Synaptic Connectivity in Medium Spiny Neurons of the Nucleus Accumbens: A Sex-Dependent Mechanism Underlying Apathy in the HIV-1 Transgenic Rat

Kristen A. McLaurin1, Anna K. Cook1, Hailong Li1, Alexis F. League1, Charles F. Mactutus1, Rosemarie M. Booze1
1Department of Psychology, Program in Behavioral Neuroscience, University of South Carolina, Columbia, SC, United States

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Abbondanzo, 2014, HIV-1 transgenic rats display alterations in immunophenotype and cellular responses associated with aging, PLoS One, 9, e105256, 10.1371/journal.pone.0105256

Alexander, 1994, Basal ganglia-thalamocortical circuits: their role in control of movements, J. Clin. Neurophysiol., 11, 420, 10.1097/00004691-199407000-00004

Alexander, 1990, Functional architecture of basal ganglia circuits: neural substrates of parallel processing, Trends Neurosci., 13, 266, 10.1016/0166-2236(90)90107-l

Alexander, 1986, Parallel organization of functionally segregated circuits linking basal ganglia and cortex, Annu. Rev. Neurosci., 9, 357, 10.1146/annurev.ne.09.030186.002041

Arellano, 2007, Ultrastructure of dendritic spines: correlation between synaptic and spine morphologies, Front. Neurosci., 1, 131, 10.3389/neuro.01.1.1.010.2007

Bertrand, 2018, HIV-1 proteins dysregulate motivational processes and dopamine circuitry, Sci. Rep., 8, 7869, 10.1038/s41598-018-25109-0

Blundo, 2015, Dopamine agonists can improve pure apathy associated with lesions of the prefrontal-basal ganglia functional system, Neurol. Sci., 36, 1197, 10.1007/s10072-014-2061-5

Bonelli, 2007, Frontal-subcortical circuitry and behavior, Dialogues Clin. Neurosci., 9, 141, 10.31887/DCNS.2007.9.2/rbonelli

Brancato, 2017, Sub-chronic variable stress induces sex-specific effects on glutamatergic synapses in the nucleus accumbens, Neuroscience, 350, 180, 10.1016/j.neuroscience.2017.03.014

Bredt, 2003, AMPA receptor trafficking at excitatory synapses, Neuron, 40, 361, 10.1016/s0896-6273(03)00640-8

Brown, 2012, Dopamine pathway loss in nucleus accumbens and ventral tegmental area predicts apathetic behavior in MPTP-lesioned monkeys, Exp. Neurol., 236, 190, 10.1016/j.expneurol.2012.04.025

Cao, 2016, Neonatal masculinization blocks increased excitatory synaptic input in female rat nucleus accumbens core, Endocrinology, 157, 3181, 10.1210/en.2016-1160

Cao, 2018, Sex differences in medium spiny neuron excitability and glutamateric synaptic input: heterogeneity across striatal regions and evidence for estradiol-dependent sexual differentiation, Front. Endocrinol., 9, 173, 10.3389/fendo.2018.00173

HIV among people aged 50 and older2018

Cheng, 1997, Differential spine loss and regrowth of striatal neurons following multiple forms of deafferentation: a golgi study, Exp. Neurol., 147, 287, 10.1006/exnr.1997.6618

Chong, 2016, The role of dopamine in the pathophysiology and treatment of apathy, Prog. Brain Res., 229, 389, 10.1016/bs.pbr.2016.05.007

Cline, 2001, Dendritic arbor development and synaptogenesis, Curr. Opin. Neurobiol., 11, 118, 10.1016/s0959-4388(00)00182-3

Cole, 2007, Relationship between psychiatric status and frontal-subcortical systems in HIV-infected individuals, J. Int. Neuropsychol. Soc., 13, 549, 10.1017/s135561770707066x

Critchley, 2005, Neural mechanisms of autonomic, affective and cognitive integration, J. Comp. Neurol., 493, 154, 10.1002/cne.20749

Crofton, 1989, Evaluation of sensory system function using reflex modification of the startle response, J. Am. Coll. Toxicol., 8, 199, 10.3109/10915818909009105

Denenberg, 1984, Some statistical and experimental considerations in the use of the analysis-of-variance procedure, Am. J. Physiol., 246, R403, 10.1152/ajpregu.1984.246.4.r403

