Interaction between decision-making and interoceptive representations of bodily arousal in frontal cortex

Decision-making and representations of arousal are intimately linked. Behavioral investigations have classically shown that either too little or too much bodily arousal is detrimental to decision-making, indicating that there is an inverted “U” relationship between bodily arousal and performance. How these processes interact at the level of single neurons as well as the neural circuits involved are unclear. Here we recorded neural activity from orbitofrontal cortex (OFC) and dorsal anterior cingulate cortex (dACC) of macaque monkeys while they made reward-guided decisions. Heart rate (HR) was also recorded and used as a proxy for bodily arousal. Recordings were made both before and after subjects received excitotoxic lesions of the bilateral amygdala. In intact monkeys, higher HR facilitated reaction times (RTs). Concurrently, a set of neurons in OFC and dACC selectively encoded trial-by-trial variations in HR independent of reward value. After amygdala lesions, HR increased, and the relationship between HR and RTs was altered. Concurrent with this change, there was an increase in the proportion of dACC neurons encoding HR. Applying a population-coding analysis, we show that after bilateral amygdala lesions, the balance of encoding in dACC is skewed away from signaling either reward value or choice direction toward HR coding around the time that choices are made. Taken together, the present results provide insight into how bodily arousal and decision-making are signaled in frontal cortex.

Interaction between decision-making and interoceptive representations of bodily arousal in frontal cortex

Decision-making and representations of arousal are intimately linked. Behavioral investigations have classically shown that either too little or too much bodily arousal is detrimental to decision-making, indicating that there is an inverted ‘U’ relationship between bodily arousal and performance. How these processes interact at the level of single neurons as well as the neural circuits involved are unclear. Here we recorded neural activity from orbitofrontal cortex (OFC) and dorsal anterior cingulate cortex (dACC) of macaque monkeys while they made reward-guided decisions. Heart rate (HR) was also recorded as a proxy for bodily arousal. Recordings were made both before and after subjects received excitotoxic lesions of the bilateral amygdala. In intact monkeys, higher HR facilitated reaction times (RTs). Concurrently, a set of neurons in OFC and dACC selectively encoded trial-by-trial variations in HR independent of reward value. After amygdala lesions, HR increased and the relationship between HR and RTs was reversed. Concurrent with this change, there was an increase in the proportion of dACC neurons encoding HR. Applying a novel population-coding analysis, we show that bilateral amygdala lesions skew the balance of encoding in dACC away from signaling either reward value or choice direction towards HR coding around the time that choices are made. Taken together, the present results provide insight into how bodily arousal and decision-making are signaled in frontal cortex. Our findings may shed light on the neural mechanisms underlying some psychiatric disorders linked to amygdala dysfunction that are characterized by heightened arousal and deficits in decision-making.Significance statementHow bodily arousal states influence decision-making has been a central question in psychology, but the neural mechanisms are unclear. We recorded heart rate, a measure of bodily arousal, while simultaneously monitoring neural activity in orbitofrontal cortex (OFC) and dorsal anterior cingulate cortex (dACC) of macaques making reward-guided decisions. In intact macaques higher HR was associated with shorter reaction times. Concurrently, the activity of a set of neurons in OFC and dACC selectively encoded HR. Following amygdala lesions, HR generally increased and now the relationship between HR and reaction times was reversed. At the neural level, the balance of encoding in dACC shifted towards signaling HR, suggesting a specific mechanism through which arousal influences decision-making.

Interoception and emotion: Shared mechanisms and clinical implications

Internal states of bodily arousal contribute to emotional feeling states and behaviors. This chapter details the influence of interoceptive processing on emotion and describes how deficits in interoceptive ability may underpin aberrant emotional processes characteristic of clinical conditions. The representation and control of bodily physiology (e.g. heart rate and blood pressure) and the encoding of emotional experience and behavior share neural substrates within forebrain regions coupled to ascending neuromodulatory systems. This functional architecture provides a basis for dynamic embodiment of emotion. This chapter will approach the relationship between interoception and emotion within the interoceptive predictive processing framework and describe how emotional states could be the product of interoceptive prediction error minimization.

On the Complex Emotion: Be Physiological, Cognitive or Situated?

The topic emotion in traditional philosophy is discussed fragmentarily. And in recent years, there are two important approaches to analyze emotions, namely neo-Jamesianism and cognitive theory of emotion. Neo-Jamesians identify emotions with states of bodily arousal, which is determined by the nerve and occurs because of the feelings of bodily changes. And the cognitivists identify emotions with representations of evaluative judgments, which is regarded as propositional content accepted or affirmed by their subjects. Besides, the situated theory suggests we should expand our attention to the cultural and social environment in which emotions are moulded.

A Pragmatic View of Disturbed Self-Reflection in Personality Disorders: Implications for Psychotherapy

Patients with personality disorders suffer from impairment in self-reflective capacities. This is not a matter of making incorrect judgments about self-experience but reflects problems with (a) labeling internal experience consistent with the type and level of bodily arousal, (b) seeing how thoughts and feelings are connected to one another within the flow of daily life, and (c) realizing that one's own ideas about interpersonal relationships are subjective and fallible and not direct perceptions of external reality. The authors offer a discussion and definition of each of these three impairments and then offer suggestions for how to address these impairments in psychotherapy.