INTPSY-10930; No of Pages 7 International Journal of Psychophysiology xxx (2015) xxx–xxx

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Neuropharmacology of altered brain oscillations in schizophrenia Michael Koch a,⁎, Christina Schmiedt-Fehr b, Birgit Mathes b a b

Brain Research Institute, Dept. of Neuropharmacology, University of Bremen, Hochschulring 18, 28359 Bremen, Germany Institute of Psychology and Cognition Research, University of Bremen, Grazerstr. 4, 28359 Bremen, Germany

a r t i c l e

i n f o

Available online xxxx Keywords: Drugs EEG Neuropsychiatric diseases Psychosis Synchronization

a b s t r a c t Impairments in spatial and temporal integration of brain network activity are a core feature of schizophrenia. Neural network oscillatory activity is considered to be fundamentally important in coordinating neural activity throughout the brain. Hence, exploration of brain oscillations has become an indispensible tool to study the neural basis of mental illnesses. However, most of the studies in schizophrenia include medicated patients. This implicates the question to what extent are changes in the electrophysiological parameters genuine illness effects, genuine drug effects or a mixture of both. We here provide a short overview of the neuropharmacology of brain oscillations with respect to schizophrenia. The core assumption of the so-called “pharmaco-EEG” approach is that drug effects on mental and cognitive functions are reflected in changes in quantitative EEG parameters. Hence, clinical efficacy of drugs might be predicted on the basis of the neuropharmacology of electrophysiological measures, such as brain oscillations. Vice versa, knowledge of drug effects on brain oscillations can be of essence in understanding schizophrenia. However, the current literature lacks systematic findings, because of at least two problems. First, the pharmacology of most antipsychotic drugs is complex including interactions with several transmitter receptors. Second, the neuropathology of schizophrenia still has no pathognomonic signature. Even though it is presently not possible to clearly dissociate drug- and illness effects in neural oscillations, this review emphasizes future studies to foster the understanding of this relationship in schizophrenia and other neuropsychiatric diseases. © 2015 Elsevier B.V. All rights reserved.

1. Introduction Schizophrenia is a severe psychiatric disorder affecting a wide range of cognitive, emotional, perceptual and motor functions. Since the etiopathogenesis probably involves diverse multiple “hits”, such as pre- or perinatal as well as pubertal noxious events, in addition to genetic predispositions (Rehn and Rees, 2005), the symptoms of the disease are quite heterogeneous (Tandon et al., 2009; Insel, 2010). Likewise, the underlying neuropathology is complex and earlier attempts to attribute symptoms to dysfunctions within specific transmitter systems (e.g. Carlsson, 2006) have largely been abandoned and replaced by more global constructs of brain dysfunctions (Pocklington et al., 2014). Longitudinal studies in schizophrenia suggest a history of cognitive impairment in premorbid phases of the illness, observable as early as the first grade in school, with further deterioration seen across school years (Nuechterlein et al., 2014). Epidemiological approaches indicate both cognitive impairments and developmental lags in these patients

⁎ Corresponding author. Tel.: +49 421 21862970. E-mail address: [email protected] (M. Koch).

with schizophrenia during childhood, well before the illness is fully manifest (Keefe, 2014). With the transition of the prodromal state into psychosis substantial cognitive deficits (Bora et al., 2014), regional specific losses in gray and white matter (Wood et al., 2011; Pantelis et al., 2005) and neurochemical alterations (Cropley et al., 2013) become evident. Cognitive decline and structural loss of brain tissue remains apparent over the course of the illness which may last several decades (Mathes et al., 2005; Wood et al., 2002; Velakoulis et al., 2001). Oscillatory brain activity, which is a fundamental process of information processing that is closely linked to perception, cognition and mood control in the brain, has been found to be altered in schizophrenia (Basar et al., 2013; Basar and Güntekin, 2013; Basar, 2013; Haenschel and Linden, 2011; Uhlhaas and Singer, 2010; Whittington et al., 2011). Investigating the pathophysiology of schizophrenia is complicated by the fact that medication also alters brain oscillations. Nearly all studies investigating changes in the oscillatory activity of schizophrenia have been conducted with patients taking antipsychotic drugs. Studies with unmedicated patients normally focus on the onset of schizophrenia (Gallinat et al., 2000). Self-administered recreational drug use (for example nicotine or cannabis) is also hard to control in patient studies. Antipsychotic treatment improves clinical symptoms, however, evaluation of first- and second-generation antipsychotics suggest that, despite

