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Published in: Brain Structure and Function 7/2017

01-09-2017 | Original Article

GABA content within medial prefrontal cortex predicts the variability of fronto-limbic effective connectivity

Authors: Stefano Delli Pizzi, Piero Chiacchiaretta, Dante Mantini, Giovanna Bubbico, Richard A. Edden, Marco Onofrj, Antonio Ferretti, Laura Bonanni

Published in: Brain Structure and Function | Issue 7/2017

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Abstract

The amygdala-medial prefrontal cortex (mPFC) circuit plays a key role in social behavior. The amygdala and mPFC are bidirectionally connected, functionally and anatomically, via the uncinate fasciculus. Recent evidence suggests that GABA-ergic neurotransmission within the mPFC could be central to the regulation of amygdala activity related to emotions and anxiety processing. However, the functional and neurochemical interactions within amygdala-mPFC circuits are unclear. In the current study, multimodal magnetic resonance imaging techniques were combined to investigate effective connectivity within the amygdala-mPFC network and its relationship with mPFC neurotransmission in 22 healthy subjects aged between 41 and 88 years. Effective connectivity in the amygdala-mPFC circuit was assessed on resting-state functional magnetic resonance imaging data using spectral dynamic causal modelling. State and trait anxiety were also assessed. The mPFC was shown to be the target of incoming outputs from the amygdalae and the source of exciting inputs to the limbic system. The amygdalae were reciprocally connected by excitatory projections. About half of the variance relating to the strength of top–down endogenous connection between right amygdala and mPFC was explained by mPFC GABA levels. State anxiety was correlated with the strength of the endogenous connections between right amygdala and mPFC. We suggest that mPFC GABA content predicts variability in the effective connectivity within the mPFC-amygdala circuit, providing new insights on emotional physiology and the underlying functional and neurochemical interactions.
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Literature
go back to reference Abbate C, Luzzatti C, Vergani C (2007) Test delle matrici: velocità e accuratezza della ricerca visiva nel corso dell’invecchiamento. G Gerontol 55:11–20 Abbate C, Luzzatti C, Vergani C (2007) Test delle matrici: velocità e accuratezza della ricerca visiva nel corso dell’invecchiamento. G Gerontol 55:11–20
go back to reference Adhikari A, Lerner TN, Finkelstein J, Pak S, Jennings JH, Davidson TJ, Ferenczi E, Gunaydin LA, Mirzabekov JJ, Ye L, Kim SY, Lei A, Deisseroth K (2015) Basomedial amygdala mediates top-down control of anxiety and fear. Nature 527:179–185. doi:10.1038/nature15698 CrossRefPubMedPubMedCentral Adhikari A, Lerner TN, Finkelstein J, Pak S, Jennings JH, Davidson TJ, Ferenczi E, Gunaydin LA, Mirzabekov JJ, Ye L, Kim SY, Lei A, Deisseroth K (2015) Basomedial amygdala mediates top-down control of anxiety and fear. Nature 527:179–185. doi:10.​1038/​nature15698 CrossRefPubMedPubMedCentral
go back to reference Adolphs R, Damasio H, Tranel D, Damasio A (1996) Cortical systems for the recognition of emotion in facial expressions. J Neurosci 16:7678–7687PubMed Adolphs R, Damasio H, Tranel D, Damasio A (1996) Cortical systems for the recognition of emotion in facial expressions. J Neurosci 16:7678–7687PubMed
