Elsevier

Journal of Psychiatric Research

Volume 72, January 2016, Pages 64-71
Journal of Psychiatric Research

Electrical mapping in bipolar disorder patients during the oddball paradigm

https://doi.org/10.1016/j.jpsychires.2015.10.012Get rights and content

Highlights

  • Higher P300 amplitude in healthy controls, low P300 amplitude in manic patients.

  • Similar P300 amplitude and latency in euthymic and depressive patients.

  • Manic group showed the smallest P300 amplitude, mainly for the frontal electrodes.

  • Small P300 amplitude for the pre-frontal area electrodes can be related to an impairment of cognitive flexibility.

  • This study provided a evidence of a delay in the information processing and reduced attention allocation of bipolar patients.

Abstract

Bipolar disorder (BD) is characterized by an alternated occurrence between acute mania episodes and depression or remission moments. The objective of this study is to analyze the information processing changes in BP (Bipolar Patients) (euthymia, depression and mania) during the oddball paradigm, focusing on the P300 component, an electric potential of the cerebral cortex generated in response to external sensorial stimuli, which involves more complex neurophysiological processes related to stimulus interpretation. Twenty-eight bipolar disorder patients (BP) (17 women and 11 men with average age of 32.5, SD: 9.5) and eleven healthy controls (HC) (7 women and 4 men with average age of 29.78, SD: 6.89) were enrolled in this study. The bipolar patients were divided into 3 major groups (i.e., euthymic, depressive and maniac) according to the score on the Clinical Global Impression – Bipolar Version (CGI-BP). The subjects performed the oddball paradigm simultaneously to the EEG record. EEG data were also recorded before and after the execution of the task. A one-way ANOVA was applied to compare the P300 component among the groups. After observing P300 and the subcomponents P3a and P3b, a similarity of amplitude and latency between euthymic and depressive patients was observed, as well as small amplitude in the pre-frontal cortex and reduced P3a response. This can be evidence of impaired information processing, cognitive flexibility, working memory, executive functions and ability to shift the attention and processing to the target and away from distracting stimuli in BD. Such neuropsychological impairments are related to different BD symptoms, which should be known and considered, in order to develop effective clinical treatment strategies.

Introduction

Bipolar disorder (BD) and its neurological, cognitive and behavioral bases have been widely investigated. BD is considered to be a relatively frequent and chronic psychiatric condition, causing professional and social difficulties or incapacitation (Akiskal et al., 2000, Fleck et al., 2003, Hisatugo et al., 2009, Kaplan et al., 1997). According to Özerdem et al. (2008), BD involves various cognitive dysfunctions, even in the euthymic phase of the illness. Emotional deregulation and cognitive deficits in euthymia are indicators of an enduring pathology in BD. Disruptions of the connections among the frontal cortex, amygdala, basal ganglia, thalamus, entorhinal cortex and hippocampus are probable participants in the underlying pathology of BD (Atagün et al., 2013, Dupont et al., 1995, Blumberg et al., 2002, Caligiuri et al., 2004, Phillips et al., 2003, Strakowski et al., 2005). These connections are also believed to serve in the modulation of cognition and emotional consonance (Strakowski et al., 2005).

Previous studies have demonstrated cognitive deficits specific for each mood phase of bipolar disorder. Özerdem et al. (2008) identified manic patients to display signs of dysfunction in attentional measures, complex processing and memory. Having an acute episode of mania or depression is suggested to cause damage to the learning and memory systems (Bearden et al., 2001). Recently, new evidence corroborates the hypothesis of inflammation and neurodegeneration in BD and the relation between number of mood episodes and neurocognitive dysfunction. The understanding of the neurobiology and neuroimaging of BD progression and activity contributes to the establishment of BD biomarkers, which include inflammatory cytokines, neurotrophins, mitochondrial dysfunction, oxidative stress, epigenetic effects, and morphometric and neurostructural abnormalities. These parameters appear to be sensitive to the illness stage, and they are indeed the first biochemical indicators of the staging model in BD (McGorry et al., 2006, Berk et al., 2007, Berk et al., 2011, Roda et al., 2015). This way, we suggest P300 components to be investigated as a BD biomarker, specifically related to information processing and cognitive deficits. According to Purcell et al. (1997), information processing is associated with neurocognitive dysfunctions of BD. Attentional and cognitive alterations are significant in different BD states and they also persist into euthymic phases (Maekawa et al., 2013). Cognitive deficits in response inhibition, verbal memory and attention persist across mood phases but are enhanced during the manic and depressive states (Robinson et al., 2006). These patients present deficits in a broad range of cognitive functions, such as verbal memory, sustained attention, executive function aspects and emotional processing (Andersson et al., 2008, Maekawa et al., 2013). Comparative studies between bipolar disorder patients (BP) and depressive patients showed that, during the manic state, it is harder to maintain attention and inhibit inadequate behaviors, while during depression the problem is shared attention (Murphy et al., 1999).

