Comorbid HIV infection and alcohol use disorders: Converging glutamatergic and dopaminergic mechanisms underlying neurocognitive dysfunction

Brain Research 1723 (2019) 146390

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Review

Comorbid HIV infection and alcohol use disorders: Converging glutamatergic and dopaminergic mechanisms underlying neurocognitive dysfunction Laura L. Giacometti, Jacqueline M. Barker

T

⁎

Department of Pharmacology and Physiology, Drexel University College of Medicine, United States

H I GH L IG H T S

and alcohol use disorder comorbidity increases risk for cognitive impairment. • HIV HIV infection and chronic alcohol dysregulate common targets. • Both projections are altered by both infection and alcohol use. • Corticostriatal • Common disruption of dopamine and glutamate signaling may drive impairments.

A R T I C LE I N FO

A B S T R A C T

Keywords: Alcohol use disorder Cognitive function HIV Glutamate Dopamine

Alcohol use disorders (AUDs) are highly comorbid with human immunodeficiency virus (HIV) infection, occurring at nearly twice the rate in HIV positive individuals as in the general population. Individuals with HIV who consume alcohol show worse long-term prognoses and may be at elevated risk for the development of HIVassociated neurocognitive disorders. The direction of this relationship is unclear, and likely multifactorial. Chronic alcohol exposure and HIV infection independently promote cognitive dysfunction and further may interact to exacerbate neurocognitive deficits through effects on common targets, including corticostriatal glutamate and dopamine neurotransmission. Additionally, drug and alcohol use is likely to reduce treatment adherence, potentially resulting in accelerated disease progression and subsequent neurocognitive impairment. The development of neurocognitive impairments may further reduce cognitive control over behavior, resulting in escalating alcohol use. This review will examine the complex relationship between HIV infection and alcohol use, highlighting impacts on dopamine and glutamate systems by which alcohol use and HIV act independently and in tandem to alter corticostriatal circuit structure and function to dysregulate cognitive function.

1. Introduction

Eggers et al., 2017; Paul, 2019; Rubin and Maki, 2019). Further, the precise cognitive domains impacted may be different following the introduction of combined antiretroviral treatment (cART) (Cysique et al., 2004; Heaton et al., 2011; Paul, 2019). As observed in patients with alcohol use disorders, only a subset of individuals with HIV develop neurocognitive impairments, and risk is impacted by a number of factors, potentially including comorbid substance use disorders. Alcohol use is highly prevalent in the HIV infected population, with the majority of people with HIV reporting alcohol use within the last year (Lefevre et al., 1995; Cook et al., 2001a; Conigliaro et al., 2004; Goulet et al., 2005; Braithwaite et al., 2007). Both heavy drinking and diagnosis of alcohol use disorders occur at nearly twice

Alcohol use disorders are chronic, relapsing conditions defined by impairments in control over behavior. The development of an alcohol use disorder is often accompanied by deficits in multiple cognitive domains, including working memory, decision making, and attention that not only negatively impact quality of life, but may also result in increased difficulty in terminating alcohol use (Tiffany, 1990; Field et al., 2010; Stavro et al., 2012; Koob and Volkow, 2016). Similar impairments in neurocognitive function are reported in individuals living with chronic HIV infection, including impaired motor and verbal learning, attention, and cognitive flexibility (Le Berre et al., 2014a;

⁎ Corresponding author at: Pharmacology and Physiology, College of Medicine, Drexel University, 245 N 15th Street, MS 488, Philadelphia, PA 19102, United States. E-mail address: [email protected] (J.M. Barker).

https://doi.org/10.1016/j.brainres.2019.146390 Received 10 June 2019; Received in revised form 2 August 2019; Accepted 13 August 2019 Available online 14 August 2019 0006-8993/ © 2019 Elsevier B.V. All rights reserved.

