Brain response to putative pheromones in lesbian women.
Proc Natl Acad Sci U S A. 2006 May 23;103(21):8269-74. Epub 2006 May 16.
Berglund H, Lindström P, Savic I.
The progesterone derivative 4,16-androstadien-3-one (AND) and the estrogen-like steroid estra-1,3,5(10),16-tetraen-3-ol (EST) are candidate compounds for human pheromones. In previous positron emission tomography studies, we found that smelling AND and EST activated regions primarily incorporating the sexually dimorphic nuclei of the anterior hypothalamus, that this activation was differentiated with respect to sex and compound, and that homosexual men processed AND congruently with heterosexual women rather than heterosexual men. These observations indicate involvement of the anterior hypothalamus in physiological processes related to sexual orientation in humans. We expand the information on this issue in the present study by performing identical positron emission tomography experiments on 12 lesbian women. In contrast to heterosexual women, lesbian women processed AND stimuli by the olfactory networks and not the anterior hypothalamus. Furthermore, when smelling EST, they partly shared activation of the anterior hypothalamus with heterosexual men. These data support our previous results about differentiated processing of pheromone-like stimuli in humans and further strengthen the notion of a coupling between hypothalamic neuronal circuits and sexual preferences.
Department of Medicine, and Stockholm Brain Institute, Karolinska University Hospital, Karolinska Institutet, 171 76 Stockholm, Sweden.
Brain response to putative pheromones in homosexual men.
Proc Natl Acad Sci U S A. 2005 May 17;102(20):7356-61. Epub 2005 May 9.
Savic I, Berglund H, Lindström P.
The testosterone derivative 4,16-androstadien-3-one (AND) and the estrogen-like steroid estra-1,3,5(10),16-tetraen-3-ol (EST) are candidate compounds for human pheromones. AND is detected primarily in male sweat, whereas EST has been found in female urine. In a previous positron emission tomography study, we found that smelling AND and EST activated regions covering sexually dimorphic nuclei of the anterior hypothalamus, and that this activation was differentiated with respect to sex and compound. In the present study, the pattern of activation induced by AND and EST was compared among homosexual men, heterosexual men, and heterosexual women. In contrast to heterosexual men, and in congruence with heterosexual women, homosexual men displayed hypothalamic activation in response to AND. Maximal activation was observed in the medial preoptic area/anterior hypothalamus, which, according to animal studies, is highly involved in sexual behavior. As opposed to putative pheromones, common odors were processed similarly in all three groups of subjects and engaged only the olfactory brain (amygdala, piriform, orbitofrontal, and insular cortex). These findings show that our brain reacts differently to the two putative pheromones compared with common odors, and suggest a link between sexual orientation and hypothalamic neuronal processes.
Department of Clinical Neuroscience, Karolinska University Hospital, 171 76 Stockholm, Sweden. ivanka.savic-berglund@neuro.ki.se
Smelling of odorous sex hormone-like compounds causes sex-differentiated hypothalamic activations in humans.
Neuron. 2001 Aug 30;31(4):661-8.
Savic I, Berglund H, Gulyas B, Roland P.
The anatomical pathways for processing of odorous stimuli include the olfactory nerve projection to the olfactory bulb, the trigeminal nerve projection to somatosensory and insular cortex, and the projection from the accessory olfactory bulb to the hypothalamus. In the majority of tetrapods, the sex-specific effects of pheromones on reproductive behavior is mediated via the hypothalamic projection. However, the existence of this projection in humans has been regarded as improbable because humans lack a discernable accessory olfactory bulb. Here, we show that women smelling an androgen-like compound activate the hypothalamus, with the center of gravity in the preoptic and ventromedial nuclei. Men, in contrast, activate the hypothalamus (center of gravity in paraventricular and dorsomedial nuclei) when smelling an estrogen-like substance. This sex-dissociated hypothalamic activation suggests a potential physiological substrate for a sex-differentiated behavioral response in humans.
Division of Human Brain Research, Department of Neuroscience, Karolinska Institute, Stockholm, Sweden. ivanka.savic-berglund@neuro.ki.se
Brain imaging studies of the functional organization of human olfaction.
Neuroscientist. 2002 Jun;8(3):204-11.
Savic I.
It is believed that sensory functions are organized in a hierarchical and parallel manner. The sense of smell differs in several aspects from other senses: odors can immediately elicit emotional evocations, they are remembered after a long time, and they are difficult to label. This raises the question of whether odorous stimuli may be processed differently from the other sensory stimuli. New data from brain imaging studies suggest that this is not the case and that the specific characteristics of the sense of smell can be attributed to the engagement of limbic structures at an early stage in the signal processing.
Department of Neuroscience, Karolinska Institute, Stockholm, Sweden. ivanka.savic-berglund@neuro.ki.se
Functional magnetic resonance imaging of human olfaction.
Neuroimaging Clin N Am. 2001 May;11(2):237-50, viii.
Weismann M, Yousry I, Heuberger E, Nolte A, Ilmberger J, Kobal G, Yousry TA, Kettenmann B, Naidich TP.
Olfaction is our basic sense phylogenetically and embryologically. Little is known, however, about how the human brain encodes the quality of odors, odor-associated memories, and emotions. Olfactory information is projected from the olfactory bulb to the primary olfactory cortex, which is composed of the anterior olfactory nucleus, the olfactory tubercle, the piriform cortex, the amygdala, the periamygdaloid region, and the entorhinal cortex. From there, the primary olfactory cortex projects to secondary olfactory regions including the hippocampus, ventral striatum and pallidum, hypothalamus, thalamus, orbitofrontal cortex, agranular insular cortex, and cingulate gyrus. Functional MR studies using olfactory stimuli as paradigms show activation of many of these areas and can advance our understanding of odor perception in humans.
Department of Radiology, Medical University, Luebeck, Germany.
Imaging of brain activation by odorants in humans.
Curr Opin Neurobiol. 2002 Aug;12(4):455-61.
Savic I.
Application of positron emission tomography and magnetic resonance imaging has provided several new insights into various olfactory functions. One is that sniffing and smelling engage separate subsystems in the human olfactory cortex. Another is that perception of odorous compounds (odorants) is mediated by a set of core regions, which are partly different for pure olfactory than for olfactory plus trigeminal odorants. Depending on the task associated with odor perception, the core regions are recruited together with other circuits, in a parallel and hierarchical manner. The sense of smell seems, therefore, to be organized similarly to other sensory modalities, and the specific psychophysical characteristics of olfaction should be attributed to an early involvement of the limbic system rather than to a conceptually different mode of processing.
Department of Neuroscience, Karolinska Institute, Retziusväg 8, 17177, Stockholm, Sweden. ivanka.savic-berglund@neuro.ki.se
Brain activation during odor perception in males and females.
Neuroreport. 2001 Jul 3;12(9):2027-33.
Bengtsson S, Berglund H, Gulyas B, Cohen E, Savic I.
Several studies indicate that women outperform men in olfactory identification tasks. The psychophysical data are more divergent when it comes to gender differences at levels of odor processing which are cognitively less demanding. We therefore compared cerebral activation with H2(15)O PET in 12 females and 11 males during birhinal passive smelling of odors and odorless air. The odorous compounds (odorants) were pure olfactory, or mixed olfactory and weakly trigeminal. Using odorless air as the baseline condition, activations were found bilaterally in the amygdala, piriform and insular cortices in both sexes, irrespective of the odor. No gender difference was detected in the pattern of cerebral activation (random effect analysis SPM99, corrected p less than 0.05) or in the subjective perception of odors. Males and females seem to use similar cerebral circuits during the passive perception of odors. The reported female superiority in assessing olfactory information including odor identification is probably an effect of a difference at a cognitive, rather than perceptive level of olfactory processing.
Division of Human Brain Research, Department of Neuroscience, Huddinge University Hospital, Karolinska Institute, Berzelius v. 3, S-171 77 Stockholm, Sweden.
Proc Natl Acad Sci U S A. 2006 May 23;103(21):8269-74. Epub 2006 May 16.
Berglund H, Lindström P, Savic I.
The progesterone derivative 4,16-androstadien-3-one (AND) and the estrogen-like steroid estra-1,3,5(10),16-tetraen-3-ol (EST) are candidate compounds for human pheromones. In previous positron emission tomography studies, we found that smelling AND and EST activated regions primarily incorporating the sexually dimorphic nuclei of the anterior hypothalamus, that this activation was differentiated with respect to sex and compound, and that homosexual men processed AND congruently with heterosexual women rather than heterosexual men. These observations indicate involvement of the anterior hypothalamus in physiological processes related to sexual orientation in humans. We expand the information on this issue in the present study by performing identical positron emission tomography experiments on 12 lesbian women. In contrast to heterosexual women, lesbian women processed AND stimuli by the olfactory networks and not the anterior hypothalamus. Furthermore, when smelling EST, they partly shared activation of the anterior hypothalamus with heterosexual men. These data support our previous results about differentiated processing of pheromone-like stimuli in humans and further strengthen the notion of a coupling between hypothalamic neuronal circuits and sexual preferences.
Department of Medicine, and Stockholm Brain Institute, Karolinska University Hospital, Karolinska Institutet, 171 76 Stockholm, Sweden.
Brain response to putative pheromones in homosexual men.
Proc Natl Acad Sci U S A. 2005 May 17;102(20):7356-61. Epub 2005 May 9.
Savic I, Berglund H, Lindström P.
The testosterone derivative 4,16-androstadien-3-one (AND) and the estrogen-like steroid estra-1,3,5(10),16-tetraen-3-ol (EST) are candidate compounds for human pheromones. AND is detected primarily in male sweat, whereas EST has been found in female urine. In a previous positron emission tomography study, we found that smelling AND and EST activated regions covering sexually dimorphic nuclei of the anterior hypothalamus, and that this activation was differentiated with respect to sex and compound. In the present study, the pattern of activation induced by AND and EST was compared among homosexual men, heterosexual men, and heterosexual women. In contrast to heterosexual men, and in congruence with heterosexual women, homosexual men displayed hypothalamic activation in response to AND. Maximal activation was observed in the medial preoptic area/anterior hypothalamus, which, according to animal studies, is highly involved in sexual behavior. As opposed to putative pheromones, common odors were processed similarly in all three groups of subjects and engaged only the olfactory brain (amygdala, piriform, orbitofrontal, and insular cortex). These findings show that our brain reacts differently to the two putative pheromones compared with common odors, and suggest a link between sexual orientation and hypothalamic neuronal processes.
Department of Clinical Neuroscience, Karolinska University Hospital, 171 76 Stockholm, Sweden. ivanka.savic-berglund@neuro.ki.se
Smelling of odorous sex hormone-like compounds causes sex-differentiated hypothalamic activations in humans.
Neuron. 2001 Aug 30;31(4):661-8.
Savic I, Berglund H, Gulyas B, Roland P.
The anatomical pathways for processing of odorous stimuli include the olfactory nerve projection to the olfactory bulb, the trigeminal nerve projection to somatosensory and insular cortex, and the projection from the accessory olfactory bulb to the hypothalamus. In the majority of tetrapods, the sex-specific effects of pheromones on reproductive behavior is mediated via the hypothalamic projection. However, the existence of this projection in humans has been regarded as improbable because humans lack a discernable accessory olfactory bulb. Here, we show that women smelling an androgen-like compound activate the hypothalamus, with the center of gravity in the preoptic and ventromedial nuclei. Men, in contrast, activate the hypothalamus (center of gravity in paraventricular and dorsomedial nuclei) when smelling an estrogen-like substance. This sex-dissociated hypothalamic activation suggests a potential physiological substrate for a sex-differentiated behavioral response in humans.