go back to reference Andersen SL, Teicher MH (1999) Serotonin laterality in amygdala predicts performance in the elevated plus maze in rats. NeuroReport 10:3497–3500CrossRefPubMed Andersen SL, Teicher MH (1999) Serotonin laterality in amygdala predicts performance in the elevated plus maze in rats. NeuroReport 10:3497–3500CrossRefPubMed
go back to reference Appollonio I, Leone M, Isella V, Piamarta F, Consoli T, Villa ML, Forapani E, Russo A, Nichelli P (2005) The Frontal Assessment Battery (FAB): normative values in an Italian population sample. Neurol Sci 26:108–116. doi:10.1007/s10072-005-0443-4 CrossRefPubMed Appollonio I, Leone M, Isella V, Piamarta F, Consoli T, Villa ML, Forapani E, Russo A, Nichelli P (2005) The Frontal Assessment Battery (FAB): normative values in an Italian population sample. Neurol Sci 26:108–116. doi:10.​1007/​s10072-005-0443-4 CrossRefPubMed
go back to reference Bastos-Leite AJ, Ridgway GR, Silveira C, Norton A, Reis S, Friston KJ (2015) Dysconnectivity within the default mode in first-episode schizophrenia: a stochastic dynamic causal modeling study with functional magnetic resonance imaging. Schizophr Bull 41:144–153. doi:10.1093/schbul/sbu080 CrossRefPubMed Bastos-Leite AJ, Ridgway GR, Silveira C, Norton A, Reis S, Friston KJ (2015) Dysconnectivity within the default mode in first-episode schizophrenia: a stochastic dynamic causal modeling study with functional magnetic resonance imaging. Schizophr Bull 41:144–153. doi:10.​1093/​schbul/​sbu080 CrossRefPubMed
go back to reference Blair K, Shaywitz J, Smith BW, Rhodes R, Geraci M, Jones M, McCaffrey D, Vythilingam M, Finger E, Jacobs M, Charney DS, Blair RJ, Drevets WC, Pine DS (2008) Response to emotional expressions in generalized social phobia and generalized anxiety disorder: evidence for separate disorders. Am J Psychiatry 165:1193–1202. doi:10.1176/appi.ajp.2008.07071060 CrossRefPubMedPubMedCentral Blair K, Shaywitz J, Smith BW, Rhodes R, Geraci M, Jones M, McCaffrey D, Vythilingam M, Finger E, Jacobs M, Charney DS, Blair RJ, Drevets WC, Pine DS (2008) Response to emotional expressions in generalized social phobia and generalized anxiety disorder: evidence for separate disorders. Am J Psychiatry 165:1193–1202. doi:10.​1176/​appi.​ajp.​2008.​07071060 CrossRefPubMedPubMedCentral
go back to reference Bogner W, Gruber S, Doelken M, Stadlbauer A, Ganslandt O, Boettcher U, Trattnig S, Doerfler A, Stefan H, Hammen T (2010) In vivo quantification of intracerebral GABA by single-voxel (1)H-MRS-How reproducible are the results? Eur J Radiol 73:526–531. doi:10.1016/j.ejrad.2009.01.014 CrossRefPubMed Bogner W, Gruber S, Doelken M, Stadlbauer A, Ganslandt O, Boettcher U, Trattnig S, Doerfler A, Stefan H, Hammen T (2010) In vivo quantification of intracerebral GABA by single-voxel (1)H-MRS-How reproducible are the results? Eur J Radiol 73:526–531. doi:10.​1016/​j.​ejrad.​2009.​01.​014 CrossRefPubMed
go back to reference Bonifazi P, Goldin M, Picardo MA, Jorquera I, Cattani A, Bianconi G, Represa A, Ben-Ari Y, Cossart R (2009) GABAergic hub neurons orchestrate synchrony in developing hippocampal networks. Science 326:1419–1424. doi:10.1126/science.1175509 CrossRefPubMed Bonifazi P, Goldin M, Picardo MA, Jorquera I, Cattani A, Bianconi G, Represa A, Ben-Ari Y, Cossart R (2009) GABAergic hub neurons orchestrate synchrony in developing hippocampal networks. Science 326:1419–1424. doi:10.​1126/​science.​1175509 CrossRefPubMed
