How do you feel — now? The anterior insula and human awareness

PersPectivesBox 5 | Future research questions following from the modelWhat are the anatomical connections of the anterior insular cortex (AIC)? Modern imaging studiesusing diffusion spectrum imaging and functional and effective connectivity analyses are neededthat incorporate the AIC’s dynamic connectivity 83 . Comprehensive analysis of the hodology of themacaque insular cortex using classic tract-tracing methods is also needed.How do the two sides of the AIC differ, and how do they interact? Does one side lead 48 and theother side monitor 23,48 at different times? Direct statistical comparisons of laterality in activationare needed. Advanced analyses based on demonstrated asymmetries (FIG. 2) can be designed; forexample, one could examine changes in activation patterns and effective connectivity during themodulation of pain by pleasant music 112 .Is there one somatotopic map that provides a common-resource pool of ‘global emotionalmoments’, represents all feelings and is dynamically accessed at each moment? Or are therenumerous modules in the AIC that are coordinated to represent different feelings at each globalemotional moment? For example, evidence suggests that the eyes and the face are represented inthe anterior ventral AIC and that the hand and the foot are represented more posteriorly, which isconsistent with the presence of one map; however, the somatotopy in the one study that includedstimulation of multiple body parts is reversed 10 .Similarly, is there only one module in each AIC that represents time, as suggested by the tinyareas of activation in the AIC found in one study 34 ? And does the activity in these areas correlatewith subjective time dilation? Are these areas asymmetric on the two sides with respect to thecontrasting effects of arousal and pleasant mood on time perception 113 ?How are comparisons made between feelings at different points in time? Where are theintermediate ‘meta-memory’ buffers and how are they interconnected?The neuropsychological construct called a ‘feeling’ is crucial. Why is it important that thisconstruct has a homeostatic basis? What do feelings from the body and feelings about objects orpeople or cognitions have in common? Do all feelings have autonomic sequelae — that is, do they‘move the heart’? Can every thought be regarded as a feeling? Are feelings indeed the commoncurrency of awareness?Does emotional congruence between individuals reflect homeostatic resonance?Do elephants really make infrasonic music together? What about whales?Infants do not pass the mirror test or show self-conscious behaviours until they are ~18 monthsold 50,53 . Does the connectivity of their AIC and anterior cingulate cortex (ACC) show a similardevelopmental threshold?The activation of the AIC or the ACC has been used for biofeedback training. Could thisapplication be refined in light of the considerations set out in this article?— and that each stage would have beeneasily realizable by evolutionaryneuroanatomical modifications.Implications and future directionsIt is fascinating that the proposed model forawareness in the AIC produces an emergentbasis for the uniquely human facultyof music: viewed as the rhythmic temporalprogression of emotionally laden moments,music arises as a natural concomitant of thisstructural model. The engagement of theAIC by emotional feelings, by the feeling ofmovement and by the sense of time encouragesthe view that this model can explain theobserved activation of the AIC by rhythm 16and by musical enjoyment 17 , as well as theprimal emotional effects of communalmusic­making, because music wouldinherently involve the core of awareness.This model also suggests a mechanismfor the subjective time dilation, or slowing oftime, that occurs during an intensely emotionalperiod 81 . A high rate of salience accumulationwould ‘fill up’ global emotionalmoments quickly, because the informationcapacity of the neural instantiation of a globalemotional moment must be finite. Thus,the endogenous timebase would effectivelyspeed up during such a period (FIG. 3b) and,consequently, time would appear to standstill to the ‘observer’. Psychophysical datafrom rapid­visual­search studies suggestthat the maximal rate of passage of individualmoments is ~8 Hz 31 . A similar processfor the recruitment of global emotionalmoments could provide the basis for ‘heightenedawareness’ of the immediate momentand for the enhanced activation of the AICthat is associated with such moments.In this model, the close integrationbetween the AIC and the ACC implies thatactivity in the AIC can incorporate the urgesof the volitional agent that is representedin the ACC, and also that feelings in theAIC can be modulated by that agent 82 , sothat each global emotional moment comprisesboth feelings and motivations (BOX 1).Indeed, the representation in the sentientself of the active behavioural agent (the ‘I’)fills a gap in the ‘somatic marker’ hypothesis51 and challenges a main criticism ofthe James–Lange theory 51 , namely that thetheory did not allow for feelings of internallygenerated emotion. In the model presentedin this article, all stimuli, incentives, intentionsand cognitions that have salience arerepresented by feelings, a crucial neuropsychologicalconstruct composed of nested setsof integrative associations that are elaboratedon an interoceptive template and endowedwith characteristic homeostatic sequelae(and thus, all feelings ‘move the heart’). Inthis model, feelings are the computationalcommon currency of awareness 59,60 .Finally, this model includes the possibilitythat emotional behaviours can occur withoutawareness (that is, by activation of the ACCwithout integration in the AIC), it impliesthat animals without these structures are notaware in the same way that we are (BOX 2)and it provides a ready basis for the inclusionof a module that would assign responsibilityfor the behavioural agent’s actions to thesentient self 64 .It is important to note this model’s currentlimitations. It does not explain howa feeling is constructed, the nature of thetimebase and its relation to homeostaticactivity (such as one’s heartbeat), the mechanismfor shifting moments across time, theneural metric of salience, the differentiationof emotions, the necessary dynamic connectivityof global emotional moments 83 orthe integration between the two sides of theAIC (BOX 3). It does not specify the locationof memories of past feelings or the locationof the internal behavioural models thatproduce anticipatory feelings. The evidencereviewed above suggests that the final representationof the sentient self in the AIC mayconsist of one coherent somatotopic mapthat has sufficiently global characteristicsand dynamic connectivity to encompassall possible feelings, but few studies havecompared different emotions and differentbody­part associations. It is even difficultto systematically predict how lesions of theAIC and the ACC should differ in terms oftheir effects considering their intimate connectivity(for example, see the contrastingresults in the literature on alexithymia 70–72 ). Ilook forward particularly to the future identificationof the various functional modulesin the AIC and the characteristics and the‘language’ of VENs. There are many otherquestions that need to be addressed, some ofwhich are listed in BOX 5.A. D. (Bud) Craig is at the Atkinson ResearchLaboratory, Barrow Neurological Institute, Phoenix,Arizona 85013, USA.e-mail: bcraig@chw.edudoi:10.1038/nrn255568 | JANuARy 2009 | VOLuME 10 www.nature.com/reviews/neuro© 2009 Macmillan Publishers Limited. All rights reserved