Somatic salience in persistent depression

A clear implication arising from the current findings relates to the utility of somatic stimuli in the study of persistent depression. In all three studies indexing attentional capture, somatic stimuli differentiated the performance of depressed individuals from that of controls, indicating that such stimuli succeeded in capturing some attribute specific to bodily information processing in this population. It is possible, tentatively, to suggest on this basis that somatic stimuli may be capable of providing a relatively tractable analogue for the study of interoceptive processing in depressive disorders. Alternatively, somatic processing may prove to be subject to the influence of depression entirely independently of any such influence on interoceptive processing; but if this is the case then the findings presented here suggest that it may be important to investigate somatic processing in persistent depression in its own right. Much work remains to be done in identifying the nature of the relationships between depression, somatosensation and interoception, but the current studies go some way towards establishing the relevance of somatosensation to the study of bodily awareness and precision in depression.

Existing formulations of disturbed somatic processes in depression posit an attenuation of somatic experience (e.g., Bylsma et al., 2008), although the self-reports of depressed individuals demonstrate that at least some forms of unpleasant somatic experience can be highly salient during depressive episodes (Ratcliffe, 2014). While a disturbance of somatic awareness was evident in all three studies of attentional capture, the natures of these respective disturbances provide somewhat different insights.

In Study 4, the instruction to ignore salient but irrelevant somatic cues seems to have precipitated a significant reduction of general attentional efficiency in depressed individuals. Although discussion of the cognitive or neurological mechanisms which may underlie this effect is speculative, a substantial and potentially relevant literature exists which relates similar patterns of reduced attentional efficiency to activity in the default mode network (DMN) of the brain (Kelly et al., 2008; Sonuga-Barke & Castellanos, 2007; Weissman et al., 2006). The DMN is known to be active during rest and ‘mind-

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wandering’ (e.g., Schooler et al., 2011), and deactivated in response to attentional demands, operating in opposition to a task-positive brain network (TPN) which mediates focused attention (Fox et al., 2005). Attentional lapses, as indexed by lengthy and variable reaction times (Weissman et al., 2006) and errors (Eichele et al., 2008; Li, Yan, Bergquist, & Sinha, 2007) during a variety of tasks have been associated with reduced DMN deactivation, while intra-individual variability in response times during an attention task has also been shown in healthy participants to relate to the strength of anticorrelations between the DMN and the TPN (Kelly et al., 2008). Such findings suggest that consistent attentional performance may depend upon efficient DMN deactivation, implying that DMN dysregulation could underlie inconsistent performance such as that observed in depressed participants in Study 4. It is well-established that abnormal patterns of intra-and extra-network resting-state functional connectivity can operate with respect to the DMN in depression (Kaiser, Andrews-Hanna, Wager, & Pizzagalli, 2015; Mulders, van Eijndhoven, Schene, Beckmann, & Tendolkar, 2015), and functional imaging studies have further demonstrated that depressed groups can be characterised by reduced DMN deactivation during focused attention, certainly when emotionally relevant stimuli are involved (Grimm et al., 2009; Sheline et al., 2009). It is plausible, therefore, that reductions in attentional efficiency in response to somatic cues could reflect reduced DMN deactivation under these conditions in depressed participants. It is possible to speculate further that an association of unwanted somatic stimuli with threat or emotion in individuals with persistent or recurrent histories of depression could exacerbate failures of DMN deactivation during blocks in which irrelevant cues are somatic, accounting for the greater response variability in these blocks.

An alternative account suggests that high response variability in the depressed group could result from peristimulus efforts to refocus attention centrally in the attempt to ignore cues as instructed. It may be the case that relative difficulty in optimising target precision at the expense of the precision of irrelevant cues, as suggested by the outcomes of the Study 6 computational model, could motivate the use of a clumsier strategy of endogenous attentional shifts among depressed participants. Heightened response variability following somatic cues would then indicate greater difficulty in ignoring such cues and more vigorous resulting efforts to endogenously control the locus of attention. Participants were not asked to provide any information about the cognitive strategies that they had used during the task and so further explication of this finding must await additional research.