go back to reference Canli T, Desmond JE, Zhao Z, Glover G, Gabrieli JDE (1998) Hemispheric asymmetry for emotional stimuli detected with fMRI. NeuroReport 9:3233–3239CrossRefPubMed Canli T, Desmond JE, Zhao Z, Glover G, Gabrieli JDE (1998) Hemispheric asymmetry for emotional stimuli detected with fMRI. NeuroReport 9:3233–3239CrossRefPubMed
go back to reference Chefer VI, Wang R, Shippenberg TS (2011) Basolateral amygdala-driven augmentation of medial prefrontal cortex GABAergic neurotransmission in response to environmental stimuli associated with cocaine administration. Neuropsychopharmacology 36:2018–2029. doi:10.1038/npp.2011.89 CrossRefPubMedPubMedCentral Chefer VI, Wang R, Shippenberg TS (2011) Basolateral amygdala-driven augmentation of medial prefrontal cortex GABAergic neurotransmission in response to environmental stimuli associated with cocaine administration. Neuropsychopharmacology 36:2018–2029. doi:10.​1038/​npp.​2011.​89 CrossRefPubMedPubMedCentral
go back to reference Constantinidis C, Williams GV, Goldman-Rakic (2002) A role for inhibition in shaping the temporal flow of information in prefrontal cortex. Nat Neurosci 5:175–180. doi:10.1038/nn799 CrossRefPubMed Constantinidis C, Williams GV, Goldman-Rakic (2002) A role for inhibition in shaping the temporal flow of information in prefrontal cortex. Nat Neurosci 5:175–180. doi:10.​1038/​nn799 CrossRefPubMed
go back to reference Courtin J, Chaudun F, Rozeske RR, Karalis N, Gonzalez-Campo C, Wurtz H, Abdi A, Baufreton J, Bienvenu TC, Herry C (2014) Prefrontal parvalbumin interneurons shape neuronal activity to drive fear expression. Nature 505:92–96. doi:10.1038/nature12755 CrossRefPubMed Courtin J, Chaudun F, Rozeske RR, Karalis N, Gonzalez-Campo C, Wurtz H, Abdi A, Baufreton J, Bienvenu TC, Herry C (2014) Prefrontal parvalbumin interneurons shape neuronal activity to drive fear expression. Nature 505:92–96. doi:10.​1038/​nature12755 CrossRefPubMed
go back to reference Crone JS, Lutkenhoff ES, Bio BJ, Laureys S, Monti MM (2017) Testing proposed neuronal models of effective connectivity within the Cortico-basal Ganglia-thalamo-cortical loop during loss of consciousness. Cereb Cortex. doi:10.1093/cercor/bhw112 (In press) Crone JS, Lutkenhoff ES, Bio BJ, Laureys S, Monti MM (2017) Testing proposed neuronal models of effective connectivity within the Cortico-basal Ganglia-thalamo-cortical loop during loss of consciousness. Cereb Cortex. doi:10.​1093/​cercor/​bhw112 (In press)
go back to reference Delli Pizzi S, Padulo C, Brancucci A, Bubbico G, Edden RA, Ferretti A, Franciotti R, Manippa V, Marzoli D, Onofrj M, Sepede G, Tartaro A, Tommasi L, Puglisi-Allegra S, Bonanni L (2016) GABA content within the ventromedial prefrontal cortex is related to trait anxiety. Soc Cogn Affect Neurosci 11:758–766. doi:10.1093/scan/nsv155 CrossRefPubMed Delli Pizzi S, Padulo C, Brancucci A, Bubbico G, Edden RA, Ferretti A, Franciotti R, Manippa V, Marzoli D, Onofrj M, Sepede G, Tartaro A, Tommasi L, Puglisi-Allegra S, Bonanni L (2016) GABA content within the ventromedial prefrontal cortex is related to trait anxiety. Soc Cogn Affect Neurosci 11:758–766. doi:10.​1093/​scan/​nsv155 CrossRefPubMed
