Skip to main content
Top
Published in: Behavioral and Brain Functions 1/2023

Open Access 01-12-2023 | Obsessive-Compulsive Disorder | Research

Mapping the neuroanatomical abnormalities in a phenotype of male compulsive rats

Authors: Elena Martín-González, Ángeles Prados-Pardo, Stephen J. Sawiak, Jeffrey W. Dalley, Daniel Padro, Pedro Ramos-Cabrer, Santiago Mora, Margarita Moreno-Montoya

Published in: Behavioral and Brain Functions | Issue 1/2023

Login to get access

Abstract

Compulsivity is considered a transdiagnostic dimension in obsessive–compulsive and related disorders, characterized by heterogeneous cognitive and behavioral phenotypes associated with abnormalities in cortico-striatal-thalamic-cortical circuitry. The present study investigated the structural morphology of white and gray matter in rats selected for low- (LD) and high- (HD) compulsive drinking behavior on a schedule-induced polydipsia (SIP) task. Regional brain morphology was assessed using ex-vivo high-resolution magnetic resonance imaging (MRI). Voxel-based morphometry of segmented MRI images revealed larger white matter volumes in anterior commissure and corpus callosum of HD rats compared with LD rats. HD rats also showed significantly larger regional volumes of dorsolateral orbitofrontal cortex, striatum, amygdala, hippocampus, midbrain, sub-thalamic nucleus, and cerebellum. By contrast, the medial prefrontal cortex was significantly smaller in HD rats compared with LD rats with no significant group differences in whole brain, ventricular, or cerebrospinal fluid volumes. These findings show that limbic cortico-basal ganglia structures implicated in impulse control disorders are distinct in rats that are vulnerable to develop compulsive behavior. Such abnormalities may be relevant to the etiology of compulsive disorders in humans.
Appendix
Available only for authorised users
Literature
7.
go back to reference Fineberg NA, Hollander E, Pallanti S, Walitza S, Grünblatt E, Dell’Osso BM, Albert U, Geller DA, Brakoulias V, Reddy YCJ, Arumugham SS, Shavitt RG, Drummond L, Grancini B, De Carlo V, Cinosi E, Chamberlain SR, Ioannidis K, Rodriguez CI, Garg K, Castle D, Van Ameringen V, Stein DJ, Carmi L, Zohar J, Menchon JM. Clinical advances in obsessive-compulsive disorder: a position statement by the International College of Obsessive-Compulsive Spectrum Disorders. Int Clin Psychopharmacol. 2020. https://doi.org/10.1097/YIC.0000000000000314.CrossRefPubMedPubMedCentral Fineberg NA, Hollander E, Pallanti S, Walitza S, Grünblatt E, Dell’Osso BM, Albert U, Geller DA, Brakoulias V, Reddy YCJ, Arumugham SS, Shavitt RG, Drummond L, Grancini B, De Carlo V, Cinosi E, Chamberlain SR, Ioannidis K, Rodriguez CI, Garg K, Castle D, Van Ameringen V, Stein DJ, Carmi L, Zohar J, Menchon JM. Clinical advances in obsessive-compulsive disorder: a position statement by the International College of Obsessive-Compulsive Spectrum Disorders. Int Clin Psychopharmacol. 2020. https://​doi.​org/​10.​1097/​YIC.​0000000000000314​.CrossRefPubMedPubMedCentral
19.
25.
go back to reference Sonne J, Reddy V, Beato MR. Neuroanatomy, Substantia Nigra. In StatPearls (Issue December 2018). 2020. Sonne J, Reddy V, Beato MR. Neuroanatomy, Substantia Nigra. In StatPearls (Issue December 2018). 2020.