In Study 5, on the other hand, participants were not instructed to ignore the cues, and cues were on average predictive of target location. Under these circumstances, no significant reductions in overall attentional efficiency were observed, but there was instead a depression-specific exacerbation of validity effects with respect to somatic cues. This finding suggests that attention within the depressed

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group was disproportionately captured by such cues, consistent with the hypothesis that the salience of somatic sensation may be amplified in persistent depression rather than attenuated. There is a well- documented and often disabling impact of somatic symptomatology in persistent depression (Ratcliffe, 2014; Vaccarino et al., 2008); and increased attentional capture by somatic signals may reflect their heightened salience in this population as a result of their frequently threatening or problematic nature. The proposed increase in the salience, or threat value, of somatic signals in persistent depression is also consistent with the proposal that they may be disproportionately likely to trigger cognitive avoidance or control strategies.

Both Studies 4 and 5 suggest, therefore, that somatic cues were associated with stronger salience for depressed participants, relative to auditory cues. Additional support for this proposal is provided by the estimated bottom-up stimulus salience parameters in the Study 6 computational model. Specifically, in Study 6, the model outcomes suggested that depressed participants found somatic stimuli disproportionately salient in comparison to controls, while the opposite pattern was observed for auditory stimuli. The finding that somatic cues are uniquely distracting or salient for depressed participants is thus consistent across all three studies, but requires some explanation, particularly given a body of literature indicating reduced bodily awareness in depressive disorders (Dunn et al., 2007; Dunn, Stefanovitch, et al., 2010; Furman et al., 2013; Harshaw, 2015). The regression analysis undertaken in Study 6 with respect to relative somatic salience suggested that (at least) two mechanisms contributed to this outcome: first, an index of physiological anxiety symptom severity predicted relative somatic salience, suggesting, perhaps uncontroversially, that more anxious individuals are likely to find bodily signals more salient. Given that depressed participants were by definition more likely to be anxious than healthy controls, this accounts in part for the group difference. Secondly, an index of interoceptive sensibility (self-reported interoceptive awareness) was negatively associated with relative somatic salience, suggesting that individuals who reported less awareness of interoceptive sensation day-to-day were more surprised (in a Bayesian sense) by somatic stimuli in our task. Because depressed participants reported reduced interoceptive sensibility relative to controls, this relationship also contributed to the group difference. It is possible that increased surprise at novel bodily sensations can result from habitual downregulation of interoceptive and other bodily signals, an explanation which can accommodate both the increased salience of the novel stimuli employed in the current studies, and the reduced salience of endogenously-occurring interoceptive signals such as heartbeats observed in tasks indexing interoceptive awareness (Dunn et al., 2007; Furman et al., 2013). Alternatively, higher salience of unwanted bodily signals may motivate more habitual cognitive and behavioural avoidance of such signals (e.g., Borkovec & Lyonfields, 1993; Hayes,

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Wilson, Gifford, Follette, & Strosahl, 1996; Moore & Garland, 2004), reflected in lower interoceptive sensibility. A more targeted approach, employing a wider range of interoceptive measures (Garfinkel et al., 2015), is needed to investigate this question further.

In theoretical terms, our finding that somatic stimuli are disproportionately salient in the context of attenuated generic sensory precision is broadly consistent with proposals by Paulus and Stein (2010) that bodily signals are both noisy and amplified in depressive disorders. The relative salience of somatic signals may also relate to clinical observations regarding the ubiquity of motivated and explicit attempts to downregulate interoceptive experience in anxiety and depression, in contrast to the more implicit mechanisms involved in the reduced precision of signals occurring in other sensory modalities. For example, while attention to sensory information of all kinds may be constrained or attenuated in depression in order to reduce energy expenditure or to regulate arousal, the disproportionate salience or threat of somatic signals may render this process more difficult, necessitating the employment of additional, more explicit emotional avoidance strategies. Studies employing dynamic causal modelling could be of great utility in developing our understanding of these processes.