go back to reference Delli Pizzi S, Chiacchiaretta P, Mantini D, Bubbico G, Edden RA, Di Giulio C, Onofrj M, Bonanni L (2017) Functional and neurochemical interactions within the amygdala-medial prefrontal cortex circuit and their relevance to emotional processing. Brain Struct Funct. doi:10.1007/s00429-016-1276-z Delli Pizzi S, Chiacchiaretta P, Mantini D, Bubbico G, Edden RA, Di Giulio C, Onofrj M, Bonanni L (2017) Functional and neurochemical interactions within the amygdala-medial prefrontal cortex circuit and their relevance to emotional processing. Brain Struct Funct. doi:10.​1007/​s00429-016-1276-z
go back to reference Duncan NW, Enzi B, Wiebking C, Northoff G (2011) Involvement of glutamate in rest-stimulus interaction between perigenual and supragenual anterior cingulate cortex: a combined fMRI-MRS study. Hum Brain Mapp 32:2172–2182. doi:10.1002/hbm.21179 CrossRefPubMed Duncan NW, Enzi B, Wiebking C, Northoff G (2011) Involvement of glutamate in rest-stimulus interaction between perigenual and supragenual anterior cingulate cortex: a combined fMRI-MRS study. Hum Brain Mapp 32:2172–2182. doi:10.​1002/​hbm.​21179 CrossRefPubMed
go back to reference Edden RA, Barker PB (2007) Spatial effects in the detection of gamma-aminobutyric acid: improved sensitivity at high fields using inner volume saturation. Magn Reson Med 58:1276–1282. doi:10.1002/mrm.21383 CrossRefPubMed Edden RA, Barker PB (2007) Spatial effects in the detection of gamma-aminobutyric acid: improved sensitivity at high fields using inner volume saturation. Magn Reson Med 58:1276–1282. doi:10.​1002/​mrm.​21383 CrossRefPubMed
go back to reference Edden RA, Puts NA, Harris AD, Barker PB, Evans CJ (2014) Gannet: a batch-processing tool for the quantitative analysis of gamma-aminobutyric acid-edited MR spectroscopy spectra. J Magn Reson Imaging 40:1445–1452. doi:10.1002/jmri.24478 CrossRefPubMed Edden RA, Puts NA, Harris AD, Barker PB, Evans CJ (2014) Gannet: a batch-processing tool for the quantitative analysis of gamma-aminobutyric acid-edited MR spectroscopy spectra. J Magn Reson Imaging 40:1445–1452. doi:10.​1002/​jmri.​24478 CrossRefPubMed
go back to reference Edden RA, Oeltzschner G, Harris AD, Puts NA, Chan KL, Boer VO, Schär M, Barker PB (2016) Prospective frequency correction for macromolecule-suppressed GABA editing at 3T. J Magn Reson Imaging. doi:10.1002/jmri.25304 Edden RA, Oeltzschner G, Harris AD, Puts NA, Chan KL, Boer VO, Schär M, Barker PB (2016) Prospective frequency correction for macromolecule-suppressed GABA editing at 3T. J Magn Reson Imaging. doi:10.​1002/​jmri.​25304
go back to reference Friston KJ, Frith CD, Fletcher P, Liddle PF, Frackowiak RSJ (1996) Functional topography: multidimensional scaling and functional connectivity in the brain. Cerebral cortex 6:156–164CrossRefPubMed Friston KJ, Frith CD, Fletcher P, Liddle PF, Frackowiak RSJ (1996) Functional topography: multidimensional scaling and functional connectivity in the brain. Cerebral cortex 6:156–164CrossRefPubMed
go back to reference Fullana MA, Harrison BJ, Soriano-Mas C, Vervliet B, Cardoner N, Àvila-Parcet A, Radua J (2015) Neural signatures of human fear conditioning: an updated and extended meta-analysis of fMRI studies. Mol Psychiatry 21:500–508. doi:10.1038/mp.2015.88 CrossRefPubMed Fullana MA, Harrison BJ, Soriano-Mas C, Vervliet B, Cardoner N, Àvila-Parcet A, Radua J (2015) Neural signatures of human fear conditioning: an updated and extended meta-analysis of fMRI studies. Mol Psychiatry 21:500–508. doi:10.​1038/​mp.​2015.​88 CrossRefPubMed
