Role of the left amygdala and right orbital frontal cortex in emotional interference resolution facilitation in working memory

Previous research has shown that emotional information aids conflict resolution in working memory (Levens & Phelps, 2008). Using a Recency-probes working memory (WM) paradigm, Levens and Phelps found that positive and negative emotional stimuli reduced the amount of interference created when information that was once relevant conflicted with currently relevant information, suggesting that emotional information facilitates interference resolution in WM. To determine what regions of the prefrontal cortex (PFC) and temporal lobes are critical to the influence of emotional stimuli on interference resolution, we conducted a Recency-probes emotion paradigm with right and left unilateral frontal and temporal lobe lesion patients. The frontal lobe lesion patient group comprised individuals with unilateral ventral and dorsal PFC lesions. The temporal lobe lesion patient group comprised individuals with lesions of the amygdala and surrounding structures. Results indicate that when the left amygdala is damaged, emotional facilitation of interference resolution is absent (equal emotional and neutral interference levels), when the right orbital frontal cortex (OFC) is damaged, in contrast, emotional interference resolution is impaired (emotional interference levels are higher than neutral levels are). Based on these unique patterns we propose specific contributions for these regions in the emotional facilitation of interference resolution in WM.

[1]  E E Smith,et al.  The neural substrate and temporal dynamics of interference effects in working memory as revealed by event-related functional MRI. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[2]  M. Kringelbach The human orbitofrontal cortex: linking reward to hedonic experience , 2005, Nature Reviews Neuroscience.

[3]  Michael Davis,et al.  Neurobiology of fear responses: the role of the amygdala. , 1997, The Journal of neuropsychiatry and clinical neurosciences.

[4]  A P Shimamura,et al.  Source memory enhancement for emotional words. , 2001, Emotion.

[5]  K. Yau,et al.  Interoception: the sense of the physiological condition of the body , 2003, Current Opinion in Neurobiology.

[6]  E. Rolls,et al.  The Orbitofrontal Cortex , 2019 .

[7]  Timothy Edward John Behrens,et al.  Quantitative Investigation of Connections of the Prefrontal Cortex in the Human and Macaque using Probabilistic Diffusion Tractography , 2005, The Journal of Neuroscience.

[8]  D. Tucker,et al.  Mood, personality, and self-monitoring: negative affect and emotionality in relation to frontal lobe mechanisms of error monitoring. , 2000, Journal of experimental psychology. General.

[9]  G. Strauss,et al.  Positive and Negative Emotions Uniquely Capture Attention , 2009, Applied neuropsychology.

[10]  Robert T. Knight,et al.  Effects of frontal lobe damage on interference effects in working memory , 2002, Cognitive, affective & behavioral neuroscience.

[11]  G. McCarthy,et al.  Dissociable prefrontal brain systems for attention and emotion , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[12]  François Mauguière,et al.  Early Amygdala Reaction to Fear Spreading in Occipital, Temporal, and Frontal Cortex A Depth Electrode ERP Study in Human , 2004, Neuron.

[13]  John A Sweeney,et al.  Affect regulation: a systems neuroscience perspective , 2005, Neuropsychiatric disease and treatment.

[14]  Adam K. Anderson,et al.  Specifying the Contributions of the Human Amygdala to Emotional Memory : A Case Study , 2008 .

[15]  L Carretié,et al.  Emotion, attention, and the 'negativity bias', studied through event-related potentials. , 2001, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[16]  G. Gainotti Anatomical functional and cognitive determinants of semantic memory disorders , 2006, Neuroscience & Biobehavioral Reviews.

[17]  Hanna Damasio,et al.  Single-neuron responses to emotional visual stimuli recorded in human ventral prefrontal cortex , 2001, Nature Neuroscience.

[18]  S. Köhler,et al.  Double dissociation of selective recollection and familiarity impairments following two different surgical treatments for temporal-lobe epilepsy , 2010, Neuropsychologia.

[19]  Gregory A. Miller,et al.  Paying attention to emotion: , 2003, Cognitive, affective & behavioral neuroscience.

[20]  Elizabeth A. Phelps,et al.  Insula and Orbital Frontal Cortex Activity Underlying Emotion Interference Resolution in Working Memory , 2010, Journal of Cognitive Neuroscience.

[21]  E. Stern,et al.  Linguistic threat activates the human amygdala. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[22]  C. Rorden,et al.  Stereotaxic display of brain lesions. , 2000, Behavioural neurology.

[23]  L. Pessoa How do emotion and motivation direct executive control? , 2009, Trends in Cognitive Sciences.

[24]  Cheuk Y. Tang,et al.  Differential amygdala activation during emotional decision and recognition memory tasks using unpleasant words: an fMRI study , 2001, Neuropsychologia.

[25]  Sara M. Levens,et al.  Rumination and impaired resource allocation in depression. , 2009, Journal of abnormal psychology.

[26]  D. Eidelberg,et al.  Functional neuroanatomy of non-verbal semantic sound processing in humans , 2006, Journal of Neural Transmission.

[27]  J. Jonides,et al.  Brain mechanisms of proactive interference in working memory , 2006, Neuroscience.

[28]  Sara M. Levens,et al.  Emotion processing effects on interference resolution in working memory. , 2008, Emotion.

[29]  Joseph E LeDoux The emotional brain , 1996 .

[30]  A. Anderson,et al.  Specifying the Contributions of the Human Amygdala to Emotional Memory: A Case Study , 1998 .

[31]  S. Corkin,et al.  Effect of negative emotional content on working memory and long-term memory. , 2003, Emotion.

[32]  E. Murray,et al.  Orbitofrontal Cortex and Amygdala Contributions to Affect and Action in Primates , 2007, Annals of the New York Academy of Sciences.

[33]  J. Grafman,et al.  The Human Amygdala: An Evolved System for Relevance Detection , 2003, Reviews in the neurosciences.

[34]  E. Tulving,et al.  Episodic and declarative memory: Role of the hippocampus , 1998, Hippocampus.

[35]  J. Jonides,et al.  Inhibition in verbal working memory revealed by brain activation. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[36]  A. Craig How do you feel? Interoception: the sense of the physiological condition of the body , 2002, Nature Reviews Neuroscience.

[37]  Kae Nakamura,et al.  Basal ganglia orient eyes to reward. , 2006, Journal of neurophysiology.

[38]  G. Schoenbaum,et al.  Basolateral Amygdala Lesions Abolish Orbitofrontal-Dependent Reversal Impairments , 2007, Neuron.

[39]  S. Monsell Recency, immediate recognition memory, and reaction time , 1978, Cognitive Psychology.

[40]  Edmund T Rolls,et al.  Convergence of sensory systems in the orbitofrontal cortex in primates and brain design for emotion. , 2004, The anatomical record. Part A, Discoveries in molecular, cellular, and evolutionary biology.

[41]  M. Bradley,et al.  Affective Norms for English Words (ANEW): Instruction Manual and Affective Ratings , 1999 .

[42]  Kelly S. Giovanello,et al.  Neural correlates of familiarity-based associative retrieval , 2010, Neuropsychologia.

[43]  J. Jonides,et al.  Interference resolution: Insights from a meta-analysis of neuroimaging tasks , 2007, Cognitive, affective & behavioral neuroscience.