Richard D. Lane

Neurobiology of emotion perception I: the neural basis of normal emotion perception

There is at present limited understanding of the neurobiological basis of the different processes underlying emotion perception. We have aimed to identify potential neural correlates of three processes suggested by appraisalist theories as important for emotion perception: 1) the identification of the emotional significance of a stimulus; 2) the production of an affective state in response to 1; and 3) the regulation of the affective state. In a critical review, we have examined findings from recent animal, human lesion, and functional neuroimaging studies. Findings from these studies indicate that these processes may be dependent upon the functioning of two neural systems: a ventral system, including the amygdala, insula, ventral striatum, and ventral regions of the anterior cingulate gyrus and prefrontal cortex, predominantly important for processes 1 and 2 and automatic regulation of emotional responses; and a dorsal system, including the hippocampus and dorsal regions of anterior cingulate gyrus and prefrontal cortex, predominantly important for process 3. We suggest that the extent to which a stimulus is identified as emotive and is associated with the production of an affective state may be dependent upon levels of activity within these two neural systems.

Neurobiology of emotion perception II: Implications for major psychiatric disorders.

To date, there has been little investigation of the neurobiological basis of emotion processing abnormalities in psychiatric populations. We have previously discussed two neural systems: 1) a ventral system, including the amygdala, insula, ventral striatum, ventral anterior cingulate gyrus, and prefrontal cortex, for identification of the emotional significance of a stimulus, production of affective states, and automatic regulation of emotional responses; and 2) a dorsal system, including the hippocampus, dorsal anterior cingulate gyrus, and prefrontal cortex, for the effortful regulation of affective states and subsequent behavior. In this critical review, we have examined evidence from studies employing a variety of techniques for distinct patterns of structural and functional abnormalities in these neural systems in schizophrenia, bipolar disorder, and major depressive disorder. In each psychiatric disorder, the pattern of abnormalities may be associated with specific symptoms, including emotional flattening, anhedonia, and persecutory delusions in schizophrenia, prominent mood swings, emotional lability, and distractibility in bipolar disorder during depression and mania, and with depressed mood and anhedonia in major depressive disorder. We suggest that distinct patterns of structural and functional abnormalities in neural systems important for emotion processing are associated with specific symptoms of schizophrenia and bipolar and major depressive disorder.

A model of neurovisceral integration in emotion regulation and dysregulation

In the present paper we present the outlines of a model that integrates autonomic, attentional, and affective systems into a functional and structural network that may help to guide us in our understanding of emotion regulation and dysregulation. We will emphasize the relationship between attentional regulation and affective processes and propose a group of underlying physiological systems that serve to integrate these functions in the service of self-regulation and adaptability of the organism. We will attempt to place this network in the context of dynamical systems models which involve feedback and feedforward circuits with special attention to negative feedback mechanisms, inhibitory processes, and their role in response selection. From a systems perspective, inhibitory processes can be viewed as negative feedback circuits that allow for the interruption of ongoing behavior and the re-deployment of resources to other tasks. When these negative feedback mechanisms are compromised, positive feedback loops may develop as a result (of dis-inhibition). From this perspective, the relative sympathetic activation seen in anxiety disorders may represent dis-inhibition due to faulty inhibitory mechanisms.

Claude Bernard and the heart-brain connection : Further elaboration of a model of neurovisceral integration

The intimate connection between the brain and the heart was enunciated by Claude Bernard over 150 years ago. In our neurovisceral integration model we have tried to build on this pioneering work. In the present paper we further elaborate our model. Specifically we review recent neuroanatomical studies that implicate inhibitory GABAergic pathways from the prefrontal cortex to the amygdala and additional inhibitory pathways between the amygdala and the sympathetic and parasympathetic medullary output neurons that modulate heart rate and thus heart rate variability. We propose that the default response to uncertainty is the threat response and may be related to the well known negativity bias. We next review the evidence on the role of vagally mediated heart rate variability (HRV) in the regulation of physiological, affective, and cognitive processes. Low HRV is a risk factor for pathophysiology and psychopathology. Finally we review recent work on the genetics of HRV and suggest that low HRV may be an endophenotype for a broad range of dysfunctions.

The role of vagal function in the risk for cardiovascular disease and mortality.