Forlano, 2010, Quantitative analysis of pre- and postsynaptic sex differences in the nucleus accumbens, J. Comp. Neurol., 518, 1330, 10.1002/cne.22279

Freire, 1978, Effects of dark rearing on dendritic spines in layer IV of the mouse visual cortex. a quantitative electron microscopical study, J. Anat., 126, 193

Freund, 1984, Tyrosine hydroxylase-immunoreactive boutons in synaptic contact with identified striatonigral neurons, with particular reference to dendritic spines, Neuroscience, 13, 1189, 10.1016/0306-4522(84)90294-x

Gelman, 2012, Prefrontal dopaminergic and enkephalinergic synaptic accomodiation in HIV-associated neurocognitive disorders and encephalitis, J. Neuroimmune Pharmacol., 7, 686, 10.1007/s11481-012-9345-4

Groves, 1983, A theory of the functional organization of the neostriatum and the neostriatal control of voluntary movement, Brain Res. Rev., 286, 109, 10.1016/0165-0173(83)90011-5

Gupta, 2010, HIV-Tat elicits microglial glutamate release: role of NAPDH oxidase and the cysteine-glutamate antiporter, Neurosci. Lett., 485, 233, 10.1016/j.neulet.2010.09.019

Haas, 2006, AMPA receptors regulate experience-dependent dendritic arbor growth in vivo, Proc. Natl. Acad. Sci. U S A, 103, 12127, 10.1073/pnas.0602670103

Harris, 1994, Dendritic spines: cellular specializations imparting both stability and flexibility to synaptic function, Annu. Rev. Neurosci., 17, 341, 10.1146/annurev.ne.17.030194.002013

Harris, 1988, Dendritic spines of rat cerebellar purkinje cells: serial electron microscopy with reference to their biophysical characteristics, J. Neurosci., 8, 4455, 10.1523/jneurosci.08-12-04455.1988

Harris, 1989, Dendritic spines of CA1 pyramidal cells in the rat hippocampus: serial electron microscopy with reference to their biophysical characteristics, J. Neurosci., 9, 2982, 10.1523/jneurosci.09-08-02982.1989

Hering, 2001, Dendritic spines: structure, dynamics and regulation, Nat. Rev. Neurosci., 2, 880, 10.1038/35104061

Hestad, 2012, Sex differences in neuropsychological performance as an effect of human immunodeficiency virus infection: a pilot study in zambia, africa, J. Nerv. Ment. Dis., 200, 336, 10.1097/nmd.0b013e31824cc225

Hodes, 2015, Sex differences in nucleus accumbens transcriptome profiles associated with susceptibility versus resilience to subchronic variable stress, J. Neurosci., 35, 16362, 10.1523/jneurosci.1392-15.2015

Ison, 1984, Reflex modification as an objective test for sensory processing following toxicant exposure, Neurobehav. Toxicol. Teratol., 6, 437

Javadi-Paydar, 2017, HIV-1 and cocaine disrupt dopamine reuptake and medium spiny neurons in female rat striatum, PLoS One, 12, e0188404, 10.1371/journal.pone.0188404

Jones, 1969, Morphological variation in the dendritic spines of the neocortex, J. Cell Sci., 5, 509, 10.1242/jcs.5.2.509

Kamat, 2013, Implications of apathy and depression for everyday functionining in HIV/AIDS in brazil, J. Affect. Disord., 150, 1069, 10.1016/j.jad.2012.11.040

Kamat, 2016, Apathy is associated with lower mental and physical quality of life in persons infected with HIV, Psychol. Health Med., 21, 890, 10.1080/13548506.2015.1131998

Kamat, 2012, Implications of apathy for everyday functioning outcomes in persons living with HIV infection, Arch. Clin. Neuropsychol., 27, 520, 10.1093/arclin/acs055

Kemp, 1971, The structure of the caudate nucleus of the cat: light and electron microscopy, Philos. Trans. R. Soc. B Biol. Sci., 262, 383, 10.1098/rstb.1971.0102

Kim, 2008, Human immunodeficiency virus protein tat induces synapse loss via a reversible process that is distinct from cell death, J. Neurosci., 28, 12604, 10.1523/jneurosci.2958-08.2008