Electroencephalography (EEG) has been used with BP to verify rhythmic changes in brain functions in both depression and mania states (Atagün et al., 2013, Cole et al., 1993, El-Badri et al., 2001). This kind of electrophysiological research is important to identify resulting changes in cognitive dysfunctions, especially attention. However, most of the studies investigating electrocortical changes in BP used different methodology and data processing. Maekawa et al. (2013) used electrical mapping to show that BP have deficits in visual information processing, starting from the very early stages all the way to higher-level cognitive functions. The EEG study of Yeap et al. (2009) also evidenced that visual processing deficit is apparent in schizophrenic patients and BP. According to Hall et al., 2007, Hall et al., 2012), sensory gating deficit has been proposed as an endophenotype for BD and schizophrenia. Early auditory gamma band response has been used to assess basic brain functions associated with auditory perception and showed that BP and schizophrenic patients featured reduced early evoked gamma band response (Hall et al., 2011, Roach and Mathalon, 2008). Donchin and Coles (1988) used P2 and P3 ERP (event related potential) components to assess higher-order cognitive processes related with attention, working memory and information processing speed. Patients with both disorders showed impaired central P3 ERPs, but P2 ERP deficit has been documented only in schizophrenic patients (O'Donnell et al., 2004). Although Donchin and Coles (1988) observed the P3 component, there is a lack of studies investigating more deeply the P300 component in the BP states, and among BP and healthy subjects. The objective of this study is to analyze the alterations of information processing in BP (euthymia, depression and mania phases) through the observation of the P300 component. We hypothesized BP to present a delay in information processing, represented by a higher P300 latency, mainly in the depressive group. On the other hand, we expect to find lower P300 amplitude for BP.

Section snippets

Subjects

Eleven healthy controls (7 women and 4 men with average age of 29.78, SD: 6.89) and twenty-eight bipolar patients (17 women and 11 men with average age of 32.5, SD: 9.5) under treatment participated of this study. Patients with a lifetime history of BD and those with only current history of BD were included. They were diagnosed according to the DSM-IV (Diagnostic and Statistical Manual of Psychiatric Disorders-fourth edition) (American Psychiatric Association, 1994), and they were asked to

reaction time

The one-way ANOVA demonstrated a main effect for group (p < 0.05). The post-hoc analysis showed no difference between euthymic (average: 451.57 ms, SD: 77.47 ms) and depression (average: 455.94 ms, SD: 81.82 ms) groups. We also observed that the control (average: 414.3109 ms, SD: 79.33134) and manic (average: 433.0641 ms, SD: 81.86123) groups differed from the other groups (Fig. 1).

Event-related potentials

P300 amplitude and latency were observed, as well as the subcomponents P3a and P3b. Results will be explained and

Discussion

The purpose of this study was to investigate neurophysiological differences and similarities between BP and HC, through the P300 analysis. Our main findings were higher P300 amplitude in HC, low P300 amplitude in manic patients, similar amplitude and latency in euthymic and depressive patients and slower reactivity of BP. P300 amplitude and latency in BP during both depressive and euthymic periods did not differ in many areas.