Cardiovascular disease (CVD) is the leading cause of death and disability worldwide. The understanding of the risk factors for CVD may yield important insights into the prevention, etiology, course, and treatment of this major public health concern. We review the evidence for the role of vagal function in the risk for cardiovascular disease and mortality. Using a broad range of indicators of vagal function including resting heart rate, heart rate recovery, heart rate variability, and baroreflex sensitivity we show that decreased vagal function is associated with an increased risk for morbidity and mortality. These effects are independent of traditional risk factors. Moreover, we show that decreased vagal function is associated with both traditional and emerging risk factors as well as modifiable and non-modifiable risk factors. Most importantly, we provide evidence to support the notion that decreased vagal function precedes the development of a number of risk factors and that modification of risk profiles in the direction of lower risk is associated with increased vagal function. We close with a brief overview of the neural concomitants of vagal function and suggest that a model of neurovisceral integration may provide a unifying framework within which to investigate the impact of risk factors, including psychosocial factors, on cardiovascular disease.

The Levels of Emotional Awareness Scale: a cognitive-developmental measure of emotion.

The Levels of Emotional Awareness Scale (LEAS) is based on a new cognitive-developmental model of emotional experience. The scale poses evocative interpersonal situations and elicits descriptions of the emotional responses of self and others which are scored using specific structural criteria. Forty undergraduates (20 of each sex) were tested. Interrater reliability and intratest homogeneity of the LEAS were strong. The LEAS was significantly correlated with two measures of maturity: the Washington University Sentence Completion Test (SCT) of Ego Development, and the Parental Descriptions Scale-a cognitive-developmental measure of object representation. In addition, the LEAS correlated positively with openness to experience and emotional range but not with measures of specific emotions, repression or the number of words used in the LEAS responses. These findings suggest that it is the level of emotion, not the specific quality of emotion, that is tapped by the LEAS.

Common effects of emotional valence, arousal and attention on neural activation during visual processing of pictures

Emotion and attention heighten sensitivity to visual cues. How neural activation patterns associated with emotion change as a function of the availability of attentional resources is unknown. We used positron emission tomography (PET) and 15O-water to measure brain activity in male volunteers while they viewed emotional picture sets that could be classified according to valence or arousal. Subjects simultaneously performed a distraction task that manipulated the availability of attentional resources. Twelve scan conditions were generated in a 3 x 2 x 2 factorial design involving three levels of valence (pleasant, unpleasant and neutral), two levels of arousal and two levels of attention (low and high distraction). Extrastriate visual cortical and anterior temporal areas were independently activated by emotional valence, arousal and attention. Common areas of activation derived from a conjunction analysis of these separate activations revealed extensive areas of activation in extrastriate visual cortex with a focus in right BA18 (12, -88, -2) (Z=5.73, P < 0.001 corrected) and right anterior temporal cortex BA38 (42, 14, -30) (Z=4.03, P < 0.05 corrected). These findings support an hypothesis that emotion and attention modulate both early and late stages of visual processing.

Impaired verbal and nonverbal emotion recognition in alexithymia.

Although clinical observations suggest that alexithymic individuals have a deficit in their ability to recognize emotional stimuli and that this deficit is not simply due to a problem in verbal labeling, these two hypotheses have not been empirically confirmed.Three hundred eighty participants in a community survey without current or past histories of psychiatric disorder completed two independent measures of alexithymia [the Levels of Emotional Awareness Scale (LEAS) and the Toronto Alexithymia Scale (TAS-20)] and the Perception of Affect Task (PAT), a 140-item measure of the ability to match emotion stimuli. The PAT includes four subtasks that require the subject to match verbal or nonverbal emotion stimuli with verbal or nonverbal emotion responses. The subtasks include matching sentences and words (verbal-verbal), faces and words (nonverbal-verbal), sentences and faces (verbal-nonverbal), and faces and photographs of scenes (nonverbal-nonverbal). Across the entire sample, higher (alexithymic) TAS-20 and lower LEAS scores were both correlated with lower accuracy rates on each of the subtasks of the PAT (p <.001), accounting for 10.5% and 18.4% of the variance, respectively. Fifty-one subjects met TAS-20 criteria for alexithymia. Alexithymic individuals scored lower than other subjects on purely nonverbal matching, purely verbal matching, and mixed verbal-nonverbal matching (all p <.001). These results suggest that alexithymia is associated with impaired verbal and nonverbal recognition of emotion stimuli and that the hallmark of alexithymia, a difficulty in putting emotion into words, may be a marker of a more general impairment in the capacity for emotion information processing.

