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Feeling, learning from and being aware of inner states: interoceptive dimensions in neurodegeneration and stroke
Abstract
Interoception is a complex process encompassing multiple dimensions, such as accuracy, learning and awareness. Here, we examined whether each of those dimensions relies on specialized neural regions distributed throughout the vast interoceptive network. To this end, we obtained relevant measures of cardiac interoception in healthy subjects and patients offering contrastive lesion models of neurodegeneration and focal brain damage: behavioural variant fronto-temporal dementia (bvFTD), Alzheimer's disease (AD) and fronto-insular stroke. Neural correlates of the three dimensions were examined through structural and functional resting-state imaging, and online measurements of the heart-evoked potential (HEP). The three patient groups presented deficits in interoceptive accuracy, associated with insular damage, connectivity alterations and abnormal HEP modulations. Interoceptive learning was differentially impaired in AD patients, evidencing a key role of memory networks in this skill. Interoceptive awareness results showed that bvFTD and AD patients overestimated their performance; this pattern was related to abnormalities in anterior regions and associated networks sub-serving metacognitive processes, and probably linked to well-established insight deficits in dementia. Our findings indicate how damage to specific hubs in a broad fronto-temporo-insular network differentially compromises interoceptive dimensions, and how such disturbances affect widespread connections beyond those critical hubs. This is the first study in which a multiple lesion model reveals fine-grained alterations of body sensing, offering new theoretical insights into neuroanatomical foundations of interoceptive dimensions.
This article is part of the themed issue ‘Interoception beyond homeostasis: affect, cognition and mental health’.
1. Introduction
Interoception is the ability to sense autonomic changes via viscero-cortical pathways [1,2]. While research on this domain has greatly illuminated normal [3] and pathological [4,5] processes, it has not fully exploited the possibilities of the lesion model approach, which allows establishing direct connections between brain lesions and behaviour [6,7]. By including two contrastive lesion models, such as focal stroke and early neurodegeneration [8,9], we aim to reveal critical links between affected brain regions and interoceptive performance. To this end, we measured behavioural, neuroimaging, and electrophysiological correlates of cardiac interoception in patients with behavioural variant fronto-temporal dementia (bvFTD, a condition with early compromise of fronto-insular-temporal structures), early stage Alzheimer's disease (AD, which includes posterior and temporal atrophy), and fronto-insular stroke (FIS). Such conditions may offer novel insights into interoception, because relevant evidence is scant in neurological disorders, and null in dementias.
Cardiac interoception tasks, which assess sensing of one's own heartbeats [5,10,11], offer robust evidence on three relevant dimensions: accuracy (behavioural precision in tracking cardiac signals [3]), learning (improvement of behavioural accuracy after feedback [11]), and awareness (metacognitive processes underlying confidence about one's own performance [3]). These dimensions rely on distributed networks critically engaging the insular cortex (IC), the anterior cingulate cortex (ACC) and the somatosensory cortex (SC) [2,12], while interactions between interoceptive and high-level functions are mediated by IC projections to the ACC, the orbitofrontal cortex (OFC), the amygdala and the hippocampus (HP) [3,4,11,13–18].
First, as shown in structural and functional studies on interoceptive accuracy, task precision and online performance are associated with IC, ACC and SC hubs [12]. Additionally, the heart-evoked potential (HEP) is a cortical marker of cardiac monitoring which is modulated by attention to one's own heartbeats (expressed by a negative deflection that peaks in a 200–500 ms window after the R-wave) [19,20], and is mainly originated in the IC and the ACC [1,2,12]. HEP modulation amplitude is larger in subjects with high interoceptive accuracy [11,19,21,22] and could be enhanced by training [23]. In addition, the HEP is attenuated in neuropsychiatric patients [20] and such an alteration is associated with interoceptive deficits [5,17,18]. Moreover, phasic signals from individual heartbeats are related to memory circuits [24]. As all such mechanisms are to some extent compromised in our three patient groups, we hypothesized they would all present impairments in interoceptive accuracy and associated cortical measures.
Second, regarding interoceptive learning, cortical and intracranial recordings show that post-feedback behavioural improvements are associated with activity modulations in the IC and the frontal cortex [11]. However, whole-brain neuroimaging analyses may reveal other regions related to impairments in this dimension. Specifically, the crucial role of the HP, adjacent temporal structures and frontal cortices in memory and learning [25] suggests that such a skill should be distinctively compromised in AD patients, as reported in many other domains.
Finally, interoceptive awareness has been associated with the ACC, IC, prefrontal cortex (PFC, Brodmann area 10 (BA10) [26,27]) and OFC [28,29]. Although this metacognitive dimension has not been examined in neurological populations, impaired awareness and diminished insight are core features of dementia [30,31]. Thus, we predicted that bvFTD and AD would be worse than controls at estimating self-performance.
Previous evidence aligns with the notion of brain hubs as a biologically costly anatomical structure, which supports higher communication rates and information processing [32]. Given the elevated metabolic rate and centrality of hubs, damage to them could disrupt important functional networks, causing both general deficits in cognitive functions and specific brain disorders [32,33]. The differential compromise of hubs in our samples (temporal and posterior in AD, fronto-insular, in FIS, and fronto-temporal in bvFTD) offers a unique opportunity to dissociate brain networks within interoception.
In sum, for interoceptive accuracy, bvFTD and FIS are expected to perform worse than controls due to damage of critical interoceptive regions; instead, for AD, we predicted that performance would depend on the extent of atrophy of the IC and other subsidiary areas that could support this process (e.g. HP). Interoceptive learning should be impaired only in AD as a result of degeneration of the HP and adjacent temporal structures. Damage to these regions, together with frontal-related areas (OFC) that play a key role in learning and memory processes, could distinctively compromise this dimension. Regarding interoceptive awareness, we hypothesized that both patient groups with dementia would estimate self-performance worse than controls as a result of reduced insight and impaired metacognition, mainly associated with fronto-temporal damage. Finally, we expected the disruption of interoceptive networks to extend beyond critical areas, also compromising relevant long-range connections. To our knowledge, this is the first study to assess the structural, functional and dynamical brain signatures of interoceptive dimensions by comparing differential lesion models of neurodegeneration and focal stroke.
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