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      Cerebral correlates of autonomic cardiovascular arousal: a functional neuroimaging investigation in humans.

      Author(s): 1 , , , ,  
      Publication date (Electronic):
      Journal: The Journal of physiology
      Publisher: Wiley

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          Abstract

          1. States of peripheral autonomic arousal accompany emotional behaviour, physical exercise and cognitive effort, and their central representation may influence decision making and the regulation of social and emotional behaviours. However, the cerebral functional neuroanatomy representing and mediating peripheral autonomic responses in humans is poorly understood. 2. Six healthy volunteer subjects underwent H215O positron emission tomography (PET) scanning while performing isometric exercise and mental arithmetic stressor tasks, and during corresponding control tasks. Mean arterial blood pressure (MAP) and heart rate (HR) were monitored during scanning. 3. Data were analysed using statistical parametric mapping (SPM99). Conjunction analyses were used to determine significant changes in regional cerebral blood flow (rCBF) during states of cardiovascular arousal common to both exercise and mental stressor tasks. 4. Exercise and mental stressor tasks, relative to their control tasks, were associated with significantly (P < 0.001) increased MAP and HR. Significant common activations (increased rCBF) were observed in cerebellar vermis, brainstem and right anterior cingulate. In both exercise and mental stress tasks, increased rCBF in cerebellar vermis, right anterior cingulate and right insula covaried with MAP; rCBF in pons, cerebellum and right insula covaried with HR. Cardiovascular arousal in both categorical and covariance analyses was associated with decreased rCBF in prefrontal and medial temporal regions. 5. Neural responses in discrete brain regions accompany peripheral cardiovascular arousal. We provide evidence for the involvement of areas previously implicated in cognitive and emotional behaviours in the representation of peripheral autonomic states, consistent with a functional organization that produces integrated cardiovascular response patterns in the service of volitional and emotional behaviours.

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          Contributions of anterior cingulate cortex to behaviour

          Orrin Devinsky, Martha J. Morrell, Brent Vogt (1995)
          Assessments of anterior cingulate cortex in experimental animals and humans have led to unifying theories of its structural organization and contributions to mammalian behaviour. The anterior cingulate cortex forms a large region around the rostrum of the corpus callosum that is termed the anterior executive region. This region has numerous projections into motor systems, however, since these projections originate from different parts of anterior cingulate cortex and because functional studies have shown that it does not have a uniform contribution to brain functions, the anterior executive region is further subdivided into 'affect' and 'cognition' components. The affect division includes areas 25, 33 and rostral area 24, and has extensive connections with the amygdala and periaqueductal grey, and parts of it project to autonomic brainstem motor nuclei. In addition to regulating autonomic and endocrine functions, it is involved in conditioned emotional learning, vocalizations associated with expressing internal states, assessments of motivational content and assigning emotional valence to internal and external stimuli, and maternal-infant interactions. The cognition division includes caudal areas 24' and 32', the cingulate motor areas in the cingulate sulcus and nociceptive cortex. The cingulate motor areas project to the spinal cord and red nucleus and have premotor functions, while the nociceptive area is engaged in both response selection and cognitively demanding information processing. The cingulate epilepsy syndrome provides important support of experimental animal and human functional imaging studies for the role of anterior cingulate cortex in movement, affect and social behaviours. Excessive cingulate activity in cases with seizures confirmed in anterior cingulate cortex with subdural electrode recordings, can impair consciousness, alter affective state and expression, and influence skeletomotor and autonomic activity. Interictally, patients with anterior cingulate cortex epilepsy often display psychopathic or sociopathic behaviours. In other clinical examples of elevated anterior cingulate cortex activity it may contribute to tics, obsessive-compulsive behaviours, and aberrent social behaviour. Conversely, reduced cingulate activity following infarcts or surgery can contribute to behavioural disorders including akinetic mutism, diminished self-awareness and depression, motor neglect and impaired motor initiation, reduced responses to pain, and aberrent social behaviour. The role of anterior cingulate cortex in pain responsiveness is suggested by cingulumotomy results and functional imaging studies during noxious somatic stimulation. The affect division of anterior cingulate cortex modulates autonomic activity and internal emotional responses, while the cognition division is engaged in response selection associated with skeletomotor activity and responses to noxious stimuli. Overall, anterior cingulate cortex appears to play a crucial role in initiation, motivation, and goal-directed behaviours.(ABSTRACT TRUNCATED AT 400 WORDS)
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            A differential neural response in the human amygdala to fearful and happy facial expressions.