go back to reference Giovagnoli AR, Del Pesce M, Mascheroni S, Simoncelli M, Laiacona M, Capitani E (1996) Trail making test: normative values from 287 normal adult controls. Ital J Neurol Sci 17:305–309. doi:10.1007/BF01997792 CrossRefPubMed Giovagnoli AR, Del Pesce M, Mascheroni S, Simoncelli M, Laiacona M, Capitani E (1996) Trail making test: normative values from 287 normal adult controls. Ital J Neurol Sci 17:305–309. doi:10.​1007/​BF01997792 CrossRefPubMed
go back to reference Gläscher J, Adolphs R (2003) Processing of the arousal of subliminal and supraliminal emotional stimuli by the human amygdala. J Neurosci 23:10274–10282PubMed Gläscher J, Adolphs R (2003) Processing of the arousal of subliminal and supraliminal emotional stimuli by the human amygdala. J Neurosci 23:10274–10282PubMed
go back to reference Greenberg T, Carlson JM, Cha J, Hajcak G, Mujica-Parodi LR (2013) Ventromedial prefrontal cortex reactivity is altered in generalized anxiety disorder during fear generalization. Depress Anxiety 30:242–250. doi:10.1002/da.22016 CrossRefPubMed Greenberg T, Carlson JM, Cha J, Hajcak G, Mujica-Parodi LR (2013) Ventromedial prefrontal cortex reactivity is altered in generalized anxiety disorder during fear generalization. Depress Anxiety 30:242–250. doi:10.​1002/​da.​22016 CrossRefPubMed
go back to reference Groenink L, Joordens RJ, Hijzen TH, Dirks A, Olivier B (2000) Infusion of flesinoxan into the amygdala blocks the fear-potentiated startle. Neuroreport 11:2285–2288CrossRefPubMed Groenink L, Joordens RJ, Hijzen TH, Dirks A, Olivier B (2000) Infusion of flesinoxan into the amygdala blocks the fear-potentiated startle. Neuroreport 11:2285–2288CrossRefPubMed
go back to reference Henry PG, Dautry C, Hantraye P, Bloch G (2001) Brain GABA editing without macromolecule contamination. Magn Reson Med 45:517–520CrossRefPubMed Henry PG, Dautry C, Hantraye P, Bloch G (2001) Brain GABA editing without macromolecule contamination. Magn Reson Med 45:517–520CrossRefPubMed
go back to reference Horn DI, Yu C, Steiner J, Buchmann J, Kaufmann J, Osoba A, Eckert U, Zierhut KC, Schiltz K, He H, Biswal B, Bogerts B, Walter M (2010) Glutamatergic and resting-state functional connectivity correlates of severity in major depression—the role of pregenual anterior cingulate cortex and anterior insula. Front Syst Neurosci. doi:10.3389/fnsys.2010.00033 PubMedPubMedCentral Horn DI, Yu C, Steiner J, Buchmann J, Kaufmann J, Osoba A, Eckert U, Zierhut KC, Schiltz K, He H, Biswal B, Bogerts B, Walter M (2010) Glutamatergic and resting-state functional connectivity correlates of severity in major depression—the role of pregenual anterior cingulate cortex and anterior insula. Front Syst Neurosci. doi:10.​3389/​fnsys.​2010.​00033 PubMedPubMedCentral
go back to reference Makovac E, Meeten F, Watson DR, Herman A, Garfinkel SN, D Critchley H, Ottaviani C (2016) Alterations in amygdala-prefrontal functional connectivity account for excessive worry and autonomic dysregulation in generalized anxiety disorder. Biol Psychiatry 80:786–795. doi:10.1016/j.biopsych.2015.10.013 CrossRefPubMed Makovac E, Meeten F, Watson DR, Herman A, Garfinkel SN, D Critchley H, Ottaviani C (2016) Alterations in amygdala-prefrontal functional connectivity account for excessive worry and autonomic dysregulation in generalized anxiety disorder. Biol Psychiatry 80:786–795. doi:10.​1016/​j.​biopsych.​2015.​10.​013 CrossRefPubMed