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Please cite this article as: Koch, M., et al., Neuropharmacology of altered brain oscillations in schizophrenia, Int. J. Psychophysiol. (2015), http:// dx.doi.org/10.1016/j.ijpsycho.2015.02.014

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slight to modest improvement in cognitive function for all treatments, no differences among medications are evident (Nuechterlein et al., 2014). In this short review, we focus on the neuropharmacological aspects of altered brain oscillations in schizophrenia. We address following questions: 1. Are different transmitter systems of specific relevance for brain oscillations in different frequency bands? 2. To what extent does oscillatory brain activity of unmedicated patients differ from that of medicated patients? 3. How does the type of medication affect oscillations in different frequency bands? 2. Effects of neurotransmitters on brain oscillations Earlier concepts of the pathophysiology of schizophrenia focussed on particular transmitters of the brain, such as dopamine and glutamate (Carlsson, 1995; Tamminga, 1998), whereas more recently, a more integrative way of thinking emerged, where the emphasis was put on interactions between different transmitter systems (Carlsson, 2006; Carlsson et al., 2001; Meyer-Lindenberg, 2010; Gonzalez-Maeso and Sealfon, 2009; Haenschel and Linden, 2011). We here review the current literature on alterations of brain oscillations related to different transmitter systems, drug treatment (Javitt et al., 2008) and their possible interactions. 2.1. Glutamate and GABA Glutamate and GABA are the prototypical excitatory and inhibitory neurotransmitters, respectively, in the brain. Their mutual interaction can be regarded as the neurophysiological basis of oscillations (particularly in short-range, high-frequency oscillations); interconnecting networks of neurons, as symbolized in Fig. 1. Ample evidence indicates that dysfunction of both glutamate and GABA are implicated in the pathophysiology of schizophrenia (Morrison and Pilowsky, 2007; Lewis et al., 2005; Coyle, 2004; Haenschel and Linden, 2011). More specifically, reduced activity of glutamate at the ionotropic NMDA receptors, e.g. by the noncompetitive receptor antagonists ketamine or phencyclidine has been shown to induce schizophrenia-like symptoms in humans and is considered an important animal model of the disease (Jentsch and Roth, 1999; Olney et al., 1999; Gainetdinov et al., 2001). A reduced number of GABAergic cortical interneurons containing the calciumbinding protein parvalbumin is evident in the brains of schizophrenia patients (Costa et al., 2004; Blum and Mann, 2002; Lewis, 2000). This, together with altered NMDA receptor function may be the basis of altered gamma band activity in the disease (Whittington, 2008).

With respect to brain oscillations, ketamine has been shown to reduce spontaneous and stimulus-evoked theta activity and to modulate gamma oscillations in the mouse hippocampus (Lazarewicz et al., 2009). Acute ketamine also increases gamma oscillations in the cortex of rats (Pinault, 2008), whereas chronic ketamine reduces gamma activity (Kocsis et al., 2013). In healthy humans, ketamine concurrently leads to increasing gamma oscillations and decreasing delta oscillations in an auditory paired-click paradigm (Hong et al., 2010). In an animal model of schizophrenia, the loss of GABAergic parvalbumin-containing neurons in the rat prefrontal cortex impairs cognitive performance and reduces gamma oscillations (Lodge et al., 2009). Selectively reducing parvalbumin GABAergic cortical interneurons by optogenetic techniques also reduced gamma activity in mice (Sohal et al., 2009). Interestingly, a recent study in mice showed that diazepam, which increases the effect of GABA at GABAA receptors via positive allosteric modulation slows down oscillatory activity in all frequency bands in the cortex (Scheffzük et al., 2013). By the same token, ethanol, which has GABA agonistic properties, reduces synchronization in all frequency bands in rodents and in humans (Ehlers et al., 2012). These findings on cortical glutamate and GABA are difficult to reconcile. Since NMDA receptors are abundant on GABAergic interneurons, one would expect that blocking these glutamate receptors by antagonists such as ketamine reduces the activity of these neurons which might have similar effects than the loss of GABAergic neurons. Also, it is unclear why GABA agonists such as the benzodiazepine diazepam have similar effects than the deletion of GABAergic neurons. It might be that drugs such as benzodiazepines shift the activity from some frequency bands to others so that there appears to be a reduction of activity in one band and an increase in another one (Whittington et al., 2000). It has to be noted that different brain regions are differentially affected in schizophrenia and that there are also regional differences in the action of drugs such as ketamine (Olney et al., 1989, 1999). It was suggested that reduced GABAergic inhibition by NMDA antagonists directly enhances beta 2 oscillations (20–29 Hz) and affects gamma rhythms in the cortex (Roopun et al., 2008). A recent paper showed that glutamate levels in the cortex specifically correlate with evoked gamma-band response in a cognitive context (Lally et al., 2014). Interestingly, altered gamma and delta-band activity probably related to GABA and NMDA receptor dysfunction is also observed in patients with bipolar disorder (Brealy et al., 2014; Özerdem et al., 2008).

