Orbitofrontal Lesion Alters Brain Dynamics of Emotion-Attention and Emotion-Cognitive Control Interaction in Humans

Abstract

Patients with lesion to the orbitofrontal cortex (OFC) experience challenges in emotional control and emotion-guided behaviors. The OFC is known to participate in executive functions and attentional control of emotion and our previous research suggests OFC lesion alters the balance between voluntary and involuntary attention and cognitive control within the context of emotion. To better understand how OFC lesion affects the dynamics and interaction of these functions, we studied EEG and performance of 12 patients with lesion to the OFC and 11 control subjects with intact OFC in a Go/NoGo visual reaction time (RT) task with neutral targets and intervening threat-related emotional distractors (Executive RT Test). Event-related potentials (ERPs), specifically N2P3 peak-to-peak amplitude and the following late positive potential (LPP), were used to measure allocation of attention and cognitive control to emotional distractors. Task performance and Behavior Rating Inventory of Executive Functions—Adult version (BRIEF-A) scores were used to assess executive functions. As expected, the Control group showed increased N2P3 amplitude in the context of threat-related distractors, particularly over the right hemisphere, while LPP was not modulated by these distractors. In contrast, patients with OFC lesion showed no such impact of threat-related distractors on N2P3 amplitude but exhibited increased and prolonged left-lateralized impact of threat on LPP in the Go-condition. In NoGo-condition, the N2P3 amplitude was increased in both groups due to threat, but the impact was seen earlier, i.e., at the N2 peak in the OFC group and later at the P3 peak in Controls. The OFC group committed more errors in the Executive RT Test and reported more problems in BRIEF-A, thus both objective and subjective evidence for challenges in executive functions was obtained in patients with orbitofrontal lesion. Furthermore, the time-course of attention allocation and cognitive control towards task-irrelevant emotional stimuli was altered as evidenced by ERPs. We conclude that orbitofrontal lesion is associated with altered neural dynamics underlying the interaction of involuntary attention to emotion and cognitive control. These alterations in brain dynamics may underlie some of the challenges patients encounter in everyday life when emotional events interact with cognitive demands.

Reduced Frontal Nogo-N2 With Uncompromised Response Inhibition During Transcutaneous Vagus Nerve Stimulation—More Efficient Cognitive Control?

“…Even when interfering with everyday life, executive dysfunction may not always be depicted in conventional neuropsychological tests, such as the Stroop test, the Tower of London test, or the Wisconsin Card Sorting Test (Hanna-Pladdy, 2007 ; Verdejo-García and Pérez-García, 2007 ; Løvstad et al, 2012a ). Conventional neuropsychological tests are performed in emotionally neutral and structured environments, as opposed to unstructured and emotionally burdening everyday life situations that require a far greater extent of cognitive control (Chaytor and Schmitter-Edgecombe, 2003 ; Kuusinen et al, 2018 ). Consider the vastly different requirements for cognitive control in a quiet testing room, where emotionally supportive neuropsychologist gives clear instructions what to do and one can fully focus on a single task at hand, in contrast to a busy office with multiple tasks, unexpected interruptions and occasional emotional events, such as a frustrated co-worker giving unpleasant feedback.…”

“…Executive RT-test is sensitive to subtle alterations, both impairment, and improvement, in executive functions and emotion-attention interaction due to neuromodulation (Hartikainen et al, 2014 ; Sun et al, 2015 , 2016 , 2017b ), cardiac surgery (Liimatainen et al, 2016 ), and brain injury (Mäki-Marttunen et al, 2015 , 2017 ; Kuusinen et al, 2018 ). The evidence for Executive RT-test truly assessing executive functions and the underlying fronto-thalamic circuits have been obtained with invasive deep brain stimulation (DBS) studies.…”

Analysis of correlation between white matter changes and functional responses in post-stroke depression

“…The orbital frontal cortex is related to working memory and mood (40). Therefore, reduced node efficiency in the area may support the hypothesis that depression is associated with orbitofrontal lesion altering brain dynamics of emotion-attention and emotion-cognitive control interaction in humans (41).…”

Executive Functions and Emotion–Attention Interaction in Assessment of Brain Health: Reliability of Repeated Testing With Executive RT Test and Correlation With BRIEF-A Questionnaire

“…Furthermore, the study was conducted in a healthy population and in order to extrapolate the relevance of the current findings to clinical populations, future studies on them are called for. However, currently our previous studies on mild head injury (Hartikainen et al, 2010), patients with focal lesion to OFC (Mäki-Marttunen et al, 2015, 2017; Kuusinen et al, 2018) and patients with DBS treatment for refractory epilepsy (Hartikainen et al, 2014) provide some support that Executive RT Test is also sensitive in detecting executive dysfunction in clinical populations.…”

“…Conventional neuropsychological tests tend to focus on isolated cognitive processes rather than co-operation and integration of several cognitive processes (Alvarez and Emory, 2006) and they are conducted in structured testing environments as opposed to distractible, unpredictable and unstructured real-world environments with parallel demands on multiple cognitive processes. Furthermore, in contrast to testing environments that are typically emotionally neutral or supportive, in real-world environments emotional challenges interact with executive functions (Chaytor and Schmitter-Edgecombe, 2003; Kuusinen et al, 2018). Thus, neuropsychological tests are conducted in ideal environments for optimal cognitive performance in contrast to unideal real-world environments that challenge executive functions to a greater extent in everyday life.…”