P300 latency indicates stimulus processing time, largely independent

Conclusion

The main findings of this study were: higher P300 amplitude in HC, low P300 amplitude in manic patients and similar amplitude and latency in euthymic and depressive patients. The manic group showed the smallest P300 amplitude, mainly for the frontal electrodes, which can be related to manic state symptoms. This study provided some evidence of cognitive deficits in BP, like a delay in information processing and reduced attention allocation, which is in agreement with previous studies about BD

Conflicts of interest

The authors and the represented institutions confirm that the content of the present article has no conflict of interest.

Funding Source

There were no funding source. The financial investment was done by the authors.

Acknowledgments

The authors wish to acknowledge grant support from the Institute of Psychiatry of the Federal University of Rio de Janeiro (Rio de Janeiro, Brazil), from the Laboratory of Panic and Respiration and from the Institute of Psychiatry and the Brain Mapping and Sensory Motor Integration Laboratory of the Federal University of Rio de Janeiro.

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      The majorities of studies exploring P300 activity in individuals with BP have been focusing on the P3b, and typically used an auditory oddball paradigm (Bersani et al., 2015; Muir et al., 1991; Friedberg et al., 2009,; Bestelmeyer et al., 2009) in which participants discriminate between frequent (background) and rare (target) tones. Abnormalities in this component have been found in BP type-I; in particular, the reduction in the amplitude of P3b component represents the most common neurophysiological abnormality observed in BP patients, compared to healthy individuals, regardless of mood status (Friedberg et al., 2009; Bersani et al., 2015; Nancy et al., 2017; Ozerdem et al., 2008; Maekawa et al., 2012; Silva et al., 2016), and it has been proposed as a potential endophenotype of BP (Nancy et al., 2017). There is also evidence of lower P300 amplitude in individuals with current depression (Zhu et al., 2018; Zhou et al., 2018), which appears to normalize when the symptoms are remitted (Feldmann et al., 2018).