27.
go back to reference Boedhoe PSW, Schmaal L, Abe Y, Ameis SH, Arnold PD, Batistuzzo MC, Benedetti F, Beucke JC, Bollettini I, Bose A, Brem S, Calvo A, Cheng Y, Cho KK, Dallaspezia S, Denys D, Fitzgerald KD, Fouche J-P, Giménez M, Gruner P, Hanna GL, Hibar DP, Hoexter MQ, Hu H, Huyser C, Ikari K, Jahanshad N, Kathmann N, Kaufmann C, Koch K, Kwon JS, Lazaro L, Liu Y, Lochner C, Marsh R, Martínez-Zalacaín I, Mataix-Cols D, Menchón JM, Minuzzi L, Nakamae T, Nakao T, Narayanaswamy JC, Piras F, Piras F, Pittenger C, Janardhan Reddy YC, Sato JR, Simpson HB, Soreni N, Soriano-Mas C, Spalletta G, Stevens MC, Szeszko PR, Tolin DF, Venkatasubramanian G, Walitza S, Wang Z, van Wingen GA, Xu J, Xu X, Yun J-Y, Zhao Q, Thompson PM, Stein DJ, vanden Heuvel OA, Abe OA, Alonso P,Ameis SH, Arnold PD, Bargalló N, Batistuzzo MC, Benedetti, Beucke JC, Boedhoe PSW, Bollettini I, Bose A, Brem S, Busatto GF, Calvo A, Calvo R, Cath DC, Cheng Y, Cho KK, Dallaspezia S, FE Vries de, Wit SJ, Denys D, Fang Y, Fitzgerald KD, Fontaine M, Fouche J-P, Giménez M, GrunerP, Hanna GL, Hibar DP, Hoexter MQ, Hu H, Huyser C, Ikari K, Jahanshad N, Kathmann N, Kaufmann C, Khadka S, Koch K, SooKwon J, Lazaro L, Liu Y, Lochner C, Marsh R, Martínez-Zalacaín I, Mataix-Cols D, Menchón JM, Miguel EC, Minuzzii L, Morer A, Nakamae T, Nakao T, Narayanaswamy JC, Piras F, Piras F, Pittenger C, JanardhanReddy YC, Sato JR, Simpson HB, Schmaal L, Soreni N, Soriano-Mas C, Spalletta G, Stein DJ, Stevens MC, Szeszko PR, Thompson PM, Tolin DF, Veltman DJ, Venkatasubramanian G, van den Heuvel OA, van der Werf YD, van Wingen GA, Walitza S, Wang Z, Xu J, Xu X, Yun J-Y, Zhao Q. Distinct subcortical volume alterations in pediatric and adult OCD: a worldwide meta- and mega-analysis. Am J Psychiatry. 2017;174(1):60. https://doi.org/10.1176/appi.ajp.2016.16020201.CrossRefPubMed Boedhoe PSW, Schmaal L, Abe Y, Ameis SH, Arnold PD, Batistuzzo MC, Benedetti F, Beucke JC, Bollettini I, Bose A, Brem S, Calvo A, Cheng Y, Cho KK, Dallaspezia S, Denys D, Fitzgerald KD, Fouche J-P, Giménez M, Gruner P, Hanna GL, Hibar DP, Hoexter MQ, Hu H, Huyser C, Ikari K, Jahanshad N, Kathmann N, Kaufmann C, Koch K, Kwon JS, Lazaro L, Liu Y, Lochner C, Marsh R, Martínez-Zalacaín I, Mataix-Cols D, Menchón JM, Minuzzi L, Nakamae T, Nakao T, Narayanaswamy JC, Piras F, Piras F, Pittenger C, Janardhan Reddy YC, Sato JR, Simpson HB, Soreni N, Soriano-Mas C, Spalletta G, Stevens MC, Szeszko PR, Tolin DF, Venkatasubramanian G, Walitza S, Wang Z, van Wingen GA, Xu J, Xu X, Yun J-Y, Zhao Q, Thompson PM, Stein DJ, vanden Heuvel OA, Abe OA, Alonso P,Ameis SH, Arnold PD, Bargalló N, Batistuzzo MC, Benedetti, Beucke JC, Boedhoe PSW, Bollettini I, Bose A, Brem S, Busatto GF, Calvo A, Calvo R, Cath DC, Cheng Y, Cho KK, Dallaspezia S, FE Vries de, Wit SJ, Denys D, Fang Y, Fitzgerald KD, Fontaine M, Fouche J-P, Giménez M, GrunerP, Hanna GL, Hibar DP, Hoexter MQ, Hu H, Huyser C, Ikari K, Jahanshad N, Kathmann N, Kaufmann C, Khadka S, Koch K, SooKwon J, Lazaro L, Liu Y, Lochner C, Marsh R, Martínez-Zalacaín I, Mataix-Cols D, Menchón JM, Miguel EC, Minuzzii L, Morer A, Nakamae T, Nakao T, Narayanaswamy JC, Piras F, Piras F, Pittenger C, JanardhanReddy YC, Sato JR, Simpson HB, Schmaal L, Soreni N, Soriano-Mas C, Spalletta G, Stein DJ, Stevens MC, Szeszko PR, Thompson PM, Tolin DF, Veltman DJ, Venkatasubramanian G, van den Heuvel OA, van der Werf YD, van Wingen GA, Walitza S, Wang Z, Xu J, Xu X, Yun J-Y, Zhao Q. Distinct subcortical volume alterations in pediatric and adult OCD: a worldwide meta- and mega-analysis. Am J Psychiatry. 2017;174(1):60. https://​doi.​org/​10.​1176/​appi.​ajp.​2016.​16020201.CrossRefPubMed
37.
