Skip to main content
Top
Published in: Journal of Neural Transmission 2/2023

21-01-2023 | Positron Emission Tomography | Psychiatry and Preclinical Psychiatric Studies - Original Article

Is abnormal metabolism in the olfactory bulb and amygdala associated with bipolar disorder?

Authors: Muhammet Sancaktar, Şengül Kocamer Şahin, Bahadır Demir, Umut Elboğa, Gülçin Elboğa, Abdurrahman Altındağ

Published in: Journal of Neural Transmission | Issue 2/2023

Login to get access

Abstract

Accumulated evidence has demonstrated abnormal amygdala activation in bipolar disorder (BD). The olfactory bulb (OB) has vigorous connections with the amygdala. Although odor-related functions of the OB decreased during the evolutionary process, we hypothesized that an evolved OB with increased activation in emotion regulation may be one of the main factors affecting amygdala functions in BD. Our aim was to investigate metabolism in the OB and amygdala in patients with BD. Twenty-six patients diagnosed with BD according to DSM-5 diagnostic criteria were included in this cross-sectional study. Metabolism in the OB and amygdala was assessed using fluorodeoxyglucose positron emission tomography/CT in patients with BD. The OB and amygdala metabolism was compared with the patients’ Z scores. Both OB and amygdala metabolic activities were significantly higher than in the controls. A positive correlation was detected between right/left amygdala metabolism and right OB metabolism (p < 0.05, r:467 and r:662, respectively). This study increased our understanding of the etiopathogenesis of BD. In BD, the main cause of hypermetabolism in the amygdala may be increased metabolism in the OB. During evolution, the OB may have assumed a dominant role in emotional processing rather than olfactory functions.
Literature
go back to reference Abler B, Greenhouse I, Ongur D et al (2008) Abnormal reward system activation in mania. Neuropsychopharmacology 33:2217–2227CrossRef Abler B, Greenhouse I, Ongur D et al (2008) Abnormal reward system activation in mania. Neuropsychopharmacology 33:2217–2227CrossRef
go back to reference Al-Mousawi AH, Evans N, Ebmeier KP et al (1996) Limbic dysfunction in schizophrenia and mania. Br J Psychiatry 169:509–516CrossRef Al-Mousawi AH, Evans N, Ebmeier KP et al (1996) Limbic dysfunction in schizophrenia and mania. Br J Psychiatry 169:509–516CrossRef
go back to reference Altshuler L, Bookheimer S, Proenza MA et al (2005) Increased amygdala activation during mania: a functional magnetic resonance imaging study. Am J Psychiatry 162:1211–1213CrossRef Altshuler L, Bookheimer S, Proenza MA et al (2005) Increased amygdala activation during mania: a functional magnetic resonance imaging study. Am J Psychiatry 162:1211–1213CrossRef
go back to reference Belvederi Murri M, Ekkekakis P, Magagnoli M et al (2019) Physical exercise in major depression: reducing the mortality gap while improving clinical outcomes. Front Psychiatry 9:762CrossRef Belvederi Murri M, Ekkekakis P, Magagnoli M et al (2019) Physical exercise in major depression: reducing the mortality gap while improving clinical outcomes. Front Psychiatry 9:762CrossRef
go back to reference Blumberg HP, Stern E, Martinez D et al (2000) Increased anterior cingulate and caudate activity in bipolar mania. Biol Psychiatry 48:1045–1052CrossRef Blumberg HP, Stern E, Martinez D et al (2000) Increased anterior cingulate and caudate activity in bipolar mania. Biol Psychiatry 48:1045–1052CrossRef
go back to reference Blumberg HP, Donegan NH, Sanislow CA et al (2005) Preliminary evidence for medication effects on functional abnormalities in the amygdala and anterior cingulate in bipolar disorder. Psychopharmacology 183:308–313CrossRef Blumberg HP, Donegan NH, Sanislow CA et al (2005) Preliminary evidence for medication effects on functional abnormalities in the amygdala and anterior cingulate in bipolar disorder. Psychopharmacology 183:308–313CrossRef
go back to reference Brewer WJ, Wood SJ, McGorry PD et al (2003) Impairment of olfactory identification ability in individuals at ultra-high risk for psychosis who later develop schizophrenia. Am J Psychiatry 160:1790–1794CrossRef Brewer WJ, Wood SJ, McGorry PD et al (2003) Impairment of olfactory identification ability in individuals at ultra-high risk for psychosis who later develop schizophrenia. Am J Psychiatry 160:1790–1794CrossRef