2.2. Acetylcholine Acetylcholine (ACh) is used as transmitter in – roughly – two projection systems: Basal forebrain projections from the medial septum and

Fig. 1. Simplified schema illustrating the interaction between excitatory (glutamatergic/green) and inhibitory (GABAergic/red) networks generating oscillatory output activity (filled and empty circles symbolize active and silent neurons, respectively).

Please cite this article as: Koch, M., et al., Neuropharmacology of altered brain oscillations in schizophrenia, Int. J. Psychophysiol. (2015), http:// dx.doi.org/10.1016/j.ijpsycho.2015.02.014

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the basal nucleus to the hippocampus, amygdala and the cortex, and the projections from the pedunculopontine (PPN) and laterodorsal tegmental nuclei to the thalamus and brainstem. Both systems are involved in cognitive processes and attention (Deco and Thiele, 2011). The immense importance of cortical and hippocampal ACh for cognitive functions such as learning and memory is reflected in the neuropathology and symptoms of Alzheimer's disease which is characterized by cognitive decline due to the loss of cholinergic forebrain neurons (Everitt and Robbins, 1997; Davies and Maloney, 1976; Singh et al., 2013). ACh acts on ionotropic receptors composed of five subunits (nicotinic receptors) and on a family of metabotropic receptors (muscarinic receptors). Despite little neuropathological evidence for a cholinergic deficit, an involvement of ACh in schizophrenia has been suggested already some years ago, mainly suggesting sensitized cholinergic cortical input related to dysfunctional muscarinic ACh receptors (Sarter et al., 2005). Animal experiments have shown that lesions of the basal forebrain cholinergic system impair event-related oscillations in all frequency bands and phase-synchronization in their cortico-limbic target areas (Sanchez-Alavez et al., 2014). Likewise, the ascending cholinergic projections from the PPN are involved in the regulation of cortical gamma oscillations during slow-wave sleep (Mena-Segovia et al., 2008). Recently, a strong case has been made on the involvement of the nicotinic ACh receptor in negative and cognitive symptoms of schizophrenia (Freedman, 2014). Genetic studies have shown that a polymorphism in the promoter of the gene encoding the α7-subunit of the nicotinic ACh receptor (CHRNA7) is associated with schizophrenia, leading to reduced levels of α7-subunit receptors (Bakanidze et al., 2013). A reduced nicotinic ACh signaling might explain why schizophrenia patients often are heavy tobacco smokers and that nicotinic receptor agonists have strongly been recommended as a treatment option for cognitive symptoms in schizophrenia (Olincy and Stevens, 2007). In fact, nicotine has been shown to increase the P300 amplitude in schizophrenia patients (Mobascher et al., 2012) and the α7-receptor partial agonist DMXB-A improved cognitive and physiological measures in patients (Tregellas et al., 2011). Interestingly, a recent animal study in non-human primates showed that the cognitive and electrophysiological enhancing effects of α7-receptor ACh signaling – at least in the dorsolateral prefrontal cortex – involve increased glutamatergic activity at NMDA receptors (Yang et al., 2013). 2.3. Dopamine Dopamine plays an essential role in memory, reward, executive functions and motor control (Robbins, 2000). In its modern form the dopamine hypothesis of schizophrenia claims that there is too much dopamine in the ventral striatum and to little dopamine in the frontal cortex (Koch, 2007; Abi-Dargham, 2004). In the rat hippocampus dopamine exerts a frequency-dependent input selection gating low frequency (theta) input to CA1 pyramidal neurons from the entorhinal cortex without affecting input from the Schaffer collaterals (Ito and Schuman, 2008). In Parkinson's disease, where there is markedly reduced dopaminergic input to the striatum, an increase of power in lower (13–20 Hz) and upper (20–35 Hz) beta frequency bands in the basal ganglia was found, probably due to increased beta activity of the cortex (Brittain and Brown, 2014). Blockade of dopamine D2 receptors by the classical neuroleptic drug haloperidol has been shown to increase slow alpha and beta activity without affecting delta or theta activity. This finding is concomittant with clinical improvement (Mucci et al., 2006; Knott, 2000). This is consistent with findings of increased beta band activity in patients with Parkinson's disease, which is due to reduced striatal dopamine (Hammond et al., 2007). Recent approaches have tried to investigate direct relations between specific polymorphisms, gamma oscillations and the dopaminergic system (Demiralp et al., 2007). This line of investigation indicates that

