Topography and significance of the dopaminergic dysfunction in schizophrenia
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1 Topography and significance of the dopaminergic dysfunction in schizophrenia Anissa Abi-Dargham MD Professor of Psychiatry and Vice Chair for Research Department of Psychiatry Stony Brook University Professor Emerita of Psychiatry Special Lecturer Columbia University New York
2 Disclosures (last 36 months) Paid Editorial duties: NPP and Biological Psychiatry Member of the board of Scientific advisors to the NMH director (BSC), member of NPAS study section Research support: Pierre Fabre, Forest, Pfizer, Otsuka, CHDI Consultant: Roche, Otsuka, System 1 Biosciences, Serenikey Therapeutics, Lundbeck, FORUM Honoraria for lectures: Otsuka
3 OUTLINE 1- Schizophrenia as a global brain disease 2- The role of dopamine within this global pathology 3- Imaging dopamine 4- Findings in striatum 5- Findings in extrastriatal brain areas 6- Modeling dopamine dysfunction in mice 7- Synthesis and future directions
4 OUTLINE 1- Schizophrenia as a global brain disease 2- The role of dopamine within this global pathology 3- Imaging dopamine 4- Findings in striatum 5- Findings in extrastriatal brain areas 6- Modeling dopamine dysfunction in mice 7- Synthesis and future directions
5 Natural course of schizophrenia Premorbid Prodromal Onset/ deterioration Residual/ stable Healthy Worsening severity of signs and symptoms Gestation/birth Puberty Years After Lieberman et al
6 Symptom clusters involve all functional domains Perception: Psychosis Hallucinations Paranoia Thought disturbance Cognition: Cognitive deficits Working memory Executive function Social cognition Reward deficits Anhedonia Movement abnormalities: Stereotypies Catatonia Mood disturbances Schizophrenia is a GLOBAL brain disease
7 Structural (anatomical) MRI Relevant findings: morphometry in schizophrenia Ellison-Wright et al. AJP 2008
8 Prefrontal Cortex in Schizophrenia: abnormal microcircuitry Somal Size GAT-1 Immunoreactivity x Dendritic Spine Density Mediodorsal Axon Terminals Excitatory Terminal Inhibitory Terminal Modulatory Terminal GAD 67 /GAT-1 mrna GABA Aa2 D 1 receptors DA Axon Density White Matter Association Cortex Mediodorsal Thalamus Neuron Number DA Lewis DA, Lieberman JA. Neuron 2000
9 Functional MRI Auditory cortex is abnormal: hyperactive during silence Horga G, Schatz KC, Abi-Dargham A, Peterson BS,. J Neurosci 2014
10 Diffusion Tensor Imaging (DTI) MRI Structural connectivity in schizophrenia: abnormal frontotemporal and genu of corpus callosum connectivity Lener et al. Schizophr Bull 2015
11 Gadolinium-enhanced T1 CBV in schizophrenia is enhances in CA1 of hippocampus in schizophrenia and prodrome, predicts conversion Schobel et al. AGP 2009
12 OUTLINE 1- Schizophrenia as a global brain disease 2- The role of dopamine within this global pathology 3- Imaging dopamine 4- Findings in striatum 5- Findings in extrastriatal brain areas 6- Modeling dopamine dysfunction in mice 7- Synthesis and future directions
13 Dopaminergic Pathways mpfc OFC DLPFC MOTOR VTA SN Courtesy of Suzanne Haber
14 LST AST SMST DA Mesocortical Mesolimbic Nigrostriatal Nigrostriatal
15 Haber and Mc Farland, Ann N Y Acad Sci.1999, Kegeles et al, Archives of Gen Psychiatry, 2010 Howes et al, Archives of Gen Psychiatry 2009