Kohno, 2010, Successful treatment of post-stroke apathy by the dopamine receptor agonist ropinirole, J. Clin. Neurosci., 17, 804, 10.1016/j.jocn.2009.09.043

Koos, 2011, Glutamatergic signaling by midbrain dopaminergic neurons: recent insights from optogenetic, molecular and behavioral studies, Curr. Opin. Neurobiol., 21, 393, 10.1016/j.conb.2011.05.010

Kumar, 2009, Human immunodeficiency virus type 1 in the central nervous system leads to decreased dopamine in different regions of postmortem human brains, J. Neurovirol., 15, 257, 10.1080/13550280902973952

Kumar, 2011, Human immunodeficiency virus infection in the CNS and decreased dopamine availability: relationship with neuropsychological performance, J. Neurovirol., 17, 26, 10.1007/s13365-010-0003-4

Lai, 2013, Structural plasticity of dendritic spines: the underlying mechanisms and its dysregulation in brain disorders, Biochim. Biophys. Acta, 1832, 2257, 10.1016/j.bbadis.2013.08.012

Lee, 2014, Imaging dopaminergic dysfunction as a surrogate marker of neuropathology in a small-animals model of HIV, Mol. Imaging, 13, 7290.2014.00031, 10.2310/7290.2014.00031

Levy, 2006, Apathy and the functional anatomy of the prefrontal cortex-basal ganglia circuits, Cereb. Cortex, 16, 916, 10.1093/cercor/bhj043

Lynch, 2005, Decreased motivation following cocaine self-administration under extended access conditions: effects of sex and ovarian hormones, Neuropsychopharmacology, 30, 927, 10.1038/sj.npp.1300656

Maki, 2009, HIV, cognition and women, Neuropsychol. Rev., 19, 204, 10.1007/s11065-009-9093-2

Maki, 2018, Differences in cognitive function between women and men with HIV, J. Acquir. Immune Defic. Syndr., 79, 101, 10.1097/QAI.0000000000001764

Maki, 2015, Cognitive function in women with HIV: findings from the women’s interagency HIV study, Neurology, 84, 231, 10.1212/wnl.0000000000001151

Mancuso, 2012, Methods of dendritic spine detection: from golgi to high-resolution optical imaging, Neuroscience, 251, 129, 10.1016/j.neuroscience.2012.04.010

Marquine, 2014, “Frontal systems” behaviors in comorbid human immunodeficiency virus infection and methamphetamine dependency, Psychiatry Res., 215, 208, 10.1016/j.psychres.2013.11.004

McLaurin, , Evolution of the HIV-1 transgenic rat: utility in assessing the progression of HIV-1-associated neurocognitive disorders, J. Neurovirol., 24, 229, 10.1007/s13365-017-0544-x

McLaurin, , Unraveling individual differences in the HIV-1 transgenic rat: therapeutic efficacy of methylphenidate, Sci. Rep., 8, 136, 10.1038/s41598-017-18300-2

McLaurin, 2016, Progression of temporal processing deficits in the HIV-1 transgenic rat, Sci. Rep., 6, 32831, 10.1038/srep32831

McLaurin, 2017, Sex matters: robust sex differences in signal detection in the HIV-1 transgenic rat, Front. Behav. Neurosci., 11, 212, 10.3389/fnbeh.2017.00212

Melendez, 2016, Decreased glial and synaptic glutamate uptake in the striatum of HIV-1 gp120 transgenic mice, J. Neurovirol., 22, 358, 10.1007/s13365-015-0403-6

Moran, , Time and time again: temporal processing demands implicate perceptual and gating deficits in the HIV-1 transgenic rat, J. Neuroimmune Pharmacol., 8, 988, 10.1007/s11481-013-9472-6

Moran, , Neurobehavioral alterations in HIV-1 transgenic rats: evidence for dopaminergic dysfunction, Exp. Neurol., 239, 139, 10.1016/j.expneurol.2012.10.008

Moran, 2014, Modeling deficits in attention, inhibition and flexibility in HAND, J. Neuroimmune Pharmacol., 9, 508, 10.1007/s11481-014-9539-z

Ostlund, 2014, Phasic mesolimbic dopamine signaling encodes the facilitation of incentive motivation produced by repeated cocaine exposure, Neuropsychopharmacology, 39, 2441, 10.1038/npp.2014.96