go back to reference Szeszko PR, MacMillan S, McMeniman M, Lorch E, Madden R, Ivey J, Banerjee SP, Moore GJ, Rosenberg DR. Amygdala volume reductions in pediatric patients with obsessive-compulsive disorder treated with paroxetine: Preliminary findings. Neuropsychopharmacol. 2004;29(4):826. https://doi.org/10.1038/sj.npp.1300399.CrossRef Szeszko PR, MacMillan S, McMeniman M, Lorch E, Madden R, Ivey J, Banerjee SP, Moore GJ, Rosenberg DR. Amygdala volume reductions in pediatric patients with obsessive-compulsive disorder treated with paroxetine: Preliminary findings. Neuropsychopharmacol. 2004;29(4):826. https://​doi.​org/​10.​1038/​sj.​npp.​1300399.CrossRef
39.
go back to reference Gowda SM, Narayanaswamy JC, Hazari N, Bose A, Chhabra H, Balachander S, Bhaskarapillai B, Shivakumar V, Venkatasubramanian G, Reddy YCJ. Efficacy of pre-supplementary motor area transcranial direct current stimulation for treatment resistant obsessive compulsive disorder: a randomized, double blinded, sham controlled trial. Brain Stimul. 2019;12(4):922. https://doi.org/10.1016/j.brs.2019.02.005.CrossRefPubMed Gowda SM, Narayanaswamy JC, Hazari N, Bose A, Chhabra H, Balachander S, Bhaskarapillai B, Shivakumar V, Venkatasubramanian G, Reddy YCJ. Efficacy of pre-supplementary motor area transcranial direct current stimulation for treatment resistant obsessive compulsive disorder: a randomized, double blinded, sham controlled trial. Brain Stimul. 2019;12(4):922. https://​doi.​org/​10.​1016/​j.​brs.​2019.​02.​005.CrossRefPubMed
41.
go back to reference Senço NM, Huang Y, D’Urso G, Parra LC, Bikson M, Mantovani A, Shavitt RG, Hoexter MQ, Miguel EC, Brunoni AR. Transcranial direct current stimulation in obsessive-compulsive disorder: emerging clinical evidence and considerations for optimal montage of electrodes. Expert Rev Med Dev. 2015;12(4):381. https://doi.org/10.1586/17434440.2015.1037832.CrossRef Senço NM, Huang Y, D’Urso G, Parra LC, Bikson M, Mantovani A, Shavitt RG, Hoexter MQ, Miguel EC, Brunoni AR. Transcranial direct current stimulation in obsessive-compulsive disorder: emerging clinical evidence and considerations for optimal montage of electrodes. Expert Rev Med Dev. 2015;12(4):381. https://​doi.​org/​10.​1586/​17434440.​2015.​1037832.CrossRef
46.