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an increase of the acoustic evoked gamma response to targets and non-targets is related to a dopamine D4 receptor (DRD4) polymorphism, which leads to the expression of a subsensitive variant of the receptor. Since DRD4 is probably functioning as release-regulating autoreceptor, this polymorphism leads to increased release of dopamine. Likewise, the genotype variation of the dopamine transporter (DAT1) which reduces DAT expression and, hence, leads to an increased level of extracellular dopamine specifically enhanced evoked gamma responses to target stimuli. Thus, the study of Demiralp and colleagues may be related to a dysfunctional dopamine system in schizophrenia (Seeman et al., 2006). 2.4. Serotonin Psychedelic drugs, such as mescaline, LSD and psilocybin (psilocin) are agonists or partial agonists at serotonin (5-hydroxytryptamine or 5-HT) 2A receptors and have been used as models for certain psychotic symptoms and altered states of consciousness in schizophrenia (Helmle et al., 1992). A recent study using psilocybin in healthy humans revealed a strong reduction of oscillatory power in the default-mode network, a reduction in spontaneous oscillatory activity between 1–50 Hz in posterior association cortices and between 8–100 Hz in frontal areas (Muthukumaraswamy et al., 2013). Even though no changes by the psychedelic state were found during a visual-motor task, this study indicates highly disturbed global network activity induced by a drug that mainly acts as an agonist on 5-HT2A receptors. Given the broad distribution of serotonergic synapses throughout the cortex and hippocampus, a widespread modulation of corticolimbic oscillatory activity and the related cognitive functions can be expected. Indeed, studies in rodents have shown a prominent modulatory role of the hippocampal theta rhythm (5–10 Hz) by serotonin, probably in the context of memory (Vertes and Kocsis, 1997; Vertes, 1990) and more recently it has been shown that activation of the 5-HT2C receptor suppresses theta in the hippocampus (Sörman et al., 2011). 5-HT receptors of different subtypes are found in several strategic nodes – e.g. on pyramidal cells and GABAergic interneurons – in cortical micronetworks, especially in the prefrontal cortex. Evidence suggests that activation of 5-HT receptors reduces gamma activity (Puig and Gulledge, 2011). However, it is very likely that “pure” effects of serotonin are rare, but rather that the rhythmic activity in the cortex is modulated by several transmitters, e.g. by serotonin and by dopamine (Wang and WongLin, 2013). Moreover, since 5-HT2 receptors are functionally coupled to metabotropic glutamate receptors (Gonzalez-Maeso and Sealfon, 2009; Wischhof and Koch, 2012) the investigation of this coupling is probably a promising target for further EEG research. 3. Event-related brain oscillations in schizophrenia 3.1. Implications from event-related oscillations Brain oscillatory activity in schizophrenia, as measured by EEG, indicates abnormal temporal integration and interregional connectivity of brain networks during neurcognitive function (Lee et al., 2003; Ford et al., 2007; Basar and Güntekin, 2008; Uhlhaas and Singer, 2010). Since gamma synchrony is suggested as a mechanism for binding and the integration of cognitive brain functions (Basar et al., 1980, 2001; Kaiser et al., 2004; Sannita et al., 2001; Singer and Gray, 1995; Tallon-Baudry et al., 1997; Varela et al., 2001), most studies investigating brain oscillations in schizophrenia focused on disturbances in the gamma frequency range (Basar-Eroglu et al., 2007; Haenschel et al., 2007; Haig et al., 2000; Herrmann and Demiralp, 2005; Spencer et al., 2008). It is suggested that integrative brain functions are obtained through multiple oscillatory processes in different frequency bands and are a necessity for temporal coherence of perceptions and