Is alexithymia the emotional equivalent of blindsight

A fundamental tenet of psychosomatic medicine is that interference with the experience and expression of emotions can have an adverse affect on health (Taylor 1987). Early in this century it was observed that the onset and course of certain physical diseases were adversely affected by the repression of certain conflictual ideas and their accompanying affects (Alexander 1950). A later alternative view was that a deficit or developmental arrest in the capacity for symbolic mental representation of emotion was the core problem in patients with psychosomatic disorders, typified by a diminished ability to identify and describe feelings (Ruesch 1948). This latter view has evolved into the concept of alexithymia, a term coined by Sifneos in 1972 meaning “absence of words for emotion” (Sifneos 1972). Sifneos and Nemiah posited that the deficit in the capacity for symbolization of emotion (in verbal behavior, fantasy, and dreams) resulted in a variety of manifestations, including abnormal physiology resulting in disease, a propensity for impulsive behavior, discomfort with and avoidance of social relationships, and an impaired capacity for self-care and self-regulation (Nemiah and Sifneos 1970). Subsequent research has revealed that alexithymia is associated with a variety of other psychiatric disorders, including posttraumatic stress disorder (PTSD), substance abuse and dependence, somatization, eating disorders, and panic disorder (Taylor et al 1991; Jimerson et al 1994; Parker et al 1993). It is not known whether the manifestations of alexithymia are similar or different in these various clinical contexts. Recent research has also demonstrated that alexithymia is associated with deficits in the recognition of both verbal and nonverbal emotional stimuli (Lane et al, in press). To obtain a current consensus about the essential features of alexithymia, Haviland and Reise (1996) recently generated a prototypical description of alexithymic individuals derived from 13 experts using the Q-sort method. The results of this survey are presented in Table 1. Alexithymic individuals manifest bland or flattened affect, tend to be somatically preoccupied, express themselves through action and nonverbal behavior, are interpersonally distant, become disorganized under stress, lack imagination and insight, and tend to be socially conforming. Early descriptions of alexithymic individuals included diminished facial expressions, which have been confirmed in recent empirical work (McDonald and Prkachin 1990), but also noted occasional brief, intense, dramatic outbursts of emotion such as tearfulness that end as abruptly as they From the Department of Psychiatry (RDL, GLA, GES, AWK) and Department of Neurology (GLA, GES, AWK), University of Arizona College of Medicine, and Department of Psychology, University of Arizona (RDL, GLA, GES, AWK), Tucson, Arizona. Address reprint request to Richard D. Lane, MD, Department of Psychiatry, Arizona Health Sciences Center, 1501 N. Campbell Avenue, Tucson, AZ 85724. Received January 18, 1996.

Impaired self-awareness and theory of mind: An fMRI study of mentalizing in alexithymia

Alexithymic individuals have difficulty in recognizing and describing emotions in themselves. We investigated the neuronal basis of mentalizing in alexithymia to determine whether there is a common neuronal substrate associated with knowing the mental states of the self and others. Individuals high in alexithymia (n = 16) and low in alexithymia (n = 14) were selected from a pool of 310 college students using a combination of the Toronto Alexithymia Scale (TAS-20) and the Structured Interview version of the Beth Israel Questionnaire (SIBIQ). We compared the two groups on psychological measures, including ratings of mentalizing and the Interpersonal Reactivity Index (IRI), and regional brain activation using functional magnetic resonance imaging (fMRI) during a mentalizing animation task. The results for both groups showed activation in regions associated with mentalizing: medial prefrontal cortices (MPFC), temporo-parietal junctions (TPJ), and the temporal pole (TP). Alexithymics had lower mentalizing and IRI perspective-taking scores and less activation in the right MPFC. Activity in the MPFC was positively correlated with the mentalizing score and the IRI perspective-taking score. Although there were no group differences in cerebral activity in the TPJ and the TP, the activity in the right TP had a positive correlation with mentalizing and IRI personal distress scores. These results suggest that alexithymic individuals have an impairment in mentalizing associated with an inability to take the perspective of others. Thus, the skills involved in comprehending the self and others are inter-related and play an important role in emotion regulation.