Padala, 2018, Methylphenidate for apathy in community-dwelling older veterans with mild Alzheimer’s disease: a double-blind, randomized, placebo-controlled trial, Am. J. Psychiatry, 175, 159, 10.1176/appi.ajp.2017.17030316

Panos, 2014, The impact of neurobehavioral features on medication adherence in HIV: evidence from longitudinal models, AIDS Care, 26, 79, 10.1080/09540121.2013.802275

Patton, 2000, Gp120-induced alterations of human astrocyte function: Na+/H+ exchange, K+ conductance and glutamate flux, Am. J. Physiol. Cell Physiol., 279, C700, 10.1152/ajpcell.2000.279.3.c700

Paxinos, 2014, The Rat Brain in Stereotaxic Coordinates.

Peng, 2010, The HIV-1 transgenic rat as a model for HIV-1 infected individuals on HAART, J. Neuroimmunol., 218, 94, 10.1016/j.jneuroim.2009.09.014

Peters, 1970, The small pyramidal neuron of the rat cerebral cortex. the perikaryon, dendrites and spines, Am. J. Anat., 127, 321, 10.1002/aja.1001270402

Pierce, 2007, Locomotor behavior, Curr. Protoc. Neurosci., 8, 8.1, 10.1002/0471142301.ns0801s40

Rajan, 1998, Glutamate receptor activity is required for normal development of tectal cell dendrites in vivo, J. Neurosci., 18, 7836, 10.1523/jneurosci.18-19-07836.1998

Ramôa, 2013, Estradiol as a mechanism for sex differences in the development of an addicted phenotype following extended access cocaine self-administration, Neuropsychopharmacology, 38, 1698, 10.1038/npp.2013.68

Reid, 2001, An HIV-1 transgenic rat that develops HIV-related pathology and immunologic dysfunction, Proc. Natl. Acad. Sci. U S A, 98, 9271, 10.1073/pnas.161290298

Richardson, 1996, Progressive ratio schedules in drug self-administration studies in rats: a method to evaluate reinforcing efficacy, J. Neurosci. Methods, 66, 1, 10.1016/0165-0270(95)00153-0

Roberts, 1989, The estrous cycle affects cocaine self-administration on a progressive ratio schedule in rats, Psychopharmacology, 98, 408, 10.1007/bf00451696

Rodriguez, 2008, Automated three-dimensional detection and shape classification of dendritic spines from fluorescence microscopy images, PLoS One, 3, e1997, 10.1371/journal.pone.0001997

Romley, 2014, Early HIV treatment led to life expectancy gains valued at $80 billion for people infected in 1996–2009, Health Aff., 33, 370, 10.1377/hlthaff.2013.0623

Roscoe, 2014, HIV-1 transgenic female rat: synaptodendritic alterations of medium spiny neurons in the nucleus accumbens, J. Neuroimmune. Pharmacol., 9, 642, 10.1007/s11481-014-9555-z

Rosenmund, 1996, Definition of the readily releasable pool of vesicles at hippocampal synapses, Neuron, 16, 1197, 10.1016/s0896-6273(00)80146-4

Rowson, 2016, Neuroinflammation and behavior in HIV-1 transgenic rats exposed to chronic adolescent stress, Front. Psychiatry, 7, 102, 10.3389/fpsyt.2016.00102

Royal, 2016, Associations between cognition, gender and monocyte activation among HIV infected individuals in nigeria, PLoS One, 11, e0147182, 10.1371/journal.pone.0147182

Schikorski, 1999, Quantitative fine-structural analysis of olfactory cortical synapses, Proc. Natl. Acad. Sci. U S A, 96, 4107, 10.1073/pnas.96.7.4107

Schikorski, 2001, Morphological correlates of functionally defined synaptic vesicle populations, Nat. Neurosci., 4, 391, 10.1038/86042

Seabold, 2010, DiOLISTIC labeling of neurons from rodent and non-human primate brain slices, J. Vis. Exp., 41, 2081, 10.3791/2081

Selemon, 1985, Longitudinal topography and interdigitation of corticostriatal projections in the rhesus monkey, J. Neurosci., 5, 776, 10.1523/jneurosci.05-03-00776.1985