go back to reference Anticevic A, Hu S, Zhang S, Savic A, Billingslea E, Wasylink S, Repovs G, Cole MW, Bednarski S, Krystal JH, Bloch MH, Li CSR, Pittenger C. Global resting-state functional magnetic resonance imaging analysis identifies frontal cortex, striatal, and cerebellar dysconnectivity in obsessive-compulsive disorder. Biol Psychiatry. 2014;75(8):595. https://doi.org/10.1016/j.biopsych.2013.10.021.CrossRefPubMed Anticevic A, Hu S, Zhang S, Savic A, Billingslea E, Wasylink S, Repovs G, Cole MW, Bednarski S, Krystal JH, Bloch MH, Li CSR, Pittenger C. Global resting-state functional magnetic resonance imaging analysis identifies frontal cortex, striatal, and cerebellar dysconnectivity in obsessive-compulsive disorder. Biol Psychiatry. 2014;75(8):595. https://​doi.​org/​10.​1016/​j.​biopsych.​2013.​10.​021.CrossRefPubMed
53.
go back to reference Falk JL. Production of polydipsia in normal rats by an intermittent food schedule. Science. 1961;133(3447):195–6.CrossRefPubMed Falk JL. Production of polydipsia in normal rats by an intermittent food schedule. Science. 1961;133(3447):195–6.CrossRefPubMed
66.
go back to reference Belin-Rauscent A, Daniel ML, Puaud M, Jupp B, Sawiak S, Howett D, McKenzie C, Caprioli D, Besson M, Robbins TW, Everitt BJ, Dalley JW, Belin D. From impulses to maladaptive actions: the insula is a neurobiological gate for the development of compulsive behavior. Mol Psychiatry. 2016;21(4):491–9. https://doi.org/10.1038/mp.2015.140.CrossRefPubMed Belin-Rauscent A, Daniel ML, Puaud M, Jupp B, Sawiak S, Howett D, McKenzie C, Caprioli D, Besson M, Robbins TW, Everitt BJ, Dalley JW, Belin D. From impulses to maladaptive actions: the insula is a neurobiological gate for the development of compulsive behavior. Mol Psychiatry. 2016;21(4):491–9. https://​doi.​org/​10.​1038/​mp.​2015.​140.CrossRefPubMed
70.
go back to reference Tobias W, Lythgoe D, Williams S. rBET: Making BET work for Rodent Brains. Proc Int Soc Magn Reson Med. 2013 Tobias W, Lythgoe D, Williams S. rBET: Making BET work for Rodent Brains. Proc Int Soc Magn Reson Med. 2013
75.
go back to reference Paxinos G, Watson C. The rat brain in stereotaxic coordinates. 6th ed. Amsterdam: Elsevier; 2007. Paxinos G, Watson C. The rat brain in stereotaxic coordinates. 6th ed. Amsterdam: Elsevier; 2007.
76.
go back to reference Straathof M, Blezer ELA, van Heijningen C, Smeele CE, van der Toorn A, Buitelaar J, de Ruiter S, Naaijen J, Akkermans S, Mennes M, Zwiers M, Ilbegi S, Hennissen L, Glennon J, van de Vondervoort I, Kapusta K, Bielczyk NA, Amiri H, Havenith M, Dijkhuizen RM. Structural and functional MRI of altered brain development in a novel adolescent rat model of quinpirole-induced compulsive checking behavior. Eur Neuropsychopharmacol. 2020. https://doi.org/10.1016/j.euroneuro.2020.02.004.CrossRefPubMed Straathof M, Blezer ELA, van Heijningen C, Smeele CE, van der Toorn A, Buitelaar J, de Ruiter S, Naaijen J, Akkermans S, Mennes M, Zwiers M, Ilbegi S, Hennissen L, Glennon J, van de Vondervoort I, Kapusta K, Bielczyk NA, Amiri H, Havenith M, Dijkhuizen RM. Structural and functional MRI of altered brain development in a novel adolescent rat model of quinpirole-induced compulsive checking behavior. Eur Neuropsychopharmacol. 2020. https://​doi.​org/​10.​1016/​j.​euroneuro.​2020.​02.​004.CrossRefPubMed
78.
go back to reference Haar CV, Martens KM, Bashir A, McInnes KA, Cheng WH, Cheung H, Stukas S, Barron C, Ladner T, Welch KA, Cripton PA, Winstanley CA, Wellington CL. Repetitive closed-head impact model of engineered rotational acceleration (CHIMERA) injury in rats increases impulsivity, decreases dopaminergic innervation in the olfactory tubercle and generates white matter inflammation, tau phosphorylation and degener. Exp Neurol. 2019. https://doi.org/10.1016/j.expneurol.2019.02.012.CrossRef Haar CV, Martens KM, Bashir A, McInnes KA, Cheng WH, Cheung H, Stukas S, Barron C, Ladner T, Welch KA, Cripton PA, Winstanley CA, Wellington CL. Repetitive closed-head impact model of engineered rotational acceleration (CHIMERA) injury in rats increases impulsivity, decreases dopaminergic innervation in the olfactory tubercle and generates white matter inflammation, tau phosphorylation and degener. Exp Neurol. 2019. https://​doi.​org/​10.​1016/​j.​expneurol.​2019.​02.​012.CrossRef
81.