go back to reference Carmichael ST, Clugnet M, Price JL (1994) Central olfactory connections in the macaque monkey. J Comp Neurol 346:403–434CrossRef Carmichael ST, Clugnet M, Price JL (1994) Central olfactory connections in the macaque monkey. J Comp Neurol 346:403–434CrossRef
go back to reference Chen C, Suckling J, Lennox BR et al (2011) A quantitative meta-analysis of fMRI studies in bipolar disorder. Bipolar Disord 13:1–15CrossRef Chen C, Suckling J, Lennox BR et al (2011) A quantitative meta-analysis of fMRI studies in bipolar disorder. Bipolar Disord 13:1–15CrossRef
go back to reference Costafreda SG, Brammer MJ, David AS, Fu CHY (2008) Predictors of amygdala activation during the processing of emotional stimuli: a meta-analysis of 385 PET and fMRI studies. Brain Res Rev 58:57–70CrossRef Costafreda SG, Brammer MJ, David AS, Fu CHY (2008) Predictors of amygdala activation during the processing of emotional stimuli: a meta-analysis of 385 PET and fMRI studies. Brain Res Rev 58:57–70CrossRef
go back to reference Croy I, Hummel T (2017) Olfaction as a marker for depression. J Neurol 264:631–638CrossRef Croy I, Hummel T (2017) Olfaction as a marker for depression. J Neurol 264:631–638CrossRef
go back to reference Doty RL, Deems DA, Stellar S (1988) Olfactory dysfunction in parkinsonism: a general deficit unrelated to neurologic signs, disease stage, or disease duration. Neurology 38:1237CrossRef Doty RL, Deems DA, Stellar S (1988) Olfactory dysfunction in parkinsonism: a general deficit unrelated to neurologic signs, disease stage, or disease duration. Neurology 38:1237CrossRef
go back to reference Drevets WC (2003) Neuroimaging abnormalities in the amygdala in mood disorders. Ann N Y Acad Sci 985:420–444CrossRef Drevets WC (2003) Neuroimaging abnormalities in the amygdala in mood disorders. Ann N Y Acad Sci 985:420–444CrossRef
go back to reference First MB (2014) Structured clinical interview for the DSM (SCID). The encyclopedia of clinical psychology 1–6 First MB (2014) Structured clinical interview for the DSM (SCID). The encyclopedia of clinical psychology 1–6
go back to reference Foland LC, Altshuler LL, Bookheimer SY et al (2008) Evidence for deficient modulation of amygdala response by prefrontal cortex in bipolar mania. Psychiatry Res Neuroimaging 162:27–37CrossRef Foland LC, Altshuler LL, Bookheimer SY et al (2008) Evidence for deficient modulation of amygdala response by prefrontal cortex in bipolar mania. Psychiatry Res Neuroimaging 162:27–37CrossRef
go back to reference Houenou J, Frommberger J, Carde S et al (2011) Neuroimaging-based markers of bipolar disorder: evidence from two meta-analyses. J Affect Disord 132:344–355CrossRef Houenou J, Frommberger J, Carde S et al (2011) Neuroimaging-based markers of bipolar disorder: evidence from two meta-analyses. J Affect Disord 132:344–355CrossRef
go back to reference Hough CJ, Ursano RJ (2006) A guide to the genetics of psychiatric disease. Psychiatry 69:1–20CrossRef Hough CJ, Ursano RJ (2006) A guide to the genetics of psychiatric disease. Psychiatry 69:1–20CrossRef
go back to reference Hughes GM, Teeling EC, Higgins DG (2014) Loss of olfactory receptor function in hominin evolution. PLoS ONE 9:e84714CrossRef Hughes GM, Teeling EC, Higgins DG (2014) Loss of olfactory receptor function in hominin evolution. PLoS ONE 9:e84714CrossRef
go back to reference Kalmar JH, Wang F, Chepenik LG et al (2009) Relation between amygdala structure and function in adolescents with bipolar disorder. J Am Acad Child Adolesc Psychiatry 48:636–642CrossRef Kalmar JH, Wang F, Chepenik LG et al (2009) Relation between amygdala structure and function in adolescents with bipolar disorder. J Am Acad Child Adolesc Psychiatry 48:636–642CrossRef
go back to reference Kazour F, Richa S, Char CA et al (2020) Olfactory memory in depression: state and trait differences between bipolar and unipolar disorders. Brain Sci 10:189CrossRef Kazour F, Richa S, Char CA et al (2020) Olfactory memory in depression: state and trait differences between bipolar and unipolar disorders. Brain Sci 10:189CrossRef