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2. Corticostriatal dysfunction following alcohol use or HIV infection

the rate of the general population in individuals with HIV (Galvan et al., 2002). Heavy alcohol use persists across the lifespan, in both younger and older adults with HIV (Ge et al., 2018). The effect of HIV infection on the development of problem drinking and AUDs is unclear. However, in a study evaluating drinking trajectories among HIV-infected women, a subset (8%) of women were shown to increase from nonheavy to heavy drinking over a 12-year follow-up period (Cook et al., 2013). Alcohol use has profound consequences in HIV-infected populations; even non-problematic alcohol use (< 5 drinks/day) can reduce life expectancy by 1 year, while hazardous use may reduce survival by over 6 years (Braithwaite et al., 2007). The increased prevalence of alcohol use among HIV-infected individuals is not surprising given that risk factors for HIV infection overlap in many ways with risk for alcohol use disorders, including impulsivity and other drug use (Jentsch and Taylor, 1999; Wojnar et al., 2009; Marquine et al., 2014). Due to this overlap in risk factors, it is difficult to establish a direct causal link between HIV infection and alcohol use. Further, alcohol use itself may increase high-risk behaviors including risky sexual activity (Berry and Johnson, 2018) and result in poor adherence to cART (Cook et al., 2001b). Many clinical and preclinical studies investigating the interface of addiction and HIV on cognitive function, both prior to cART and in the current era, focus on psychostimulant use (Nath et al., 2001; Rippeth et al., 2004; Nath, 2010; Meade et al., 2011, 2017; Paris et al., 2014; Wayman et al., 2015a; Soontornniyomkij et al., 2016; Javadi-Paydar et al., 2017; Bertrand et al., 2018). This research has implicated prefrontal cortex and striatal circuitry in substance use and HIV comorbidity. For example, cocaine interacts with HIV to exacerbate impairments in decision making and sensitivity to risk, and to mediate activation of the prefrontal cortex when making decisions (Meade et al., 2017). The more limited data that we have on alcohol use in HIV suggests that alcohol use contributes to cognitive deficits in HIV-infected populations. Chronic alcohol use and HIV act independently to alter neurocognitive function which may impair subsequent ability to reduce or discontinue alcohol use in HIV-infected individuals. A history of alcohol use is associated with exacerbation of HIV-associated cognitive deficits, including memory and executive functions, working memory, impulsivity, and spatial reasoning tasks (Farinpour et al., 2000; Martin et al., 2004a,b; Rothlind et al., 2005). However, the understanding of mechanisms by which alcohol use interacts with HIV to drive development of neurocognitive impairments remains limited. The precise nature of the relationship between HIV infection and alcohol use is unclear and may be correlational, unidirectional, or bidirectional and may involve biological, psychological, and social components. Both HIV infection and chronic alcohol use are independently associated with profound neurobiological impairments, including structural abnormalities and aberrant neurotransmission (Nath et al., 2000; Olive, 2009; Seo et al., 2011; Sjoerds et al., 2013; Burnett et al., 2014a; Le Berre et al., 2014b; Marquine et al., 2014; Festa et al., 2015; McGuier et al., 2015a; Ann et al., 2016; Ye et al., 2017; Gaskill et al., 2017). Of particular note, perturbation of the glutamate and dopamine systems within limbic corticostriatal circuits has been implicated in the etiology of substance use disorders and the development of cognitive impairments (Murphy et al., 1996; Kalivas, 2009; Olive, 2009; Floresco, 2013; Dauvermann et al., 2017). Individual differences in glutamatergic and dopaminergic system function predating drug use or infection have been identified, and may serve as risk factors for both HIV exposure, maintenance or escalation of drug use, and subsequent cognitive impairment. Further, repeated alcohol use alters both glutamate and dopamine system function in similar ways to chronic HIV infection, even with cART treatment. Thus, these systems may represent a target whereby HIV infection and chronic alcohol use interface to drive risk for exacerbated neurocognitive impairment (Fig. 1).

