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Berntson1 - European Journal of Neuroscience Vol 18 pp...

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REVIEW ARTICLE Ascending visceral regulation of cortical affective information processing Gary G. Berntson, 1 Martin Sarter 1 and John T. Cacioppo 2 1 The Ohio State University, 1885 Neil Avenue, Columbus, OH 43210, USA 2 The University of Chicago, 5848 S. University Avenue, Chicago, IL 60637, USA Keywords : acetylcholine, amygdala, anxiety, basal forebrain, memory, visceral afference Abstract Over a century ago, William James proposed that strong emotions represent the perceptual consequences of somato-visceral feedback. Although the strong form of this conception is no longer viable, considerable evidence has accumulated indicating a range of visceral in¯uences on higher neurobehavioural processes. This literature has only recently begun to consolidate, because earlier reports generally remained at the demonstration level, and pathways and mechanisms for such in¯uences were uncertain. Recently, speci®c effects of visceral feedback have become apparent on cortical activity, cerebral auditory-evoked responses, anxiety, memory and behavioural aspects of immunological sickness. Moreover, considerable progress has been made recently in determining the speci®c neural pathways and systems underlying these actions, especially the role of noradrenergic projections from the nucleus of the tractus solitarius and the locus coeruleus to the amygdala in memory processes, and to the basal forebrain in the processing of anxiety- related information. The present paper highlights selected recent ®ndings in this area, and outlines relevant structures and pathways involved in the ascending visceral in¯uence on higher neurobehavioural processes. Introduction Contemporary neurobehavioural models often emphasize top-down in¯uences from rostral neural systems onto lower effector mechan- isms. Since William James (1884) proposed that certain emotions may represent the perceptual consequence of somatovisceral feedback, however, there has been also a growing recognition of the importance of ascending, bottom-up in¯uences on higher neural substrates. Although variations of the James concept continue to have proponents (Ekman et al ., 1983; Damasio, 2003), neither the original conception nor these variations are strongly supported by the extant data. Con- siderable evidence has accumulated, however, indicating a range of visceral in¯uences on higher neurobehavioural processes (Cameron, 2002; Morris, 2002). This literature has only recently begun to consolidate, because earlier reports generally remained at the demon- stration level, and pathways and mechanisms for such in¯uences were uncertain. Recently, speci®c effects of visceral feedback have become apparent on cortical activity (Berntson et al ., 2002), cerebral auditory- evoked responses (Berntson et al ., 2003), anxiety (Berntson et al ., 1998), memory (Williams & Clayton, 2001; McGaugh, 2002) and the immunological sickness response (see Romanovsky, 2002; the rest of the special issue of Autonomic Neuroscience). Moreover, considerable progress has been made in determining the speci®c neural pathways
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