go back to reference Mandal MK, Tandon SC, Asthana HS (1991) Right brain damage impairs recognition of negative emotions. Cortex 27:247–253CrossRefPubMed Mandal MK, Tandon SC, Asthana HS (1991) Right brain damage impairs recognition of negative emotions. Cortex 27:247–253CrossRefPubMed
go back to reference Markowitsch HJ (1998) Differential contribution of right and left amygdala to affective information processing. Behavioral. Neurology 11:233–244 Markowitsch HJ (1998) Differential contribution of right and left amygdala to affective information processing. Behavioral. Neurology 11:233–244
go back to reference McKlveen JM, Morano RL, Fitzgerald M, Zoubovsky S, Cassella SN, Scheimann JR, Ghosal S, Mahbod P, Packard BA, Myers B, Baccei ML, Herman JP (2016) Chronic stress increases prefrontal inhibition: a mechanism for stress-induced prefrontal dysfunction. Biol Psychiatry 80(10):754–764. doi:10.1016/j.biopsych.2016.03.2101 CrossRefPubMed McKlveen JM, Morano RL, Fitzgerald M, Zoubovsky S, Cassella SN, Scheimann JR, Ghosal S, Mahbod P, Packard BA, Myers B, Baccei ML, Herman JP (2016) Chronic stress increases prefrontal inhibition: a mechanism for stress-induced prefrontal dysfunction. Biol Psychiatry 80(10):754–764. doi:10.​1016/​j.​biopsych.​2016.​03.​2101 CrossRefPubMed
go back to reference Muthukumaraswamy SD, Evans CJ, Edden RA, Wise RG, Singh KD (2012) Individual variability in the shape and amplitude of the BOLD-HRF correlates with endogenous GABAergic inhibition. Hum Brain Mapp 33:455–465. doi:10.1002/hbm.21223 CrossRefPubMed Muthukumaraswamy SD, Evans CJ, Edden RA, Wise RG, Singh KD (2012) Individual variability in the shape and amplitude of the BOLD-HRF correlates with endogenous GABAergic inhibition. Hum Brain Mapp 33:455–465. doi:10.​1002/​hbm.​21223 CrossRefPubMed
go back to reference Near J, Edden R, Evans CJ, Paquin R, Harris A, Jezzard P (2015) Frequency and phase drift correction of magnetic resonance spectroscopy data by spectral registration in the time domain. Magn Reson Med 73:44–50. doi:10.1002/mrm.25094 CrossRefPubMed Near J, Edden R, Evans CJ, Paquin R, Harris A, Jezzard P (2015) Frequency and phase drift correction of magnetic resonance spectroscopy data by spectral registration in the time domain. Magn Reson Med 73:44–50. doi:10.​1002/​mrm.​25094 CrossRefPubMed
go back to reference Northoff G, Walter M, Schulte RF, Beck J, Dydak U, Henning A, Boeker H, Grimm S, Boesiger P (2007) GABA concentrations in the human ACC predict negative BOLD responses in fMRI. Nat Neurosci 10:1515–1517. doi:10.1038/nn2001 CrossRefPubMed Northoff G, Walter M, Schulte RF, Beck J, Dydak U, Henning A, Boeker H, Grimm S, Boesiger P (2007) GABA concentrations in the human ACC predict negative BOLD responses in fMRI. Nat Neurosci 10:1515–1517. doi:10.​1038/​nn2001 CrossRefPubMed
go back to reference Ochsner KN, Knierim K, Ludlow DH, Hanelin J, Ramachandran T, Glover G, Mackey SC (2004) Reflecting upon feelings: an fMRI study of neural systems supporting the attribution of emotion to self and other. J Cogn Neurosci 16:1746–1772. doi:10.1162/0898929042947829 CrossRefPubMed Ochsner KN, Knierim K, Ludlow DH, Hanelin J, Ramachandran T, Glover G, Mackey SC (2004) Reflecting upon feelings: an fMRI study of neural systems supporting the attribution of emotion to self and other. J Cogn Neurosci 16:1746–1772. doi:10.​1162/​0898929042947829​ CrossRefPubMed