The prefrontal cortex (PFC) is often thought to be a key contributor to ‘executive’ function, acting as a regulator of behavior and a substrate underlying learning and memory (Arnsten and Goldman-Rakic, 1998; Arnsten, 2011; Kim and Lee, 2011). In both humans and nonhuman primates, the PFC can be roughly divided into distinct medial, dorsolateral, and orbitofrontal cortices (Van Eden and Uylings, 1985; Berendse et al., 1992; Schilman et al., 2008) defined in part by cytoarchitectural, anatomical, and neurochemical data. Functional distinction between these subregions in primates remains somewhat controversial and it is likely that PFC subregions contribute to multiple cognitive domains with some functional separation. For example, the medial PFC (mPFC) is a key regulator of behavioral inhibition and flexibility as well as action selection (Seamans et al., 2008a; Balleine and O’Doherty, 2010; Passingham and Wise, 2012). The orbitofrontal cortex (OFC) has been implicated in contingency tracking and credit assignment, enabling the OFC to regulate multiple forms of reward seeking behavior (Roberts, 2006; Rygula et al., 2010; Tsuchida et al., 2010; Noonan et al., 2012). The primate dorsolateral PFC (dlPFC) has historically been investigated for its well-established role in working memory (Goldman-Rakic, 1991; Arnsten et al., 2015). The anatomy of the rodent PFC differs substantially from that of the human and nonhuman primate (Seamans et al., 2008b; Laubach et al., 2018). The agranular mPFC, including the infralimbic and prelimbic cortices, and OFC are thought to be roughly homologous in rodent brain, but greater debate exists about homology in the rodent cortex to primate dlPFC (Seamans et al., 2008a; Alexander et al., 2019). Based on functional and behavioral studies, many have suggested that the dorsal anterior cingulate cortex of the rodent shares at least partial homology with human dlPFC (Seamans et al., 2008b). Chronic exposure to alcohol produces a host of neurobiological perturbations that may drive cognitive impairment (Koob et al., 1998; Allen et al., 2011; Kroener et al., 2012; Burnett et al., 2014b; TranthamDavidson et al., 2014; Griffin et al., 2015; Koob and Volkow, 2016). Independent of HIV, high levels of alcohol drinking are associated with cognitive impairments that increase as individuals age (Woods et al., 2016). In patients with alcohol use disorders, significant dysregulation of PFC anatomy and function have been reported, including cortical atrophy, white matter disruption, and reductions in glucose metabolism (Pfefferbaum et al., 1997, 2009; Harris et al., 2008; Stavro et al., 2012; John et al., 2014; Vanes et al., 2014; Koob and Volkow, 2016). Reductions in PFC volume in patients with alcohol use disorders has been associated with impaired cognitive flexibility, attention, and decision making (Chanraud et al., 2007; Le Berre et al., 2014a). Even in healthy individuals and heavy drinkers without alcohol use disorders, alcohol impairs planning and memory (Peterson et al., 1990; Christian et al., 1995). Cognitive impairment in nondependent individuals has been associated with daily drinking behavior (Parsons and Nixon, 1998). Despite these findings, data from clinical populations are difficult to interpret as risk for alcohol use disorders may be associated with a predisposition toward cognitive impairment and corticostriatal dysregulation and animal models can provide clarity on the causal nature of these relationships. While HIV does not infect neurons, it does infect CD4 + T cells, microglia/macrophages, and astrocytes (Cosenza et al., 2002; FischerSmith et al., 2001; Falangola et al., 1995; Petito et al., 1999; Churchill et al., 2009; Finzi et al., 1999; Jordan et al., 1991), resulting in substantial perturbations in corticostriatal structure and function. Even with cART, HIV-infected individuals still show alterations in PFC function and anatomy, including reductions in functional connectivity between PFC and subcortical targets (Ann et al., 2016) and alterations in white matter structure (Pomara et al., 2001), which is further exacerbated in HIV-patients with comorbid AUDs (Pfefferbaum et al., 2006). HIV-patients also show thinning of the PFC (du Plessis et al., 2