Shapiro, 2013, Apathy correlates with cognitive performance, functional disability and HIV RNA plasma levels in HIV-positive individuals, J. Clin. Exp. Neuropsychol., 35, 934, 10.1080/13803395.2013.838941

Shen, 2009, Altered dendritic spine plasticity in cocaine-withdrawn rats, J. Neurosci., 29, 2876, 10.1523/jneurosci.5638-08.2009

Sholl, 1953, Dendritic organization in the neurons of the visual and motor cortices of the cat, J. Anat., 87, 387

Sinharay, 2017, Cross-sectional and longitudinal small animal PET shows pre and post-synaptic striatal dopaminergic deficits in an animal model of HIV, Nucl. Med. Biol., 55, 27, 10.1016/j.nucmedbio.2017.08.004

Smit, 2015, Future challenges for clinical care of an ageing population infected with HIV: a modelling study, Lancet Infect. Dis., 15, 810, 10.1016/s1473-3099(15)00056-0

Spiga, 2014, The “addicted” spine, Front. Neuroanat., 8, 110, 10.3389/fnana.2014.00110

Stevens, 2015, Creatine protects against mitochondrial dysfunction associated with HIV-1 tat-induced neuronal injury, Curr. HIV Res., 12, 378, 10.2174/1570162x13666150121101544

Teeraananchai, 2017, Life expectancy of HIV-positive people after starting combination antiretroviral therapy: a meta-analysis, HIV Med., 18, 256, 10.1111/hiv.12421

Thobois, 2013, Parkinsonian apathy response to dopaminergic stimulation of D2/D3 receptors with piribedil, Brain, 136, 1568, 10.1093/brain/awt067

Tian, 2015, Neuroimaging analysis of the dopamine basis for apathetic behaviors in an MPTP-lesioned primate model, PLoS One, 10, e0132064, 10.1371/journal.pone.0132064

AIDS by the numbers2016

Vigorito, 2015, The HIV-1 transgenic rat model of neuroHIV, Brain Behav. Immun., 48, 336, 10.1016/j.bbi.2015.02.020

Vigorito, 2007, Spatial learning and memory in HIV-1 transgenic rats, J. Neuroimmune Pharmacol., 2, 319, 10.1007/s11481-007-9078-y

Wang, 2003, Reduced expression of glutamate transporter EAAT2 and impaired glutamate transport in human primary astrocytes exposed to HIV-1 or gp120, Virology, 312, 60, 10.1016/s0042-6822(03)00181-8

Wears, 2002, Advanced statistics: statistical methods for analyzing cluster and cluster-randomized data, Acad Emerg. Med., 9, 330, 10.1197/aemj.9.4.330

Wecker, 1985, Reflex modification as a test for sensory function, Neurobehav. Toxicol. Teratol., 7, 733

Wilson, 2017, Valid statistical approaches for analyzing sholl data: mixed effects versus simple linear models, J. Neurosci. Methods, 279, 33, 10.1016/j.jneumeth.2017.01.003

Wissman, 2011, Sex differences and effects of cocaine on excitatory synapses in the nucleus accumbens, Neurophamacology, 61, 217, 10.1016/j.neuropharm.2011.04.002

Yao, 2008, Dopaminergic signaling in dendritic spines, Biochem. Pharmacol., 75, 2055, 10.1016/j.bcp.2008.01.018

Yuste, 2010, Dendritic Spines., 10.7551/mitpress/9780262013505.001.0001

Zahm, 1992, An electron microscopic morphometric comparison of tyrosine hydroxylase immunoreactive innervation in the neostriatum and the nucleus accumbens core and shell, Brain Res., 575, 341, 10.1016/0006-8993(92)90102-f

Zhou, 2017, HIV-1 glycoprotein 120 enhancement of N-Methyl-D-Aspartate NMDA receptor-mediated excitatory postsynaptic currents: implications for HIV-1-associated neural injury, J. Neuroimmune. Pharmacol., 12, 314, 10.1007/s11481-016-9719-0

Zhu, 2016, HIV-1 transgenic rats display an increase in [3H] dopamine uptake in the prefrontal cortex and striatum, J. Neurovirol., 22, 282, 10.1007/s13365-015-0391-6