16 Abi-Dargham et al, Biol Psychiatry cover, Jan 2017
17 Dopamine encodes reward prediction-error (rpe) Schultz et al., O Doherty et al., Daw et al., Glimcher et al.
18 Dopamine modulates the balance of Excitation/ inhibition in the prefrontal cortex GLU DA DA GLU GABA+ CR-/PV- GABA+ PV+ P GLU DA Adapted from D. Lewis
19 O Donnnell, SCZ bull, 2011
20 Dopamine is historically related to symptomatology and treatment Antipsychotic properties of chlorpromazine (Delay & Denicker, 1952) Dopamine turnover increased by antipsychotics (Carlsson & Lindqvist, 1963) Overstimulation of DA receptors in SCZ (Van Rossum, 1966) DA agonists produce psychosis (Angrist and Van kammen 1984, Lieberman 1987) All antipsychotics are D2 drugs, D2 potency dictates clinical dose (Seaman, Snyder ). This lead to numerous hypotheses: First hypothesis: mesolimbic DA excess Second hypothesis: subcortical excess and cortical deficit (Weinberger 1987, Davis,1990)
21 OUTLINE 1- Schizophrenia as a global brain disease 2- The role of dopamine within this global pathology 3- Imaging dopamine 4- Findings in striatum 5- Findings in extrastriatal brain areas 6- Modeling dopamine dysfunction in mice 7- Synthesis and future directions
22 Imaging the striatal dopaminergic synapse Presynaptic Tyrosine hydroxylase AADC [18F]f-DOPA: synthesis and presynaptic storage (activity of Aromatic L-amino acid decarboxylase AADC) (but also uptake in DA neurons, VMAT activity and uptake in vesicles, ph in vesicles, metabolism in cytoplasm ) VMAT VMAT2 radiotracers: [11C]DTBZ DAT MAO COMT D 2 receptor Dopamine levels DAT radiotracer: [123I]BCIT, [11C]PE2I D 2 receptor D2 receptor (but also affected by dopamine occupancy, internalization, affinity state ) Postsynaptic STR medium Spiny neuron
23 Baseline Imaging synaptic Dopamine Amphetamine Challenge D2 radiotracer Dopamine Alpha-methyl-para-tyrosine
24 D2/3 PET radiotracers [11C]raclopride [11C]Fallypride [11C]FLB457
25 FUNCTIONALSUBDIVISIONS OF STRIATUM LIMBIC ASSOCIATIVE SENSORIMOTOR Post CA Post PUT PRECOMMISSURAL (ANTERIOR) POSTCOMMISSURAL (POSTERIOR)
26 OUTLINE 1- Schizophrenia as a global brain disease 2- The role of dopamine within this global pathology 3- Imaging dopamine 4- Findings in striatum 5- Findings in extrastriatal brain areas 6- Modeling dopamine dysfunction in mice 7- Synthesis and future directions
27 STRIATAL dopamine alterations in schizophrenia Presynaptic DAT MAO VMAT Tyrosine hydroxylase AADC COMT D 2 receptor Dopamine synthesis Reith et al., 1994 Hietala et al., 1995, 1999 Lindstorm et al., 1999 Meyer-Lindenberg et al., 2002 McGowan et al., 2004 Nozaki S et al., 2009 Howes et al., 2009 Dopamine release - Amphetamine challenge - Laruelle et al., 1996 Breier et al., 1997 Abi-Dargham et al., AMPT - Abi-Dargham et al., 2000 Kegeles et al., 2010 D 2 receptors - Meta analyses - Weinberger & Laruelle, 2001 Howes et al., 2012 Postsynaptic STR medium Spiny neuron D 1 receptors Normal DAT and VMAT2: Normal
28 AMPT-induced increase in [11C]raclopride BP (% baseline) Intrasynaptic dopamine in STR subdivisions in SCZ Healthy controls (n = 18) Patients with schizophrenia (n = 18) VST AST SMST * VST predca predpu postca postpu * p < 0.05, Kegeles et al, Archives of Gen Psychiatry, 2010
29 Striatal Dopamine Release predicts Psychotic Symptoms Schizophrenia, n= 34 [ 123 I]IBZM displacement (% baseline) r P = 0.55 STRIATUM Change in Psychosis scores (PANSS)
30 Intrasynaptic baseline DA predicts psychosis treatment response Abi-Dargham et al, PNAS, 2002 e
31 DA synthesis predicts psychosis treatment response Demjaha et al, AJP, 2012
32 Striatal Dopamine Release predicts Psychotic Symptoms [ 123 I]IBZM displacement (% baseline) Schizophrenia, n= 34 SCZ DD, n=10 r P = 0.55 STRIATUM [ 11 C]raclopride BP ND in predca r S = 0.69 (r P = 0.62) ROSTRAL caudate Change in Psychosis scores (PANSS)
33 Negative Symptoms inversely related to Dopamine Levels in Ventral Striatum AMPT-induced increase in D 2 availability (%) PANSS negative symptom total Kegeles LS et al. Arch Gen Psychiatry 2010;67(3):
34 Striatal D2 stimulation predicts Psychotic Symptoms [ 123 I]IBZM displacement (% baseline) Schizophrenia, n= 34 SCZ DD, n=10 r P = 0.55 STRIATUM [ 11 C]raclopride BP ND in predca r S = 0.69 (r P = 0.62) ROSTRAL caudate Change in Psychosis scores (PANSS)
35 Frankle et al
36 Pre or Post synaptic: the striatal DA dysregulation in schizophrenia Slifstein and Abi-Dargham, 2018, Biol Psychiatry
37 Pre or Post synaptic: the striatal DA dysregulation in schizophrenia Slifstein and Abi-Dargham, 2018, Biol Psychiatry
38 Dopamine synthesis in the prodrome: [18F]f-DOPA increased in striatum Howes et al, Arch Gen Psych 2009 Howes et al, Molecular Psych 2011 Howes et al, Am J Psychiatry 2011
High D2 stimulation Psychosis. Low DA Negative symptoms. Relates to psychosis And its treatment response
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