go back to reference Phillips ML, Ladouceur CD, Drevets WC (2008) A neural model of voluntary and automatic emotion regulation: implications for understanding the pathophysiology and neurodevelopment of bipolar disorder. Mol Psychiatry 13:833–857. doi:10.1038/mp.2008.65 CrossRef Phillips ML, Ladouceur CD, Drevets WC (2008) A neural model of voluntary and automatic emotion regulation: implications for understanding the pathophysiology and neurodevelopment of bipolar disorder. Mol Psychiatry 13:833–857. doi:10.​1038/​mp.​2008.​65 CrossRef
go back to reference Russchen FT (1982) Amygdalopetal projections in the cat. I. Cortical afferent connections. A study with retrograde and anterograde tracing techniques. J Comp Neurol 206:159–179CrossRefPubMed Russchen FT (1982) Amygdalopetal projections in the cat. I. Cortical afferent connections. A study with retrograde and anterograde tracing techniques. J Comp Neurol 206:159–179CrossRefPubMed
go back to reference Sesack SR, Deutch AY, Roth RH, Bunney BS (1989) Topographical organization of the efferent projections of the medial prefrontal cortex in the rat: an anterograde tract-tracing study with Phaseolus vulgaris leucoagglutinin. J Comp Neurol 290:213–242CrossRefPubMed Sesack SR, Deutch AY, Roth RH, Bunney BS (1989) Topographical organization of the efferent projections of the medial prefrontal cortex in the rat: an anterograde tract-tracing study with Phaseolus vulgaris leucoagglutinin. J Comp Neurol 290:213–242CrossRefPubMed
go back to reference Sladky R, Höflich A, Küblböck M, Kraus C, Baldinger P, Moser E, Lanzenberger R, Windischberger C (2015) Disrupted effective connectivity between the amygdala and orbitofrontal cortex in social anxiety disorder during emotion discrimination revealed by dynamic causal modeling for fMRI. Cereb Cortex 25:895–903. doi:10.1093/cercor/bht279 CrossRefPubMed Sladky R, Höflich A, Küblböck M, Kraus C, Baldinger P, Moser E, Lanzenberger R, Windischberger C (2015) Disrupted effective connectivity between the amygdala and orbitofrontal cortex in social anxiety disorder during emotion discrimination revealed by dynamic causal modeling for fMRI. Cereb Cortex 25:895–903. doi:10.​1093/​cercor/​bht279 CrossRefPubMed
go back to reference Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TE, Johansen-Berg H, Bannister PR, De Luca M, Drobnjak I, Flitney DE, Niazy RK, Saunders J, Vickers J, Zhang Y, De Stefano N, Brady JM, Matthews PM (2004) Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23:S208–S219. doi:10.1016/j.neuroimage.2004.07.051 CrossRefPubMed Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TE, Johansen-Berg H, Bannister PR, De Luca M, Drobnjak I, Flitney DE, Niazy RK, Saunders J, Vickers J, Zhang Y, De Stefano N, Brady JM, Matthews PM (2004) Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23:S208–S219. doi:10.​1016/​j.​neuroimage.​2004.​07.​051 CrossRefPubMed
go back to reference Somerville LH, Wagner DD, Wig GS, Moran JM, Whalen PJ, Kelley WM (2013) Interactions between transient and sustained neural signals support the generation and regulation of anxious emotion. Cereb Cortex 23:49–60. doi:10.1093/cercor/bhr373 CrossRefPubMed Somerville LH, Wagner DD, Wig GS, Moran JM, Whalen PJ, Kelley WM (2013) Interactions between transient and sustained neural signals support the generation and regulation of anxious emotion. Cereb Cortex 23:49–60. doi:10.​1093/​cercor/​bhr373 CrossRefPubMed