Please cite this article as: Koch, M., et al., Neuropharmacology of altered brain oscillations in schizophrenia, Int. J. Psychophysiol. (2015), http:// dx.doi.org/10.1016/j.ijpsycho.2015.02.014

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actions (Basar, 2006; Basar et al., 2001). On the neurophysiological level, low frequencies have been linked to the transfer of information over long distances, while high frequencies are more important for local communication between neurons (von Stein and Sarnthein, 2000), although the importance of long-range communication for higher frequencies has also been discussed (Siegel et al., 2012). Accordingly, current thinking emphasizes that investigating oscillations across all frequencies is very useful to understand the neural basis of schizophrenia and the evidence that oscillatory activity in low frequencies is also disturbed accumulated in recent years (Schmiedt et al., 2005; Fehr et al., 2003; Ramos-Loyo et al., 2009; Ergen et al., 2008). It has been emphasized that different markers of oscillatory brain activity should be considered to more precisely describe the assumed changes in temporal integration and interregional connectivity of brain networks in schizophrenia (Basar-Eroglu et al., 2009; Basar and Güntekin, 2008). Changes in temporal integration or temporal coordination of oscillatory brain activity are indicated by reduced brain activity that is precisely time-locked to perceptual, cognitive or behavioral events, although the amplitude in single trials does not necessarily differ between patients and healthy persons (Ergen et al., 2008). These studies also underline that earlier assumptions about a general lack of activation in patients are not sufficient (Basar-Eroglu et al., 2007; Hong et al., 2012). Disturbances in the temporal integration of brain activity also becomes apparent by investigating cross-frequency coupling, a measure testing for temporal integration between frequency ranges (Kirihara et al., 2012). Investigation of large-scale networks is important to demonstrate that in schizophrenia spatial specificity of oscillatory networks is reduced (Basar-Eroglu et al., 2008, 2013). Thus, many studies report deviations in a wide range of frequencies in schizophrenia, but additional information is needed to tackle the inconsistencies about the topographical distribution, the specificity of disturbances within different frequency bands or the occurrence of an over- or undershoot of the activation. Important factors are also task demands. For example, spontaneous theta activity may be increased, while task-related activity may be diminished already for low task demands (Schmiedt et al., 2005; Bates et al., 2009; Missionnier et al., 2012; Boutros et al., 2008). The relation between different oscillatory brain states may become of increasing importance in the understanding the consequences of disrupted spatio-temporal neural integration in schizophrenia (Hanslmayr et al., 2013). 3.2. Antipsychotic drugs and event-related oscillations in schizophrenia As mentioned above, it is often reported that in schizophrenia gamma band activity is disrupted (Lee et al., 2003). Positive symptoms such as hallucinations are reported to be associated with increased, while negative symptoms are more related to reduced gamma activity (Herrmann and Demiralp, 2005). EEG studies directly comparing medicated and unmedicated patients with schizophrenia are rare, but most of those studies also point towards disease-related abnormalities in the gamma band. Minzenberg and co-workers investigated changes in gamma oscillations at frontal sites during a response inhibition task and showed that compared to healthy controls patients with schizophrenia showed impaired task performance and deficient gamma power irrespective of medication (Minzenberg et al., 2010). In unmedicated patients frontal gamma oscillations elicited by target detection were found to be reduced compared to healthy controls at frontal sites (Gallinat et al., 2000, 2004) A more recent study found reduced gamma and increased beta activity in a face-perception task in first-episode unmedicated patients compared to controls (Sun et al., 2013). Spencer et al. (2008) reported reduced phase locking of visualevoked gamma oscillations at occipital electrodes in schizophrenia using a visual oddball paradigm. They suggest that the deficit in gamma activity might be a general phenomenon in schizophrenia as it

