Effects of prefrontal cortex damage on emotion understanding: EEG and behavioural evidence

ABSTRACT

Humans are highly social beings that interact with each other on a daily basis. In these complex interactions, we get along by being able to identify others’ actions and infer their intentions, thoughts and feelings. One of the major theories accounting for this critical ability assumes that the understanding of social signals is based on a primordial tendency to simulate observed actions by activating a mirror neuron system. If mirror neuron regions are important for action and emotion recognition, damage to regions in this network should lead to deficits in these domains. In the current behavioural and EEG study, we focused on the lateral prefrontal cortex including dorsal and ventral prefrontal cortex and utilized a series of task paradigms, each measuring a different aspect of recognizing others’ actions or emotions from body cues. We examined 17 patients with lesions including (n = 8) or not including (n = 9) the inferior frontal gyrus, a core mirror neuron system region, and compared their performance to matched healthy control subjects (n = 18), in behavioural tasks and in an EEG observation—execution task measuring mu suppression. Our results provide support for the role of the lateral prefrontal cortex in understanding others’ emotions, by showing that even unilateral lesions result in deficits in both accuracy and reaction time in tasks involving the recognition of others’ emotions. In tasks involving the recognition of actions, patients showed a general increase in reaction time, but not a reduction in accuracy. Deficits in emotion recognition can be seen by either direct damage to the inferior frontal gyrus, or via damage to dorsal lateral prefrontal cortex regions, resulting in deteriorated performance and less EEG mu suppression over sensorimotor cortex.

AUTHORS

• Anat Perry

• Samantha N. Saunders

• Jennifer Stiso

• Callum Dewar

• James Lubell

• Torstein Meling

• Anne-Kristin Solbakk

• Tor Endestad

• Robert T. Knight

Date: 2017

DOI: 10.1093/brain/awx031

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ERP Correlates of Proactive and Reactive Cognitive Control in Treatment-Naïve Adult ADHD

ABSTRACT

This study investigated whether treatment naïve adults with Attention Deficit Hyperactivity Disorder (ADHD; n = 33; 19 female) differed from healthy controls (n = 31; 17 female) in behavioral performance, event-related potential (ERP) indices of preparatory attention (CueP3 and late CNV), and reactive response control (Go P3, NoGo N2, and NoGo P3) derived from a visual cued Go/NoGo task. On several critical measures, Cue P3, late CNV, and NoGo N2, there were no significant differences between the groups. This indicated normal preparatory processes and conflict monitoring in ADHD patients. However, the patients had attenuated Go P3 and NoGoP3 amplitudes relative to controls, suggesting reduced allocation of attentional resources to processes involved in response control. The patients also had a higher rate of Go signal omission errors, but no other performance decrements compared with controls. Reduced Go P3 and NoGo P3 amplitudes were associated with poorer task performance, particularly in the ADHD group. Notably, the ERPs were not associated with self-reported mood or anxiety. The results provide electrophysiological evidence for reduced effortful engagement of attentional resources to both Go and NoGo signals when reactive response control is needed. The absence of group differences in ERP components indexing proactive control points to impairments in specific aspects of cognitive processes in an untreated adult ADHD cohort. The associations between ERPs and task performance provided additional support for the altered electrophysiological responses.

AUTHORS

• Venke A. Grane

• Jan F. Brunner

• Tor Endestad

• Ida E.S. Aasen

• Juri Kropotov

• Robert T. Knight

• Anne-Kristin Solbakk

Date: 2016

DOI: 10.1371/journal.pone.0159833

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Impact of orbitofrontal lesions on electrophysiological signals in a stop signal task

Authors:

• Anne-Kristin Solbakk

• Ingrid Funderud

• Tor Endestad

• Torstein Meling

• Magnus Lindgren

• Robert T. Knight

• Ulrike M. Krämer

Date: 2014

DOI: 10.1162/jocn_a_00561

PubMed: 24392904

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Abstract:

Behavioral inhibition and performance monitoring are critical cognitive functions supported by distributed neural networks including the pFC. We examined neurophysiological correlates of motor response inhibition and action monitoring in patients with focal orbitofrontal (OFC) lesions (n = 12) after resection of a primary intracranial tumor or contusion because of traumatic brain injury. Healthy participants served as controls (n = 14). Participants performed a visual stop signal task. We analyzed behavioral performance as well as event-related brain potentials and oscillations. Inhibition difficulty was adjusted individually to yield an equal amount of successful inhibitions across participants. RTs of patients and controls did not differ significantly in go trials or in failed stop trials, and no differences were observed in estimated stop signal RT. However, electrophysiological response patterns during task performance distinguished the groups. Patients with OFC lesions had enhanced P3 amplitudes to congruent condition go signals and to stop signals. In stop trials, patients had attenuated N2 and error-related negativity, but enhanced error positivity. Patients also showed enhanced and prolonged post-error beta band increases for stop errors. This effect was particularly evident in patients whose lesion extended to the subgenual cingulate cortex. In summary, although response inhibition was not impaired, the diminished stop N2 and ERN support a critical role of the OFC in action monitoring. Moreover, the increased stop P3, error positivity, and post-error beta response indicate that OFC injury affected action outcome evaluation and support the notion that the OFC is relevant for the processing of abstract reinforcers such as performing correctly in the task.

Low attentional engagement makes attention network activity susceptible to emotional interference

Authors:

• Robert T. Knight

• Kaisa M. Hartikainen

• Keith H. Ogawa

• Natasha Pickard

• Anne-Kristin Solbakk

• Verónica Mäki-Marttu

Date: 2014

DOI: 10.1097/WNR.0000000000000223

PubMed: 4162342

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Abstract:

The aim of this study was to investigate whether emotion–attention interaction depends on attentional engagement. To investigate emotional modulation of attention network activation, we used a functional MRI paradigm consisting of a visuospatial attention task with either frequent (high-engagement) or infrequent (low-engagement) targets and intermittent emotional or neutral distractors. The attention task recruited a bilateral frontoparietal network with no emotional interference on network activation when the attentional engagement was high. In contrast, when the attentional engagement was low, the unpleasant stimuli interfered with the activation of the frontoparietal attention network, especially in the right hemisphere. This study provides novel evidence for low attentional engagement making attention control network activation susceptible to emotional interference.

Preparatory attention after lesions to the lateral or orbital prefrontal cortex: an event-related potential study

Authors:

• Ingrid Funderud

• Marianne Lovstad

• Magnus Lindgren

• Tor Endestad

• Paulina Due-Tønnesse

• Torstein Meling

• Robert T. Knight

• Anne-Kristin Solbakk

Date: 2013

PubMed: 23831520

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Abstract:

The prefrontal cortex (PFC) plays a central role in preparatory and anticipatory attentional processes. To investigate whether subregions of the PFC play differential roles in these processes we investigated the effect of focal lesions to either lateral prefrontal (lateral PFC; n=11) or orbitofrontal cortex (OFC; n=13) on the contingent negative variation (CNV), an electrophysiological index of preparatory brain processes. The CNV was studied using a Go/NoGo delayed response task where an auditory S1 signaled whether or not an upcoming visual S2 was a Go or a NoGo stimulus. Neither early (500–1000 ms) nor late (3200–3700 ms) phase Go trial CNV amplitude was reduced for any of the patient groups in comparison to controls. However, the lateral PFC group showed enhanced Go trial early CNV and reduced late CNV Go/NoGo differentiation. These data suggests that normal orienting and evaluation as reflected by the CNV is intact after OFC lesions. The enhanced early CNV after lateral PFC damage may be due to failure in inhibition and the reduced late CNV difference wave confirms a deficit in preparatory attention after damage to this frontal subregion.

Differential Go/NoGo activity in both contingent negative variation and spectral power

Authors:

• Ingrid Funderud

• Magnus Lindgren

• Marianne Lovstad

• Tor Endestad

• Bradley Voytek

• Robert T. Knight

• Anne-Kristin Solbakk

Date: 2012

DOI: 10.1371/journal.pone.0048504

PubMed: 23119040

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Abstract:

We investigated whether both the contingent negative variation (CNV), an event-related potential index of preparatory brain activity, and event-related oscillatory EEG activity differentiated Go and NoGo trials in a delayed response task. CNV and spectral power (4-100 Hz) were calculated from EEG activity in the preparatory interval in 16 healthy adult participants. As previously reported, CNV amplitudes were higher in Go compared to NoGo trials. In addition, event-related spectral power of the Go condition was reduced in the theta to low gamma range compared to the NoGo condition, confirming that preparing to respond is associated with modulation of event-related spectral activity as well as the CNV. Altogether, the impact of the experimental manipulation on both slow event-related potentials and oscillatory EEG activity may reflect coordinated dynamic changes in the excitability of distributed neural networks involved in preparation.