go back to reference Lahera G, Ruiz-Murugarren S, Fernandez-Liria A et al (2013) 2078–Relationship between olfactory function and social cognition in euthymic bipolar patients. Eur Psychiatry 28:1 Lahera G, Ruiz-Murugarren S, Fernandez-Liria A et al (2013) 2078–Relationship between olfactory function and social cognition in euthymic bipolar patients. Eur Psychiatry 28:1
go back to reference Lahera G, Ruiz-Murugarren S, Fernández-Liria A et al (2016) Relationship between olfactory function and social cognition in euthymic bipolar patients. CNS Spectr 21:53–59CrossRef Lahera G, Ruiz-Murugarren S, Fernández-Liria A et al (2016) Relationship between olfactory function and social cognition in euthymic bipolar patients. CNS Spectr 21:53–59CrossRef
go back to reference Lawrence NS, Williams AM, Surguladze S et al (2004) Subcortical and ventral prefrontal cortical neural responses to facial expressions distinguish patients with bipolar disorder and major depression. Biol Psychiatry 55:578–587CrossRef Lawrence NS, Williams AM, Surguladze S et al (2004) Subcortical and ventral prefrontal cortical neural responses to facial expressions distinguish patients with bipolar disorder and major depression. Biol Psychiatry 55:578–587CrossRef
go back to reference Liu H, Tang Y, Womer F et al (2014) Differentiating patterns of amygdala-frontal functional connectivity in schizophrenia and bipolar disorder. Schizophr Bull 40:469–477CrossRef Liu H, Tang Y, Womer F et al (2014) Differentiating patterns of amygdala-frontal functional connectivity in schizophrenia and bipolar disorder. Schizophr Bull 40:469–477CrossRef
go back to reference Lledo P-M, Valley M (2016) Adult olfactory bulb neurogenesis. Cold Spring Harb Perspect Biol 8:a018945CrossRef Lledo P-M, Valley M (2016) Adult olfactory bulb neurogenesis. Cold Spring Harb Perspect Biol 8:a018945CrossRef
go back to reference Mah L, Zarate CA Jr, Singh J et al (2007) Regional cerebral glucose metabolic abnormalities in bipolar II depression. Biol Psychiatry 61:765–775CrossRef Mah L, Zarate CA Jr, Singh J et al (2007) Regional cerebral glucose metabolic abnormalities in bipolar II depression. Biol Psychiatry 61:765–775CrossRef
go back to reference Mak GK, Enwere EK, Gregg C et al (2007) Male pheromone–stimulated neurogenesis in the adult female brain: possible role in mating behavior. Nat Neurosci 10:1003–1011CrossRef Mak GK, Enwere EK, Gregg C et al (2007) Male pheromone–stimulated neurogenesis in the adult female brain: possible role in mating behavior. Nat Neurosci 10:1003–1011CrossRef
go back to reference Mesholam RI, Moberg PJ, Mahr RN, Doty RL (1998) Olfaction in neurodegenerative disease: a meta-analysis of olfactory functioning in Alzheimer’s and Parkinson’s diseases. Arch Neurol 55:84–90CrossRef Mesholam RI, Moberg PJ, Mahr RN, Doty RL (1998) Olfaction in neurodegenerative disease: a meta-analysis of olfactory functioning in Alzheimer’s and Parkinson’s diseases. Arch Neurol 55:84–90CrossRef
go back to reference Ming G, Song H (2005) Adult neurogenesis in the mammalian central nervous system. Annu Rev Neurosci 28:223–250CrossRef Ming G, Song H (2005) Adult neurogenesis in the mammalian central nervous system. Annu Rev Neurosci 28:223–250CrossRef
go back to reference Minoshima S, Frey KA, Koeppe RA et al (1995) A diagnostic approach in Alzheimer’s disease using three-dimensional stereotactic surface projections of fluorine-18-FDG PET. J Nucl Med 36:1238–1248 Minoshima S, Frey KA, Koeppe RA et al (1995) A diagnostic approach in Alzheimer’s disease using three-dimensional stereotactic surface projections of fluorine-18-FDG PET. J Nucl Med 36:1238–1248
go back to reference Northcutt RG (2002) Understanding vertebrate brain evolution. Integr Comp Biol 42:743–756CrossRef Northcutt RG (2002) Understanding vertebrate brain evolution. Integr Comp Biol 42:743–756CrossRef
go back to reference Odone A, Lugo A, Amerio A et al (2020) COVID-19 lockdown impact on lifestyle habits of Italian adults. Acta Bio Medica: Atenei Parmensis 91:87 Odone A, Lugo A, Amerio A et al (2020) COVID-19 lockdown impact on lifestyle habits of Italian adults. Acta Bio Medica: Atenei Parmensis 91:87
