From hidden springs to endless oceans: exploring the complementary roles of the amygdala and hippocampus in phenomenal experience

Abstract Current theories of consciousness often emphasize its ego-centric functions, highlighting the role of the insular cortex in interoceptive self-modeling and subcortical brain regions in qualitative experience and motivation, aptly described as the ‘hidden spring’ of consciousness. From ecological and pragmatic perspectives, conscious experience may facilitate the self-organization of complex organisms by optimizing goals that are typically parallel, multifaceted, and difficult to reconcile. However, the notion that all forms of conscious experience are ego-centric, or at least grounded in a minimal sense of self, is challenged by credible reports of minimal phenomenal experience (MPE), which occur without any self-referential content. I propose that this apparent duality in conscious experience can be explained by the dual-origin theory of cortical development. This theory suggests a gradual expansion of cortical cytoarchitecture from two distinct subcortical origins. The ‘Amygdala-System’ supports interoceptive self-modeling for habitual interactions with the body and the environment. It expands ventrally from the olfactory system and amygdala, enabling ego-centric processing. In contrast, the ‘Hippocampus-System’, centered on the hippocampus and expanding dorsally, supports allocentric cognition and experiences that are not constrained by self-referential processing. This complementary system allows for open-ended, selfless forms of experience, akin to an ‘endless ocean’. In this framework, MPE may represent a fragile form of consciousness, typically overshadowed by the self-related interoceptive and exteroceptive functions of the Amygdala-System. Finally, I discuss how real-time functional magnetic resonance imaging (fMRI) neurofeedback could be used to upregulate the Hippocampus-System, potentially enabling the controlled study of MPE in neuroscientific settings. Highlights Evidence from developmental neuroanatomy suggests two different subcortical origins of the mammalian cerebral cortex, potentially entailing two modes of conscious experience. An amygdala-centered developmental gradient could allow for ego-centric functions relevant for adaptive self-regulation including survival in a physical and social world. A hippocampus-centered system could allow for allo-centric world modeling, which is less constrained by an ego-centric perspective. Several hypotheses are proposed to investigate the neuroanatomical and phenomenological claims by using real-time functional MRI-based neurofeedback in a controlled experimental setting.