Anterior Cingulate Cortex and Cognitive Control: Neuropsychological and Electrophysiological Findings in Two Patients with Lesions to Dorsomedial Prefrontal Cortex

Authors:

• Marianne Lovstad

• Ingrid Funderud

• Torstein Meling

• Ulrike M. Krämer

• Bradley Voytek

• Paulina Due-Tønnesse

• Tor Endestad

• Magnus Lindgren

• Robert T. Knight

• Anne-Kristin Solbakk

Date: 2012

DOI: 10.1016/j.bandc.2012.07.008

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Abstract:

Whereas neuroimaging studies of healthy subjects have demonstrated an association between the anterior cingulate cortex (ACC) and cognitive control functions, including response monitoring and error detection, lesion studies are sparse and have produced mixed results. Due to largely normal behavioral test results in two patients with medial prefrontal lesions, a hypothesis has been advanced claiming that the ACC is not involved in cognitive operations. In the current study, two comparably rare patients with unilateral lesions to dorsal medial prefrontal cortex (MPFC) encompassing the ACC were assessed with neuropsychological tests as well as Event-Related Potentials in two experimental paradigms known to engage prefrontal cortex (PFC). These included an auditory Novelty Oddball task and a visual Stop-signal task. Both patients performed normally on the Stroop test but showed reduced performance on tests of learning and memory. Moreover, altered attentional control was reflected in a diminished Novelty P3, whereas the posterior P3b to target stimuli was present in both patients. The error-related negativity, which has been hypothesized to be generated in the ACC, was present in both patients, but alterations of inhibitory behavior were observed. Although interpretative caution is generally called for in single case studies, and the fact that the lesions extended outside the ACC, the findings nevertheless suggest a role for MPFC in cognitive control that is not restricted to error monitoring.

Contribution of Subregions of Human Frontal Cortex to Novelty Processing

Authors:

• Marianne Lovstad

• Ingrid Funderud

• Magnus Lindgren

• Tor Endestad

• Paulina Due-Tønnesse

• Torstein Meling

• Bradley Voytek

• Robert T. Knight

• Anne-Kristin Solbakk

Date: 2012

DOI: 10.1162/jocn_a_00099

PubMed: 21812562

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Abstract:

Novelty processing was studied in patients with lesions centered in either OFC or lateral pFC (LPFC). An auditory novelty oddball ERP paradigm was applied with environmental sounds serving as task irrelevant novel stimuli. Lesions to the LPFC as well as the OFC resulted in a reduction of the frontal Novelty P3 response, supporting a key role of both frontal subdivisions in novelty processing. The posterior P3b to target sounds was unaffected in patients with frontal lobe lesions in either location, indicating intact posterior cortical target detection mechanisms. LPFC patients displayed an enhanced sustained negative slow wave (NSW) to novel sounds not observed in OFC patients, indicating prolonged resource allocation to task-irrelevant stimuli after LPFC damage. Both patient groups displayed an enhanced NSW to targets relative to controls. However, there was no difference in behavior between patients and controls suggesting that the enhanced NSW to targets may index an increased resource allocation to response requirements enabling comparable performance in the frontal lesioned patients. The current findings indicate that the LPFC and OFC have partly shared and partly differential contributions to the cognitive subcomponents of novelty processing.

The role of the lateral prefrontal cortex in inhibitory motor control

Authors:

• Ulrike M. Krämer

• Anne-Kristin Solbakk

• Ingrid Funderud

• Marianne Lovstad

• Tor Endestad

• Robert T. Knight

Date: 2012

DOI: 10.1016/j.cortex.2012.05.003

PubMed: 22699024

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Abstract:

Research on inhibitory motor control has implicated several prefrontal as well as subcortical and parietal regions in response inhibition. Whether prefrontal regions are critical for inhibition, attention or task-set representation is still under debate. We investigated the influence of the lateral prefrontal cortex (PFC) in a response inhibition task by using cognitive electrophysiology in prefrontal lesion patients. Patients and age- and education-matched controls performed in a visual Stop-signal task featuring lateralized stimuli, designed to challenge either the intact or lesioned hemisphere. Participants also underwent a purely behavioral Go/Nogo task, which included a manipulation of inhibition difficulty (blocks with 50 vs. 80% go-trials) and a Change-signal task that required switching to an alternative response. Patients and controls did not differ in their inhibitory speed (stop-signal and change-signal reaction time, SSRT and CSRT), but patients made more errors in the Go/Nogo task and showed more variable performance. The behavioral data stress the role of the PFC in maintaining inhibitory control but not in actual inhibition. These results support a dissociation between action cancellation and PFC-dependent action restraint. Laplacian transformed event-related potentials (ERPs) revealed reduced parietal activity in PFC patients in response to the stop-signals, and increased frontal activity over the intact hemisphere. This electrophysiological finding supports altered PFC-dependent visual processing of the stop-signal in parietal areas and compensatory activity in the intact frontal cortex. No group differences were found in the mu and beta decrease as measures of response preparation and inhibition at electrodes over sensorimotor cortex. Taken together, the data provide evidence for a central role of the lateral PFC in attentional control in the context of response inhibition.

Executive functions after orbital or lateral prefrontal lesions: neuropsychological profiles and self-reported executive functions in everyday living

Authors:

• Marianne Lovstad

• Ingrid Funderud

• Tor Endestad

• Paulina Due-Tønnesse

• Torstein Meling

• Magnus Lindgren

• Robert T. Knight

• Anne-Kristin Solbakk

Date: 2012

DOI: 10.3109/02699052.2012.698787

PubMed: 22731818

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Abstract:

OBJECTIVE: This study examined the effects of chronic focal lesions to the lateral prefrontal cortex (LPFC) or orbitofrontal cortex (OFC) on neuropsychological test performance and self-reported executive functioning in everyday living. METHODS: Fourteen adults with OFC lesions were compared to 10 patients with LPFC injuries and 21 healthy controls. Neuropsychological tests with emphasis on measures of cognitive executive function were administered along with the Behavior Rating Inventory of Executive Functions (BRIEF-A) and a psychiatric screening instrument. RESULTS: The LPFC group differed from healthy controls on neuropsychological tests of sustained mental effort, response inhibition, working memory and mental switching, while the BRIEF-A provided more clinically important information on deficits in everyday life in the OFC group compared to the LPFC group. Correlations between neuropsychological test results and BRIEF-A were weak, while the BRIEF-A correlated strongly with emotional distress. CONCLUSIONS: It was demonstrated that LPFC damage is particularly prone to cause cognitive executive deficit, while OFC injury is more strongly associated with self-reported dysexecutive symptoms in everyday living. The study illustrates the challenge of identifying executive deficit in individual patients and the lack of strong anatomical specificity of the currently employed methods. There is a need for an integrative methodological approach where standard testing batteries are supplemented with neuropsychiatric and frontal-specific rating scales.

Altered prefrontal function with aging: insights into age-associated cognitive decline

Authors:

• Anne-Kristin Solbakk

• Galit Fuhrmann Alpert

• Ansgar J. Furst

• Laura A. Hale

• Tatsuhide Oga

• Sundari Chetty

• Natasha Pickard

• Robert T. Knight

Date: 2008

DOI: 10.1016/j.brainres.2008.07.060

PubMed: 18691562

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Abstract:

We examined the effects of aging on visuo-spatial attention. Participants performed a bi-field visual selective attention task consisting of infrequent target and task-irrelevant novel stimuli randomly embedded among repeated standards in either attended or unattended visual fields. Blood oxygenation level dependent (BOLD) responses to the different classes of stimuli were measured using functional magnetic resonance imaging. The older group had slower reaction times to targets, and committed more false alarms but had comparable detection accuracy to young controls. Attended target and novel stimuli activated comparable widely distributed attention networks, including anterior and posterior association cortex, in both groups. The older group had reduced spatial extent of activation in several regions, including prefrontal, basal ganglia, and visual processing areas. In particular, the anterior cingulate and superior frontal gyrus showed more restricted activation in older compared with young adults across all attentional conditions and stimulus categories. The spatial extent of activations correlated with task performance in both age groups, but the regional pattern of association between hemodynamic responses and behavior differed between the groups. Whereas the young subjects relied on posterior regions, the older subjects engaged frontal areas. The results indicate that aging alters the functioning of neural networks subserving visual attention, and that these changes are related to cognitive performance.