Brain Research 1723 (2019) 146390

L.L. Giacometti and J.M. Barker

Fig. 1. Common effects on corticostriatal circuits in HIV infection and alcohol use disorder. Chronic exposure to ethanol and HIV infection both act to impair key aspects of corticostriatal function including (A) prefrontal neurotransmission, (B) regulation of extracellular glutamate levels, and (C) dopamine signaling in the PFC and striatum. Both chronic ethanol exposure and HIV infection result in alterations in dendritic spine density and maturity, but in opposing directions. Both chronic ethanol exposure and HIV infection result in hyperglutamatergic states via downregulation of the glutamate transporter. Decreases in D2 receptor signaling have been observed in the PFC following both chronic ethanol exposure and HIV infection, while additional alterations in DAT levels and D2 receptor excitability have also been observed in the striatum following HIV infection. The precise factors underlying these effects are somewhat distinct may intersect to produce elevated risk for neurocognitive impairment in individuals with comorbid HIV infection and alcohol use disorder.

2016) and the orbitofrontal cortex (McGuier et al., 2015b), though these findings may be specific to the age of alcohol exposure (Jury et al., 2017). Ethanol exposure has also been shown to result in increases in dendritic arborization in the medial PFC (Holmes et al., 2012; Kim et al., 2015; Navarro and Mandyam, 2015; Holmes et al 2012; Kim et al., 2015). In contrast, in animal models of HIV infection, spine loss and reductions in dendritic branching were observed in the PFC that

2016), which is associated with impairments in cognitive function, as well as alterations in frontostriatal connectivity during risky decision making (Connolly et al., 2014). Both chronic alcohol exposure and HIV infection alter synaptic architecture of PFC pyramidal neurons in rodents. Ethanol exposure has been shown to result in greater spine densities, particularly mushroomtype spines, and spine maturity in the medial PFC (Klenowski et al., 3

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were associated with deficits in behavioral flexibility (Festa et al., 2015). In another animal model of HIV infection, PFC neurons were found to be hyperexcitable, consistent with observed alterations in calcium channel expression in pyramidal neurons (Wayman et al., 2015a, 2016).

hyperglutamatergic state, which is most likely in part mediated by reductions in glutamate transport via downregulation of glutamate transporters and loss of presynaptic metabotropic glutamate receptors (Melendez et al., 2005; Olive, 2009; Griffin et al., 2013; Meinhardt et al., 2013). This increase in extracellular glutamate likely impairs normal learning and memory by disrupting normal synaptic communication (Corlett et al., 2011; Holmes et al., 2013). Elevations in glutamate levels may lead to overlearning of events or generalized failure in ‘signal-to-noise’ processing, thus impairing neurocognitive function (Parsons et al., 2007). Both in human alcoholics and animals models of alcohol dependence, reductions in EAAT2/GLT-1 have been observed which may reduce clearance of extrasynaptic glutamate (Melendez et al., 2005; Sari et al., 2013; Rao et al., 2015). In tissue from HIV positive patients, a nonhuman primate model of HIV infection, and a mouse model of HIV-1 infection, astrocyte expression of EAAT2/GLT1 was also downregulated, potentially similarly driving an increase in extrasynaptic glutamate levels which may impair normal neuronal activity and signaling (Xing et al., 2009; Melendez et al., 2016). Consistent with this finding, in vitro work has shown attenuated astrocytic EAAT expression and function, potentially mediated by viral proteins themselves or by indirect effects on inflammation (Fine et al., 1996; Patton et al., 2000).

3. Acquired alterations in corticostriatal glutamate neurotransmission following alcohol use or HIV infection The principal neurons within the PFC are glutamatergic pyramidal neurons which project to a variety of subcortical targets, notably including striatal subregions (McGeorge and Faull, 1989; Sesack et al., 1989; Schilman et al., 2008). Glutamate signaling occurs via both ionotropic and metabotropic receptors, which are expressed on both neuronal and glial populations. It is generally thought that fast acting signaling occurs at postsynaptic ionotropic receptors, while postsynaptic metabotropic glutamate receptors can modulate neuronal firing. Presynaptically, Gi-coupled metabotropic glutamate receptors act as autoreceptors, regulating neurotransmitter release, while the role of presynaptic ionotropic glutamate receptors is less clear. Synaptic glutamate levels are regulated by neuronal and vesicular glutamate transporters (EAATs and vGLUTs) (Arriza et al., 1997; Furuta et al., 1997; Li et al., 2013). Extrasynaptic glutamate is cleared by astrocytic glutamate transporters (GLT1 and GLAST) (Anderson and Swanson, 2000) and released by astrocytes via system xc- (Bridges et al., 2012). The topographically organized glutamatergic corticostriatal projections are highly conserved from rodent to primate and are known to be critical in the regulation of behavior and learning and memory (McGeorge and Faull, 1989; Berendse et al., 1992; Haber, 2008; Balleine and O’Doherty, 2010; Haber and Knutson, 2010; Barker et al., 2015). The striatum consists of dorsal and ventral subregions, with the dorsal striatum divided into the caudate and putamen, and the ventral subregion consisting of the nucleus accumbens core and shell in addition to the less well-characterized ventrolateral striatum. Glutamatergic projections from the ventral subregions of the medial PFC in rodents – especially the infralimbic PFC and ventral portions of the prelimbic PFC – innervate the nucleus accumbens shell and to a lesser extent the core (Room et al., 1985; Sesack et al., 1989; Vertes, 2004; Alexander et al., 2019). The more dorsal aspects of the prelimbic PFC and the anterior cingulate send glutamatergic projections to the nucleus accumbens core and the dorsomedial striatum. Projections from the OFC similarly innervate the dorsomedial striatum as well as the ventrolateral striatum and aspects of the accumbens core. The dorsolateral portions of the striatum are not extensively innervated by the mPFC, OFC, or dlPFC, but rather receive extensive glutamatergic projections from sensorimotor cortices. As such, the dorsolateral striatum is thought to participate less in the emotional, cognitive, evaluative, or associative aspects assigned to other striatal subregions, but rather it contributes to motor planning and behaviors elicited in the absence of cognitive control (Haber et al., 2000; Featherstone and McDonald, 2004; Yin and Knowlton, 2006). Evidence of polymorphisms within the glutamate system that contribute directly to the development of alcohol use disorders is sparse. Single nucleotide polymorphisms within genes encoding subunits of both NMDA and kainate receptors have been implicated in alcohol use disorders (Kranzler et al., 2009, 2014), but the precise mechanisms by which these mutations are associated with alcohol use disorders remains unclear. Two polymorphisms in particular - in the GRIN2c gene encoding a subunit of the NMDA receptor and the GRIK1 gene encoding a subunit of the kainate receptor – are associated with alcohol cue reactivity in the PFC and craving for alcohol (Bach et al., 2015). Beyond specific gene associations, a genome wide study assessing genetic variation associated with response to alcohol identified glutamate systemassociated genes, including GRIN2b and GRIK1 (Joslyn et al., 2010). Extracellular glutamate levels are dysregulated by both ethanol exposure and HIV infection. Chronic alcohol use results in a

4. Acquired alterations in corticostriatal dopamine neurotransmission following alcohol use or HIV infection Both prefrontal and striatal subregions are extensively innervated by midbrain dopaminergic projections. Prefrontal pyramidal neurons have reciprocal connections with dopaminergic cells within the ventral tegmental area (VTA) such that PFC neurons synapse directly onto VTA neurons that project to the PFC, but not to VTA projections to the accumbens (Carr and Sesack, 2000). Within the PFC, both the D1-like receptors (D1 and D5) and the D2-like receptors (D2-4) are expressed. Both dopamine receptor families are G protein coupled. Dopamine D1 receptors signal via Gαs, and agonism results in subsequent production of cyclic AMP and PKA. In contrast, dopamine D2 receptors are Gαi/o coupled, thus their activation inhibits adenylyl cyclase activity. In addition to expression on glutamatergic pyramidal neurons, D2 receptors are expressed on prefrontal GABAergic interneurons where their agonism may further inhibit downstream activity in corticostriatal glutamatergic projection neurons (Tseng and O’Donnell, 2007). Beyond canonical G-protein mediated signaling, dopamine receptors also act through beta-arrestin pathways, which have also been implicated in dopamine effects on cognitive function (Urs et al., 2017). Dopaminergic synapses have been shown to be in close apposition to glutamatergic projections within the striatum and there is substantial evidence that these projections to the striatum can modulate not only medium spiny neuron activity, but also neurotransmitter release from neighboring terminals. There is some debate about whether D1 and D2 containing neurons within the PFC represent separate populations, as some suggest that PFC neurons express mRNA for both D1 and D2 receptors (Vincent et al., 1995). Others suggest that D1- vs D2- containing PFC cells are not only distinct populations, but that they may be functionally and anatomically distinct (Gee et al., 2012; Land et al., 2014). Dopamine acts in the PFC to modulate neural activity and thus regulate cognitive function. Appropriate regulation of prefrontal DA is critical in a number of behaviors requiring cognitive control including goal-directed actions (Hitchcott et al., 2007; Barker et al., 2013), set shifting (Floresco, 2013), and decision-making (Groman et al., 2011). A variety of theories have been posited suggesting the precise mechanisms by which dopamine exerts this effect. It has long been suggested that the ability of dopamine to modulate cognitive function is through an ‘inverted U’ curve, where both high and low levels of dopamine signaling result in impaired cognition, potentially by dysregulating the signal-to-noise ratio of prefrontal projections (Berridge and Arnsten, 2013). This perspective has been expanded by further understanding of 4

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impairment in HIV positive populations. In both animals and humans, abnormalities in cognitive control have also been associated with gene polymorphisms in catechol-o-methyl transferase (COMT), which encodes the enzyme primarily responsible for DA degradation in the PFC (Malloy-Diniz et al., 2013; Soeiro-De-Souza et al., 2013; Ziegler et al., 2014). Though findings are inconsistent, COMT polymorphisms have also been implicated in the development of alcohol use disorders (Hendershot et al., 2012; Schellekens et al., 2012, 2013; Guillot et al., 2014). As with the Taq1a polymorphism, COMT polymorphisms may interact with additional factors to facilitate cognitive impairment in HIV positive individuals. In particular, the val/val polymorphism, associated with higher enzyme activity and thus lower prefrontal dopamine concentrations than the met/met polymorphism, has been associated with greater risk for cognitive impairments in HIV positive men and women (Sundermann et al., 2015; Saloner et al., 2019) (but see (Levine et al., 2012)). What is unclear from genetic studies is whether the genetic differences that predispose individuals to alcohol use disorders are, in parallel, predisposing individuals to neurocognitive impairment or if these deficits occur consecutively. For example, while dopamine D2 receptor polymorphisms are associated with drug use as well as cognitive performance in HIV infected individuals, the direction of the relationship between HIV infection and D2 genotype was opposite in substance dependent versus nondependent populations, suggesting that the directionality and relationship of these genotypic differences in risk are complex and modulated by experience (Jacobs et al., 2013). In animal models of alcohol use disorders, chronic alcohol exposure is associated with deficits in cognitive flexibility and working memory. These deficits may be mediated, at least in part, by ethanol-induced alterations in PFC DA signaling and function (Trantham-Davidson et al., 2015). While acute ethanol consumption results in elevated DA levels in both the PFC and subcortical targets such as the accumbens, chronic ethanol exposure appears to result in a hypodopaminergic state within the PFC (Volkow et al., 2002). These alterations in DA signaling and PFC function can produce deficits in behavioral flexibility and cognitive control over actions that may promote addictive behavior and make achieving and maintaining abstinence difficult (Hogarth et al., 2013; Barker et al., 2015). These effects are closely simulated by chronic intermittent ethanol (CIE) exposure, a mouse model of alcohol dependence (Hodge et al., 2006; Becker, 2012; Lopez et al., 2014; Barker et al., 2016). Specifically, this model alters signaling via D2 receptors on both pyramidal neurons and fast spiking interneurons in the medial PFC, which may lead to a loss of coordination of prefrontal networks and subsequent impairments in cognitive function (Trantham-Davidson et al., 2014). The dopamine system also appears to be particularly vulnerable to perturbation by HIV infection, which may, in part, underlie the development of neurocognitive deficits in HIV-associated neurocognitive disorders (HAND) (Nath et al., 2000; Purohit et al., 2011, 2013). Individuals with HIV associated dementia have been shown to have lower dopamine transporter expression in both the ventral striatum and the putamen (Wang et al., 2004), which is likely associated with dysregulation of dopamine levels. In addition to alterations in dopamine concentration (Wang et al., 2004; Chang et al., 2008), PFC-specific alterations in dopamine receptor expression are associated with HIV infection (Gelman et al., 2012). Exposure of dopaminergic neurons to HIV viral proteins directly can be neurotoxic (Nath et al., 2000; Ferris et al., 2008). The striatal DA system is also dysregulated in rodent models of HIV infection. Striatal injections of the HIV-1 viral protein Tat result in a reduction of TH positive cells in rats (Zauli et al., 2000). Further, in Tat-expressing transgenic mice, striatal dopamine D2 receptor-containing medium spiny neurons populations are vulnerable to disruption, showing hyperexcitability and dendritic damage (Schier et al., 2017). While in the cART era it appears likely that a preponderance of HIV-associated impairments in corticostriatal structure and function are not directly initiated by gross loss of neurons, these

the contribution of dopamine receptor subtypes in cognition. It has been suggested that dopamine signaling through D1-like vs D2-like receptors can enable toggling between stable maintenance of information when D1 signaling predominates, but flexible and more readily updated states when D2 signaling predominates (Durstewitz and Seamans, 2008). Further, development of novel genetic and pharmacological tools has revealed that dopamine signaling at receptors within a class in the PFC may have differing effects on cognitive function (Floresco, 2013), potentially consistent with differential expression patterns on prefrontal neurons and/or with differential receptor coupling. The GABAergic projection neurons of the striatum, in contrast, are segregated into distinct D1 vs D2 receptor-containing populations with minimal overlap in expression (Robertson et al., 1992; Le Moine and Bloch, 1995). Both D1 and D2 containing medium spiny neurons are present throughout the ventral striatal subregions, including the nucleus accumbens core and shell, as well as the dorsal striatal subregions (Levey et al., 1993). As with prefrontal glutamatergic inputs, dopaminergic projections to the striatum are topographically organized. In both rodents and primates, the ventral striatum is innervated by the VTA, with the shell receiving projections from the medial VTA and the core from central portions of the VTA (Haber et al., 2000; Haber, 2008). In rodents, both the lateral portion of the VTA and the substantia nigra project to the dorsomedial striatum, while in primates this associative aspect of the striatum primarily receives dopaminergic inputs from the substantia nigra. The dorsolateral/sensorimotor striatum is innervated by nigral dopaminergic neurons. Unlike the PFC, striatal subregions are not extensively interconnected, and communicate via parallel processing loops. Striatal dopamine signaling has been heavily implicated in multiple forms of learning and memory, but one of the most well-studied phenomena has been dopaminergic encoding of prediction error (Schultz, 1997, 2015; Berridge, 2007; Oyama et al., 2010; Asaad and Eskandar, 2011). Learning and memory necessarily involves experiencing and encoding of outcomes. Early work investigating dopamine signaling within the striatum suggests that dopamine release is associated with reward delivery when reward is unexpected, but that phasic dopamine signaling is attenuated or absent when reward delivery is ‘predicted’ (Schultz et al., 1997; Oyama et al., 2010; Schultz, 2015). Similarly, when a reward is expected, but omitted, dopamine levels are reduced. This bidirectional encoding of outcome information in relationship to expectations is thought to function as a teaching signal and is critical for many forms of new learning as well as for updating behavior when expectations or contingencies are changed. While a long history of both candidate-gene based and unbiased screens have not identified clear single gene contributors to substance use disorders, some genetic differences in the dopamine system may impact the risk for development of alcohol seeking behaviors. A substantial literature has investigated the relationship between the Taq1a polymorphism – a polymorphism in the gene encoding the D2 dopamine receptor (DRD2/ANKK1) associated with reduced D2 binding in carriers of the minor (A1) allele – with the development of alcohol use disorders (Hoenicka et al., 2009; Schellekens et al., 2012; Villalba et al., 2015; Klaus et al., 2019; Tunbridge et al., 2019). Behavioral and cognitive impairments associated with alterations in D2 signaling in individuals with the Taq1A polymorphism are not restricted to elevated risk for alcohol use disorders, and it has been suggested that the alterations in dopamine D2 receptor binding in individuals with the polymorphism may be associated general alterations in cognition (Fagundo et al., 2014; Verdejo-Garcia et al., 2015). This mutation in the D2 gene has been further shown to mediate cognitive impairment in HIV infected individuals who use alcohol, suggesting that this genetic difference may predispose risk for the development of alcohol use disorders and, further, subsequent risk for HIV-associated neurocognitive dysfunction (Villalba et al., 2015). The same study also identified dopamine D4 receptor polymorphisms as risk factors for cognitive 5

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dysregulations in dopamine signaling could impair cognitive function in a variety of ways, potentially by impairing novel memory formation, disrupting synaptic stability and function, or inducing compensatory effects in receptor expression.

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5. Integrating HIV and alcohol research for a mechanistic understanding of cognitive impairment Comorbid HIV infection and alcohol use disorder are associated with increased risk for the development of neurocognitive impairment. Human research into the neurobiological substrates and mechanisms underlying neurocognitive impairment in HIV infection and chronic alcohol use is necessarily lacking a clear demonstration of causality. Beyond these challenges, the relationship between alcohol use and infection appears to be multidirectional, further complicating our understanding of the factors underlying enhanced risk. Genetic differences in both glutamate and dopamine systems appear to place individuals at risk for the development of HIV associated neurocognitive impairments as well as alcohol use disorders, but comorbid drug use may interact with genetics to moderate genetic risk. It is further difficult to dissociate neurobiological changes that may be compensatory and, in fact, protective from the development of cognitive deficits. In addition to reducing medication adherence, ethanol exposure may also facilitate HIVinduced neurocognitive consequences by reducing bioavailability of antiretroviral drugs (Shibata et al., 2003), though this is not always observed (McCance-Katz et al., 2013). In the opposing direction, individuals with HIV exhibit increased sensitivity to alcohol, requiring fewer drinks to experience intoxication and maintaining higher blood ethanol concentrations (McCance-Katz et al., 2012; McGinnis et al., 2016). A precise elucidation of the peripheral and central mechanisms underlying exacerbated risk for neurocognitive impairment will require translational and preclinical research. Historically, animal models have contributed substantially to the understanding of the neurobiology of both HIV and alcohol use disorders, but these models are particularly challenging in studying progressive HIV infection. Nonhuman primate models have the advantage of high homology between prefrontal and striatal anatomy and function with humans (Seamans et al., 2008b; Burnett et al., 2014b), and nonhuman primates can be infected with simian immunodeficiency virus (SIV) or simian-human immunodeficiency virus (SHIV) (Evans and Silvestri, 2013). Transgenic rodent models expressing viral proteins have enabled assessment of the impact of these proteins on both cognition and behavioral flexibility as well as neuronal structure and function (Festa et al., 2015; Wayman et al., 2015b, 2016). To investigate the progressive effects of HIV infection, mouse models with humanized immune systems have been developed that become infected with HIV (Gorantla et al., 2010; Li et al., 2017). Through the development of novel animal models and the combination of these varied animal models with established models of ethanol self-administration and ethanol dependence, we can move toward a clear understanding of the causal mechanisms underlying increased risk for cognitive impairment in patients with comorbid alcohol use disorders and HIV. This careful elucidation of the impact of infection and chronic alcohol use on glutamatergic and dopaminergic systems may lead toward novel treatment strategies for this population to reduce alcohol use, promote cART adherence, and reduce risk for neurocognitive impairment. Acknowledgment This work was supported by US NIH/NIAAA Grant R00AA024499 and US NIH/NIDA Grant R03DA047917. References Alexander, L., Clarke, H.F., Roberts, A.C., 2019. A focus on the functions of area 25. Brain Sci. 9, 129.

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