is observed in unmedicated, first-episode patients with schizophrenia and in chronic, medicated patients with schizophrenia. Interestingly, in a parallel performed auditory oddball paradigm the evoked gamma did not differ from healthy subjects (Spencer et al., 2008). The pharmacological profile of clinically active atypical antipsychotic compounds is complex (Miyamoto et al., 2005). For example, the classical atypical neuroleptic drug clozapine has the following dissociation constants as an antagonist (n.b.: the lower the dissociation constant the higher the affinity of a ligand for a receptor): dopamine D2 receptor: 180, dopamine D4 receptor: 10, 5-HT2A receptor: 1.6, muscarinic 1 acetylcholine receptor: 8, histamine 1 receptor: 3, noradrenergic alpha 1 receptor: 9. The new-generation antipsychotic drug aripiprazole is a partial agonist at dopamine D2 receptors, a full agonist at 5-HT1A receptors and an antagonist at 5-HT2A receptors (Koch, 2007). Hence, the effect of these antipsychotic drugs on oscillatory activity is likely to be complex. Interestingly, clozapine and olanzapine were reported to reduce global alpha and beta activity (Galderisi et al., 1996; Hubl et al., 2001; Hyun et al., 2011), but have little effect on gamma oscillations. Animal studies have shown that clozapine reduced basal cortical gamma (30–80 Hz) power in rats but had no effect on ketamineinduced gamma hyperactivity (Jones et al., 2012). 4. Implications and future prospects: Combined methodological approaches Unfortunately, the number of double-blind studies including healthy controls as well as patients before and after medication at comparable stages of the illness (e.g., within the first episode) and with a comparable symptomatic profile are limited, especially considering brain oscillations. The requirements on studies like this are very high and they will probably remain rare. However, the importance of those studies is obvious considering that brain oscillations are a marker of neural spatio-temporal integration, that is for a core deficit in schizophrenia (Andreasen, 2000). It is, therefore, of profound interest to validate hypotheses on the neurochemical basis of brain oscillations in schizophrenia, and combine such studies with evidence from elaborate neuropharmacological studies in healthy individuals, as well as with appropriate animal studies. In a recent review, Haenschel and Linden (Haenschel and Linden, 2011) focussed on the relationship between genes, neurotransmitters, neural systems, as reflected for example in brain oscillations, and the behavioral output. Basar and Güntekin (Basar and Güntekin, 2008) further emphasized that effects of study sample characteristics, such as gender and age, needs to be taken into account. Further, selecting specific behavioral measures meeting the qualities of an endophenotype of schizophrenia (Gottesman and Gould, 2003), and characterizing those in healthy humans and patients using brain oscillations as well as in animal models may provide a useful experimental approach (Light et al., 2012; Swerdlow et al., 2006, 2008). One such behavioral measure might be prepulse-inhibition (PPI) of startle which is known to be impaired in schizophrenia, although it does not specifically correlate with particular symptoms (Swerdlow et al., 2008; Fendt and Koch, 2013). Concurrent PPI and EEG studies have shown that prominent evoked potentials such as P50, P1, N1, P2 and P300 are reduced for acoustic stimuli when preceded by a prepulse (Ford and Roth, 1999; Ford et al., 1999; Schall et al., 1997). Within the first 500 ms poststimulus onset PPI is reflected in the oscillatory theta (4–7 Hz), alpha (8–13 Hz) and gamma (28–48 Hz) response (Kedzior et al., 2006, 2007). An important aspect that should also find consideration in systematic studies of pharmacological effects is the lack of specificity in psychotropic treatments ranging from lithium and antipsychotics to serotonin reuptake inhibitors and acetylcholinesterase inhibitors. These therapeutics show efficacy in a wide spectrum of psychiatric disorders ranging from autism, schizophrenia, depression, and bipolar disorder to Alzheimer's disease. This implies that psychiatric symptoms as well as treatments may share aspects of pathophysiology and mechanisms