go back to reference Giona F, Pagano J, Verpelli C, Sala C. Another step toward understanding brain functional connectivity alterations in autism: an Editorial Highlight for “Neurobiological substrates underlying corpus callosum hypoconnectivity and brain metabolic patterns in the valproic acid rat model of autism. J Neurochem. 2021;159(1):12. https://doi.org/10.1111/jnc.15452.CrossRefPubMed Giona F, Pagano J, Verpelli C, Sala C. Another step toward understanding brain functional connectivity alterations in autism: an Editorial Highlight for “Neurobiological substrates underlying corpus callosum hypoconnectivity and brain metabolic patterns in the valproic acid rat model of autism. J Neurochem. 2021;159(1):12. https://​doi.​org/​10.​1111/​jnc.​15452.CrossRefPubMed
82.
go back to reference Uccelli NA, Codagnone MG, Traetta ME, Levanovich N, Rosato Siri MV, Urrutia L, Falasco G, Vázquez S, Pasquini JM, Reinés AG. Neurobiological substrates underlying corpus callosum hypoconnectivity and brain metabolic patterns in the valproic acid rat model of autism spectrum disorder. J Neurochem. 2021;159(1):128. https://doi.org/10.1111/jnc.15444.CrossRefPubMed Uccelli NA, Codagnone MG, Traetta ME, Levanovich N, Rosato Siri MV, Urrutia L, Falasco G, Vázquez S, Pasquini JM, Reinés AG. Neurobiological substrates underlying corpus callosum hypoconnectivity and brain metabolic patterns in the valproic acid rat model of autism spectrum disorder. J Neurochem. 2021;159(1):128. https://​doi.​org/​10.​1111/​jnc.​15444.CrossRefPubMed
84.
go back to reference Radua J, Grau M, Van Den Heuvel OA, De Schotten MT, Stein DJ, Canales-Rodríguez EJ, Catani M, Mataix-Cols D. Multimodal voxel-based meta-analysis of white matter abnormalities in obsessive-compulsive disorder. Neuropsychopharmacology. 2014;39(7):1577. https://doi.org/10.1038/npp.2014.5.CrossRef Radua J, Grau M, Van Den Heuvel OA, De Schotten MT, Stein DJ, Canales-Rodríguez EJ, Catani M, Mataix-Cols D. Multimodal voxel-based meta-analysis of white matter abnormalities in obsessive-compulsive disorder. Neuropsychopharmacology. 2014;39(7):1577. https://​doi.​org/​10.​1038/​npp.​2014.​5.CrossRef
86.
go back to reference Courchesne E, Karns CM, Davis HR, Ziccardi R, Carper RA, Tigue ZD, Chisum HJ, Moses P, Pierce K, Lord C, Lincoln AJ, Pizzo S, Schreibman L, Haas RH, Akshoomoff NA, Courchesne RY. Unusual brain growth patterns in early life in patients with autistic disorder: an MRI study. Neurology. 2001;57(2):245. https://doi.org/10.1212/WNL.57.2.245.CrossRefPubMed Courchesne E, Karns CM, Davis HR, Ziccardi R, Carper RA, Tigue ZD, Chisum HJ, Moses P, Pierce K, Lord C, Lincoln AJ, Pizzo S, Schreibman L, Haas RH, Akshoomoff NA, Courchesne RY. Unusual brain growth patterns in early life in patients with autistic disorder: an MRI study. Neurology. 2001;57(2):245. https://​doi.​org/​10.​1212/​WNL.​57.​2.​245.CrossRefPubMed
94.