go back to reference Pouliot S, Jones-Gotman M (2008) Medial temporal-lobe damage and memory for emotionally arousing odors. Neuropsychologia 46:1124–1134CrossRef Pouliot S, Jones-Gotman M (2008) Medial temporal-lobe damage and memory for emotionally arousing odors. Neuropsychologia 46:1124–1134CrossRef
go back to reference Rich BA, Vinton DT, Roberson-Nay R et al (2006) Limbic hyperactivation during processing of neutral facial expressions in children with bipolar disorder. Proc Natl Acad Sci 103:8900–8905CrossRef Rich BA, Vinton DT, Roberson-Nay R et al (2006) Limbic hyperactivation during processing of neutral facial expressions in children with bipolar disorder. Proc Natl Acad Sci 103:8900–8905CrossRef
go back to reference Sah P, Faber ESL, Lopez de Armentia M, Power J (2003) The amygdaloid complex: anatomy and physiology. Physiol Rev 83:803–834CrossRef Sah P, Faber ESL, Lopez de Armentia M, Power J (2003) The amygdaloid complex: anatomy and physiology. Physiol Rev 83:803–834CrossRef
go back to reference Song C, Leonard BE (2005) The olfactory bulbectomised rat as a model of depression. Neurosci Biobehav Rev 29:627–647CrossRef Song C, Leonard BE (2005) The olfactory bulbectomised rat as a model of depression. Neurosci Biobehav Rev 29:627–647CrossRef
go back to reference Spielberg JM, Beall EB, Hulvershorn LA et al (2016) Resting state brain network disturbances related to hypomania and depression in medication-free bipolar disorder. Neuropsychopharmacology 41:3016–3024CrossRef Spielberg JM, Beall EB, Hulvershorn LA et al (2016) Resting state brain network disturbances related to hypomania and depression in medication-free bipolar disorder. Neuropsychopharmacology 41:3016–3024CrossRef
go back to reference Szymanski LA, Keller M (2014) Activation of the olfactory system in response to male odors in female prepubertal mice. Behav Brain Res 271:30–38CrossRef Szymanski LA, Keller M (2014) Activation of the olfactory system in response to male odors in female prepubertal mice. Behav Brain Res 271:30–38CrossRef
go back to reference Thome J, Deloyer J, Coogan AN et al (2021) The impact of the early phase of the COVID-19 pandemic on mental-health services in Europe. World J Biol Psychiatry 22:516–525CrossRef Thome J, Deloyer J, Coogan AN et al (2021) The impact of the early phase of the COVID-19 pandemic on mental-health services in Europe. World J Biol Psychiatry 22:516–525CrossRef
go back to reference Turetsky BI, Kamath V, Calkins ME et al (2012) Olfaction and schizophrenia clinical risk status: just the facts. Schizophr Res 139:260CrossRef Turetsky BI, Kamath V, Calkins ME et al (2012) Olfaction and schizophrenia clinical risk status: just the facts. Schizophr Res 139:260CrossRef
go back to reference Wesley MS, Manjula M, Thirthalli J (2018) Interepisodic functioning in patients with bipolar disorder in remission. Indian J Psychol Med 40:52–60CrossRef Wesley MS, Manjula M, Thirthalli J (2018) Interepisodic functioning in patients with bipolar disorder in remission. Indian J Psychol Med 40:52–60CrossRef
go back to reference Wrynn AS, Mac Sweeney CP, Franconi F et al (2000) An in-vivo magnetic resonance imaging study of the olfactory bulbectomized rat model of depression. Brain Res 879:193–199CrossRef Wrynn AS, Mac Sweeney CP, Franconi F et al (2000) An in-vivo magnetic resonance imaging study of the olfactory bulbectomized rat model of depression. Brain Res 879:193–199CrossRef
Metadata
Title
Is abnormal metabolism in the olfactory bulb and amygdala associated with bipolar disorder?
Authors
Muhammet Sancaktar
Şengül Kocamer Şahin
Bahadır Demir
Umut Elboğa
Gülçin Elboğa
Abdurrahman Altındağ
Publication date
21-01-2023
Publisher
Springer Vienna
Published in
Journal of Neural Transmission / Issue 2/2023
Print ISSN: 0300-9564
Electronic ISSN: 1435-1463
DOI
https://doi.org/10.1007/s00702-023-02587-9

Other articles of this Issue 2/2023

Journal of Neural Transmission 2/2023 Go to the issue

Psychiatry and Preclinical Psychiatric Studies - Original Article

Brain instability in dynamic functional connectivity in schizophrenia

Psychiatry and Preclinical Psychiatric Studies - Original Article

Genome-wide methylation analysis of treatment resistant schizophrenia

Neurology and Preclinical Neurological Studies - Original Article

Axial postural abnormalities and pain in Parkinson’s disease

Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine