upheld, is bound to lead to a marked
foetal hypothalami were insufficiently feminised            change in the attitudes of the public and professions
and/or protected from normal amounts of oestrogen by        to homosexuals and to a different view of society by
deficits in progesterone and subjects whose brains were     the homosexuals themselves.
masculinised by abnormal amounts of androgen in the
presence of a normal amount of progesterone.
                                                            References
The nature of the in utero defect                           'Feldman, M P and MacCulloch, M J (I971). Homosexual
                                                                  behaviour: therapy and assessment. In: H J Eysenck
Bidlingmaier et al'3 in a very striking experiment have           (Ed). Experimental psychology, vol I4. Oxford,
described how an immune reaction to testosterone in               Pergamon Press. pp 20-30, 55-64, 95-I05.
the pregnant rabbit could alter the sexual development      2Jost, A (1953). Recent progress in hormone research, 8,
of male offsprings. They produced pregnant female                 319-4I3.
rabbits whose serum contained antibodies capable of         3Demoor, P (I968). Endocrinology, 82, 480-492.
neutralising the biological activity of testosterone and    4Pfeiffer, C A (1936). American journal of anatomy, 58,
whose male offsprings were shown to have elevated                195-225.
serum testosterone levels and a development of their        5Wilson, J G, Hamilton, J B and Young, W C (i94i). Endoc-
                                                                 rinology, 29, 784-789.
reproductive system identical to that in a normal           6Barraclough, C A and Gorski, R A (I961 ). Endocrinology, 68,
female rabbit. This experiment demonstrates that tes-            68-79.
tosterone antibodies can pass the placental barrier and     7Grady, K L, Phoenix, C H and Young, W C (i965).Journal
that developing sex organs can be deprived ofthe effect          ofcomparative and physiological psychology, 59, 176-i82.
of testosterone (despite a feedback-induced increase in     8Grady, K L and Phoenix, C H (I963). American zoologist, 3,
absolute testosterone level) leading to changes in mor-          482-483.
phogenesis similar to testicular atrophy experiments in     9Harris, G W (I964). EndocrinologY, 74, 627-648.
other species.                                               °0Phoenix, C H, Goy, R W, Gerrall, A A and Young, W C
                                                                  (I959). Endocrinology, 65, 369-382.
                                                            "Shapiro, B H, Goldman, A S, Bongiouanni, A M and
Conclusion                                                        Marino, J M (0976b). Nature, 264, 795-796.
                                                            "Wilkins, L, Jones, H W, Holman, G H and Stempeel, R S
Where an identifiable enduring pattern of behaviour is            (I958). Journal of clinical endocrinology, x8, 559-585.
known to arise predominantly from environmental fac-         3Bidlingmaier, F, Knorr, D and Neumann, F (I977).
tors, life experience and self regulated behaviour, soci-         Nature, 266, 647-648.

				
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