Division of Human Brain Research, Department of Neuroscience, Karolinska Institute, Stockholm, Sweden. ivanka.savic-berglund@neuro.ki.se
Brain imaging studies of the functional organization of human olfaction.
Neuroscientist. 2002 Jun;8(3):204-11.
Savic I.
It is believed that sensory functions are organized in a hierarchical and parallel manner. The sense of smell differs in several aspects from other senses: odors can immediately elicit emotional evocations, they are remembered after a long time, and they are difficult to label. This raises the question of whether odorous stimuli may be processed differently from the other sensory stimuli. New data from brain imaging studies suggest that this is not the case and that the specific characteristics of the sense of smell can be attributed to the engagement of limbic structures at an early stage in the signal processing.
Department of Neuroscience, Karolinska Institute, Stockholm, Sweden. ivanka.savic-berglund@neuro.ki.se
Functional magnetic resonance imaging of human olfaction.
Neuroimaging Clin N Am. 2001 May;11(2):237-50, viii.
Weismann M, Yousry I, Heuberger E, Nolte A, Ilmberger J, Kobal G, Yousry TA, Kettenmann B, Naidich TP.
Olfaction is our basic sense phylogenetically and embryologically. Little is known, however, about how the human brain encodes the quality of odors, odor-associated memories, and emotions. Olfactory information is projected from the olfactory bulb to the primary olfactory cortex, which is composed of the anterior olfactory nucleus, the olfactory tubercle, the piriform cortex, the amygdala, the periamygdaloid region, and the entorhinal cortex. From there, the primary olfactory cortex projects to secondary olfactory regions including the hippocampus, ventral striatum and pallidum, hypothalamus, thalamus, orbitofrontal cortex, agranular insular cortex, and cingulate gyrus. Functional MR studies using olfactory stimuli as paradigms show activation of many of these areas and can advance our understanding of odor perception in humans.
Department of Radiology, Medical University, Luebeck, Germany.
Imaging of brain activation by odorants in humans.
Curr Opin Neurobiol. 2002 Aug;12(4):455-61.
Savic I.
Application of positron emission tomography and magnetic resonance imaging has provided several new insights into various olfactory functions. One is that sniffing and smelling engage separate subsystems in the human olfactory cortex. Another is that perception of odorous compounds (odorants) is mediated by a set of core regions, which are partly different for pure olfactory than for olfactory plus trigeminal odorants. Depending on the task associated with odor perception, the core regions are recruited together with other circuits, in a parallel and hierarchical manner. The sense of smell seems, therefore, to be organized similarly to other sensory modalities, and the specific psychophysical characteristics of olfaction should be attributed to an early involvement of the limbic system rather than to a conceptually different mode of processing.
Department of Neuroscience, Karolinska Institute, Retziusväg 8, 17177, Stockholm, Sweden. ivanka.savic-berglund@neuro.ki.se
Brain activation during odor perception in males and females.
Neuroreport. 2001 Jul 3;12(9):2027-33.
Bengtsson S, Berglund H, Gulyas B, Cohen E, Savic I.
Several studies indicate that women outperform men in olfactory identification tasks. The psychophysical data are more divergent when it comes to gender differences at levels of odor processing which are cognitively less demanding. We therefore compared cerebral activation with H2(15)O PET in 12 females and 11 males during birhinal passive smelling of odors and odorless air. The odorous compounds (odorants) were pure olfactory, or mixed olfactory and weakly trigeminal. Using odorless air as the baseline condition, activations were found bilaterally in the amygdala, piriform and insular cortices in both sexes, irrespective of the odor. No gender difference was detected in the pattern of cerebral activation (random effect analysis SPM99, corrected p less than 0.05) or in the subjective perception of odors. Males and females seem to use similar cerebral circuits during the passive perception of odors. The reported female superiority in assessing olfactory information including odor identification is probably an effect of a difference at a cognitive, rather than perceptive level of olfactory processing.
Division of Human Brain Research, Department of Neuroscience, Huddinge University Hospital, Karolinska Institute, Berzelius v. 3, S-171 77 Stockholm, Sweden.
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