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      History of psychosis was associated with 811 (60.9%) patients. There were more than 3 studies that measured P3a amplitude with an auditory paradigm (Andersson et al., 2008; Hamm et al., 2013; Jahshan et al., 2012; Suazo et al., 2016), P3b amplitude with an auditory paradigm (Andersson et al., 2008; Bersani et al., 2015; Bestelmeyer et al., 2009; Dutt et al., 2012; Ethridge et al., 2015, 2012; Fridberg et al., 2009; Hall et al., 2015a, 2014, 2007; Hall et al., 2009; Hamm et al., 2013; Johannesen et al., 2013; Kaya et al., 2007; Lahera et al., 2009; Muir et al., 1991; O'Donnell et al., 2004; Salisbury et al., 1999; Schulze et al., 2008; Souza et al., 1995; Strik et al., 1998; Suazo et al., 2016; Vuurman et al., 2002), P3b latency with an auditory paradigm (Andersson et al., 2008; Bersani et al., 2015; Bestelmeyer et al., 2009; Dutt et al., 2012; Ethridge et al., 2015, 2012; Fridberg et al., 2009; Hall et al., 2015a, 2014, 2007; Hall et al., 2009; Johannesen et al., 2013; Kaya et al., 2007; Lahera et al., 2009; Muir et al., 1991; O'Donnell et al., 2004; Salisbury et al., 1999; Schulze et al., 2008; Souza et al., 1995; Strik et al., 1998; Vuurman et al., 2002), P3b amplitude with a visual paradigm (Bange and Bathien, 1998; Bestelmeyer, 2012; Bestelmeyer et al., 2009; Di Giorgio Silva et al., 2016; Maekawa et al., 2013; Ryu et al., 2010; Sokhadze et al., 2011), P3b latency with a visual paradigm (Bange and Bathien, 1998; Bestelmeyer, 2012; Bestelmeyer et al., 2009; Di Giorgio Silva et al., 2016; Maekawa et al., 2013; Sokhadze et al., 2011), P3b amplitude with an auditory paradigm in patients who had history of psychosis (Dutt et al., 2012; Ethridge et al., 2015, 2012; Fridberg et al., 2009; Hall et al., 2015a, 2014, 2007; Hall et al., 2009; Hamm et al., 2013; O'Donnell et al., 2004; Salisbury et al., 1999; Schulze et al., 2008; Suazo et al., 2016), P3b latency with an auditory paradigm in patients who had history of psychosis (Dutt et al., 2012; Ethridge et al., 2015, 2012; Fridberg et al., 2009; Hall et al., 2015a, 2014, 2007; Hall et al., 2009; O'Donnell et al., 2004; Salisbury et al., 1999; Schulze et al., 2008), P3b amplitude with an auditory paradigm at euthymic phase (Andersson et al., 2008; Bersani et al., 2015; Bestelmeyer et al., 2009; Dutt et al., 2012; Ethridge et al., 2015, 2012; Hall et al., 2015a, 2014, 2007; Hamm et al., 2013; Kaya et al., 2007; Lahera et al., 2009; Muir et al., 1991; Souza et al., 1995; Suazo et al., 2016; Vuurman et al., 2002), P3b amplitude with a visual paradigm at euthymic phase (Bestelmeyer et al., 2009; Di Giorgio Silva et al., 2016; Maekawa et al., 2013; Sokhadze et al., 2011), P3b latency with an auditory paradigm at euthymic phase (Andersson et al., 2008; Bersani et al., 2015; Bestelmeyer et al., 2009; Dutt et al., 2012; Ethridge et al., 2015, 2012; Hall et al., 2015a, 2014, 2009; Kaya et al., 2007; Lahera et al., 2009; Muir et al., 1991; Souza et al., 1995; Vuurman et al., 2002), P3b latency with a visual paradigm at euthymic phase (Bestelmeyer et al., 2009; Di Giorgio Silva et al., 2016; Maekawa et al., 2013; Sokhadze et al., 2011), P3b amplitude with an auditory paradigm at manic phase (Muir et al., 1991; Salisbury et al., 1999; Strik et al., 1998), P3b latency with an auditory paradigm at manic phase (Muir et al., 1991; Salisbury et al., 1999; Strik et al., 1998), P3b amplitude with an auditory paradigm in patients with BD-I (Bersani et al., 2015; Dutt et al., 2012; Ethridge et al., 2015, 2012; Fridberg et al., 2009; Hall et al., 2015a, 2014, 2007; Hall et al., 2009; Johannesen et al., 2013; Kaya et al., 2007; Lahera et al., 2009; Muir et al., 1991; O'Donnell et al., 2004; Salisbury et al., 1999; Schulze et al., 2008; Souza et al., 1995; Strik et al., 1998; Suazo et al., 2016; Vuurman et al., 2002), P3b amplitude with a visual paradigm in patients with BD-I (Bestelmeyer, 2012; Ryu et al., 2010; Sokhadze et al., 2011), P3b latency with an auditory paradigm in patients with BD-I (Bersani et al., 2015; Dutt et al., 2012; Ethridge et al., 2015, 2012; Fridberg et al., 2009; Hall et al., 2015a, 2014, 2007; Hall et al., 2009; Johannesen et al., 2013; Kaya et al., 2007; Lahera et al., 2009; Muir et al., 1991; O'Donnell et al., 2004; Salisbury et al., 1999; Schulze et al., 2008; Souza et al., 1995; Strik et al., 1998; Vuurman et al., 2002), P3b amplitude with an auditory paradigm in patients with BD-II (Andersson et al., 2008; Bersani et al., 2015; Muir et al., 1991; Vuurman et al., 2002), and P3b latency with an auditory paradigm in patients with BD-II (Andersson et al., 2008; Bersani et al., 2015; Muir et al., 1991). We were not able to conduct meta-analyses of the studies with the other paradigms including P3a amplitude with a visual paradigm, P3a latency whit any paradigm, P3a amplitude or latency with any paradigm in patients with psychosis, euthymic phase, manic phase, depressive phase, BD-I, BD-II, P3b amplitude or latency with a visual paradigm patients with psychosis, manic phase or BD-II, P3b amplitude or latency with any paradigm in patients at depressive phase, P3b latency with visual paradigm in patients with BD-I due to insufficient number of studies.

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