Please cite this article as: Koch, M., et al., Neuropharmacology of altered brain oscillations in schizophrenia, Int. J. Psychophysiol. (2015), http:// dx.doi.org/10.1016/j.ijpsycho.2015.02.014

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of action that violate current symptom-based diagnostic and neuronbased therapeutic notion. Bartzokis and colleagues emphasize that mechanisms of myelination could help to understand this unspecifity in psychotropic treatments (see Bartzokis, 2012 for review). Their myelin-centred model of human brain function criticises that most current clinical pharmacology is assumed to primarily affect neuronal synapses that are largely confined to gray matter. Their framework encourages a more integrated perspective of brain therapeutics that could be helpful for both clinical and research schemes. Specifically, it is suggested that direct and indirect effects on glia, oligodendrocytes and the myelin sheaths they produce in optimizing the timing and synchrony of action potentials, may represent a substantial portion of the efficacy provided by pharmaco- and other therapies. This approach mainly considers complex signaling pathways such as Akt and glycogen synthase kinase-3 (GSK3) that affect myelination, its plasticity, and repair (Bartzokis, 2012). Indeed, it is undisputable that myelination is a relevant feature for optimized timing and synchrony of action potentials, and in turn of efficient function of neuronal networks underlying cognition and behavior. The here reviewed studies on altered brain oscillations in schizophrenia, underline that timing is of essence to all cortical operations, and that this metric is critical in several psychiatric diseases including schizophrenia. Systematic investigation of pharmacologic effects on both brain oscillations and brain's oligodendrocyte populations may provide a promising approach not only to explain underlying disease processes, but to help optimize treatment opportunities and prevention of developmental and degenerative brain disorders (Bartzokis, 2003, 2012; Cropley et al., 2013). Thus, understanding the interaction between cognition, neurotransmitters, brain oscillations and myelinisation may help to understand the structural and functional disruptions of the brains communication mechanisms in schizophrenia (Cocchi et al., 2014). Well controlled studies may help to differentiate between genuine illness-related and medication-related effects. 5. Summary The search for biomarkers for complex diseases such as schizophrenia is important, because they might help investigating the symptomatology, etiopathogenesis and rational treatment of the illness. Taken together, EEG oscillations are considered as potential biomarkers for complex states in health and disease. However, we here report a very heterogeneous body of literature concerning schizophrenia-related changes in brain oscillations. The heterogeneity is due, first, to the complex neuropathology and course of the disease and, second, due to the fact that most studies include medicated patients. The literature presently does not allow disentangling the treatment effects and the disease effects on oscillations. We emphasize the necessity of systematic studies. Linking the approaches of EEG-neuropharmacology (e.g., using brain oscillations) with the assessment of the trajectory of human myelin development and its potential breakdown (e.g., using diffusion tensor imaging), could provide new insights into developmental and degenerative disease etiologies as well as treatment mechanisms. References Abi-Dargham, A., 2004. Do we still believe in the dopamine hypothesis? New data bring new evidence. Int. J. Neuropsychopharmacol. 7, 1–5. Andreasen, N.C., 2000. Schizophrenia: the fundamental questions. Brain Res. Rev. 31, 106–112. Bakanidze, G., Roinishvili, M., Chkonia, E., Kitzrow, W., Richter, S., Neumann, K., Herzog, M.H., Brand, A., Puls, I., 2013. Association of the nicotinic receptor a7 subunit gene (CHRNA7) with schizophrenia and visual backward masking. Front. Psychiatry 4, 133. Bartzokis, G., 2003. Schizophrenia: breakdown in the well-regulated lifelong process of brain development and maturation. Neuropsychopharmacology 27, 672–683. Bartzokis, G., 2012. Neurogliapharmacology: myelination as a shared mechanism of action of psychotropic treatments. Neuropharmacology 62, 2137–2153.

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Please cite this article as: Koch, M., et al., Neuropharmacology of altered brain oscillations in schizophrenia, Int. J. Psychophysiol. (2015), http:// dx.doi.org/10.1016/j.ijpsycho.2015.02.014

Neuropharmacology of altered brain oscillations in schizophrenia.

Impairments in spatial and temporal integration of brain network activity are a core feature of schizophrenia. Neural network oscillatory activity is ...
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