go back to reference Spielberger CD (1983) Manual for the state–trait anxiety inventory STAI (Form Y). Mind Garden, Palo Alto Spielberger CD (1983) Manual for the state–trait anxiety inventory STAI (Form Y). Mind Garden, Palo Alto
go back to reference Stagg CJ, Bachtiar V, Amadi U, Gudberg CA, Ilie AS, Sampaio-Baptista C, O'Shea J, Woolrich M, Smith SM, Filippini N, Near J, Johansen-Berg H (2014) Local GABA concentration is related to network-level resting functional connectivity. eLife 3:e01465. doi:10.7554/eLife.01465 Stagg CJ, Bachtiar V, Amadi U, Gudberg CA, Ilie AS, Sampaio-Baptista C, O'Shea J, Woolrich M, Smith SM, Filippini N, Near J, Johansen-Berg H (2014) Local GABA concentration is related to network-level resting functional connectivity. eLife 3:e01465. doi:10.​7554/​eLife.​01465
go back to reference Urry HL, van Reekum CM, Johnstone T, Kalin NH, Thurow ME, Schaefer HS, Jackson CA, Frye CJ, Greischar LL, Alexander AL, Davidson RJ (2006) Amygdala and ventromedial prefrontal cortex are inversely coupled during regulation of negative affect and predict the diurnal pattern of cortisol secretion among older adults. J Neurosci 26:4415–4425. doi:10.1523/JNEUROSCI.3215-05.2006 CrossRefPubMed Urry HL, van Reekum CM, Johnstone T, Kalin NH, Thurow ME, Schaefer HS, Jackson CA, Frye CJ, Greischar LL, Alexander AL, Davidson RJ (2006) Amygdala and ventromedial prefrontal cortex are inversely coupled during regulation of negative affect and predict the diurnal pattern of cortisol secretion among older adults. J Neurosci 26:4415–4425. doi:10.​1523/​JNEUROSCI.​3215-05.​2006 CrossRefPubMed
go back to reference Wechsler D (1939) The measurement of adult intelligence. Williams & Wilkins Co, Baltimore Wechsler D (1939) The measurement of adult intelligence. Williams & Wilkins Co, Baltimore
go back to reference Wright CI, Martis B, Schwartz CE, Shin LM, Fischer HH, McMullin K et al (2003) Novelty responses and differential effects of order in the amygdala, substantia innominata, and inferior temporal cortex. Neuroimage 18:660–669CrossRefPubMed Wright CI, Martis B, Schwartz CE, Shin LM, Fischer HH, McMullin K et al (2003) Novelty responses and differential effects of order in the amygdala, substantia innominata, and inferior temporal cortex. Neuroimage 18:660–669CrossRefPubMed
go back to reference Zald DH, Donndelinger MJ, Pardo JV (1998) Elucidating dynamic brain interactions with across-subjects correlational analyses of positron emission tomographic data: the functional connectivity of the amygdala and orbitofrontal cortex during olfactory tasks. J Cereb Blood Flow 18:896–905CrossRef Zald DH, Donndelinger MJ, Pardo JV (1998) Elucidating dynamic brain interactions with across-subjects correlational analyses of positron emission tomographic data: the functional connectivity of the amygdala and orbitofrontal cortex during olfactory tasks. J Cereb Blood Flow 18:896–905CrossRef
Metadata
Title
GABA content within medial prefrontal cortex predicts the variability of fronto-limbic effective connectivity
Authors
Stefano Delli Pizzi
Piero Chiacchiaretta
Dante Mantini
Giovanna Bubbico
Richard A. Edden
Marco Onofrj
Antonio Ferretti
Laura Bonanni
Publication date
01-09-2017
Publisher
Springer Berlin Heidelberg
Published in
Brain Structure and Function / Issue 7/2017
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-017-1399-x

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