go back to reference Zhou C, Xu J, Ping L, Zhang F, Chen W, Shen Z, Jiang L, Xu X, Cheng Y. Cortical thickness and white matter integrity abnormalities in obsessive–compulsive disorder: a combined multimodal surface-based morphometry and tract-based spatial statistics study. Depress Anxiety. 2018;35(8):742. https://doi.org/10.1002/da.22758.CrossRefPubMed Zhou C, Xu J, Ping L, Zhang F, Chen W, Shen Z, Jiang L, Xu X, Cheng Y. Cortical thickness and white matter integrity abnormalities in obsessive–compulsive disorder: a combined multimodal surface-based morphometry and tract-based spatial statistics study. Depress Anxiety. 2018;35(8):742. https://​doi.​org/​10.​1002/​da.​22758.CrossRefPubMed
100.
go back to reference Merchán A, Mora S, Gago B, Rodriguez-Ortega E, Fernández-Teruel A, Puga JL, Sánchez-Santed F, Moreno M, Flores P. Excessive habit formation in schedule-induced polydipsia: Microstructural analysis of licking among rat strains and involvement of the orbitofrontal cortex. Genes Brain Behav. 2019. https://doi.org/10.1111/gbb.12489.CrossRefPubMed Merchán A, Mora S, Gago B, Rodriguez-Ortega E, Fernández-Teruel A, Puga JL, Sánchez-Santed F, Moreno M, Flores P. Excessive habit formation in schedule-induced polydipsia: Microstructural analysis of licking among rat strains and involvement of the orbitofrontal cortex. Genes Brain Behav. 2019. https://​doi.​org/​10.​1111/​gbb.​12489.CrossRefPubMed
102.
go back to reference Tapias-Espinosa C, Río-Álamos C, Sánchez-González A, Oliveras I, Sampedro-Viana D, del Mar Castillo-Ruiz M, Cañete T, Tobeña A, Fernández-Teruel A. Schizophrenia-like reduced sensorimotor gating in intact inbred and outbred rats is associated with decreased medial prefrontal cortex activity and volume. Neuropsychopharmacology. 2019;44(11):1975. https://doi.org/10.1038/s41386-019-0392-x.CrossRefPubMedPubMedCentral Tapias-Espinosa C, Río-Álamos C, Sánchez-González A, Oliveras I, Sampedro-Viana D, del Mar Castillo-Ruiz M, Cañete T, Tobeña A, Fernández-Teruel A. Schizophrenia-like reduced sensorimotor gating in intact inbred and outbred rats is associated with decreased medial prefrontal cortex activity and volume. Neuropsychopharmacology. 2019;44(11):1975. https://​doi.​org/​10.​1038/​s41386-019-0392-x.CrossRefPubMedPubMedCentral
106.
go back to reference Conti E, Retico A, Palumbo L, Spera G, Bosco P, Biagi L, Fiori S, Tosetti M, Cipriani P, Cioni G, Muratori F, Chilosi A, Calderoni S. Autism spectrum disorder and childhood apraxia of speech: Early language-related hallmarks across structural mri study. J Personal Med. 2020;10(4):275. https://doi.org/10.3390/jpm10040275.CrossRef Conti E, Retico A, Palumbo L, Spera G, Bosco P, Biagi L, Fiori S, Tosetti M, Cipriani P, Cioni G, Muratori F, Chilosi A, Calderoni S. Autism spectrum disorder and childhood apraxia of speech: Early language-related hallmarks across structural mri study. J Personal Med. 2020;10(4):275. https://​doi.​org/​10.​3390/​jpm10040275.CrossRef
111.
go back to reference Seo S, Beck A, Matthis C, Genauck A, Banaschewski T, Bokde ALW, Bromberg U, Büchel C, Quinlan EB, Flor H, Frouin V, Garavan H, Gowland P, Ittermann B, Martinot JL, Martinot MLP, Nees F, Orfanos DP, Poustka L, Hohmann S, Fröhner JH, Smolka MN, Walter H, Whelan R, Desrivières S, Heinz A, Schumann G, Obermayer K. Risk profiles for heavy drinking in adolescence: differential effects of gender. Addict Biol. 2019;24(4):787. https://doi.org/10.1111/adb.12636.CrossRefPubMed Seo S, Beck A, Matthis C, Genauck A, Banaschewski T, Bokde ALW, Bromberg U, Büchel C, Quinlan EB, Flor H, Frouin V, Garavan H, Gowland P, Ittermann B, Martinot JL, Martinot MLP, Nees F, Orfanos DP, Poustka L, Hohmann S, Fröhner JH, Smolka MN, Walter H, Whelan R, Desrivières S, Heinz A, Schumann G, Obermayer K. Risk profiles for heavy drinking in adolescence: differential effects of gender. Addict Biol. 2019;24(4):787. https://​doi.​org/​10.​1111/​adb.​12636.CrossRefPubMed
112.
113.
go back to reference Fineberg NA, Apergis-Schoute AM, Vaghi MM, Banca P, Gillan CM, Voon V, Chamberlain SR, Cinosi E, Reid J, Shahper S, Bullmore ET, Sahakian BJ, Robbins TW. Mapping compulsivity in the DSM-5 obsessive compulsive and related disorders: cognitive domains, neural circuitry, and treatment. Int J Neuropsychopharmacol. 2018;21(1):42. https://doi.org/10.1093/ijnp/pyx088.CrossRefPubMed Fineberg NA, Apergis-Schoute AM, Vaghi MM, Banca P, Gillan CM, Voon V, Chamberlain SR, Cinosi E, Reid J, Shahper S, Bullmore ET, Sahakian BJ, Robbins TW. Mapping compulsivity in the DSM-5 obsessive compulsive and related disorders: cognitive domains, neural circuitry, and treatment. Int J Neuropsychopharmacol. 2018;21(1):42. https://​doi.​org/​10.​1093/​ijnp/​pyx088.CrossRefPubMed
114.
go back to reference Whelan R, Conrod PJ, Poline JB, Lourdusamy A, Banaschewski T, Barker GJ, Bellgrove MA, Büchel C, Byrne M, Cummins TDR, Fauth-Bühler M, Flor H, Gallinat J, Heinz A, Ittermann B, Mann K, Martinot JL, Lalor EC, Lathrop M, Loth E, Nees F, Paus T, Rietschel M, Smolka MN, Spanagel R, Stephens DN, Struve M, Thyreau B, Robbins TW, Vollstaedt-Klein S, Schumann G, Garavan H. Adolescent impulsivity phenotypes characterized by distinct brain networks. Nat Neurosci. 2012;15(6):920. https://doi.org/10.1038/nn.3092.CrossRefPubMed Whelan R, Conrod PJ, Poline JB, Lourdusamy A, Banaschewski T, Barker GJ, Bellgrove MA, Büchel C, Byrne M, Cummins TDR, Fauth-Bühler M, Flor H, Gallinat J, Heinz A, Ittermann B, Mann K, Martinot JL, Lalor EC, Lathrop M, Loth E, Nees F, Paus T, Rietschel M, Smolka MN, Spanagel R, Stephens DN, Struve M, Thyreau B, Robbins TW, Vollstaedt-Klein S, Schumann G, Garavan H. Adolescent impulsivity phenotypes characterized by distinct brain networks. Nat Neurosci. 2012;15(6):920. https://​doi.​org/​10.​1038/​nn.​3092.CrossRefPubMed
122.
130.
142.
go back to reference Draganski B, Gaser C, Busch V, Schuierer G, Bogdahn U, May A. Neuroplasticity: changes in grey matter induced by training. Nature. 2004;427(6972):311.CrossRefPubMed Draganski B, Gaser C, Busch V, Schuierer G, Bogdahn U, May A. Neuroplasticity: changes in grey matter induced by training. Nature. 2004;427(6972):311.CrossRefPubMed
Metadata
Title
Mapping the neuroanatomical abnormalities in a phenotype of male compulsive rats
Authors
Elena Martín-González
Ángeles Prados-Pardo
Stephen J. Sawiak
Jeffrey W. Dalley
Daniel Padro
Pedro Ramos-Cabrer
Santiago Mora
Margarita Moreno-Montoya
Publication date
01-12-2023
Publisher
BioMed Central
Published in
Behavioral and Brain Functions / Issue 1/2023
Electronic ISSN: 1744-9081
DOI
https://doi.org/10.1186/s12993-023-00221-y

Other articles of this Issue 1/2023

Behavioral and Brain Functions 1/2023 Go to the issue