            J. S. Morris, C D Frith, D. Perrett … (1996)
            The amygdala is thought to play a crucial role in emotional and social behaviour. Animal studies implicate the amygdala in both fear conditioning and face perception. In humans, lesions of the amygdala can lead to selective deficits in the recognition of fearful facial expressions and impaired fear conditioning, and direct electrical stimulation evokes fearful emotional responses. Here we report direct in vivo evidence of a differential neural response in the human amygdala to facial expressions of fear and happiness. Positron-emission tomography (PET) measures of neural activity were acquired while subjects viewed photographs of fearful or happy faces, varying systematically in emotional intensity. The neuronal response in the left amygdala was significantly greater to fearful as opposed to happy expressions. Furthermore, this response showed a significant interaction with the intensity of emotion (increasing with increasing fearfulness, decreasing with increasing happiness). The findings provide direct evidence that the human amygdala is engaged in processing the emotional salience of faces, with a specificity of response to fearful facial expressions.
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              Individuals with sociopathic behavior caused by frontal damage fail to respond autonomically to social stimuli.

              A. Damasio (1990)
              Following damage to ventromedial frontal cortices, adults with previously normal personalities develop defects in decision-making and planning that are especially revealed in an abnormal social conduct. The defect repeatedly leads to negative personal consequences. The physiopathology of this disorder is an enigma. We propose that the defect is due to an inability to activate somatic states linked to punishment and reward, that were previously experienced in association with specific social situations, and that must be reactivated in connection with anticipated outcomes of response options. During the processing that follows the perception of a social event, the experience of certain anticipated outcomes of response options would be marked by the reactivation of an appropriate somatic state. Failure to reactivate pertinent somatic markers would deprive the individual of an automatic device to signal ultimately deleterious consequences relative to responses that might nevertheless bring immediate reward (or, alternatively, signal ultimately advantageous outcomes relative to responses that might bring immediate pain). As an example, activation of somatic markers would (1) force attention to future negative consequences, permitting conscious suppression of the responses leading to them and deliberate selection of biologically advantageous responses, and (2) trigger non-conscious inhibition of response states by engagement of subcortical neurotransmitter systems linked to appetitive behaviors. An investigation of this theory in patients with frontal damage reveals that their autonomic responses to socially meaningful stimuli are indeed abnormal, suggesting that such stimuli fail to activate somatic states at the most basic level. On the contrary, elementary unconditioned stimuli (e.g. a loud noise) produce normal autonomic responses.
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                Author and article information

                Journal
                Journal ID (iso-abbrev): J Physiol
                Title: The Journal of physiology
                Publisher: Wiley
                ISSN: 0022-3751
                ISSN (Print): 0022-3751
                Publication date (Electronic): Feb 15 2000
                Volume: 523 Pt 1
                Affiliations
                [1 ] Wellcome Department of Cognitive Neurology, Institute of Neurology and Autonomic Unit, National Hospital for Neurology and Neurosurgery, Institute of Neurology, University College London, Queen Square, London, UK. hugo@fil.ion.ucl.ac.uk
                Article
                Publisher Item ID: PHY_9838
                DOI: 10.1111/j.1469-7793.2000.t01-1-00259.x
                PMC ID: 2269796
                PubMed ID: 10673560
                SO-VID: f2709d44-3169-4072-9c33-ee0d250d1430
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