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. 2023 Apr 14;13(3):20220076.
doi: 10.1098/rsfs.2022.0076. eCollection 2023 Jun 6.

As without, so within: how the brain's temporo-spatial alignment to the environment shapes consciousness

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As without, so within: how the brain's temporo-spatial alignment to the environment shapes consciousness

Georg Northoff et al. Interface Focus. .

Abstract

Consciousness is constituted by a structure that includes contents as foreground and the environment as background. This structural relation between the experiential foreground and background presupposes a relationship between the brain and the environment, often neglected in theories of consciousness. The temporo-spatial theory of consciousness addresses the brain-environment relation by a concept labelled 'temporo-spatial alignment'. Briefly, temporo-spatial alignment refers to the brain's neuronal activity's interaction with and adaption to interoceptive bodily and exteroceptive environmental stimuli, including their symmetry as key for consciousness. Combining theory and empirical data, this article attempts to demonstrate the yet unclear neuro-phenomenal mechanisms of temporo-spatial alignment. First, we suggest three neuronal layers of the brain's temporo-spatial alignment to the environment. These neuronal layers span across a continuum from longer to shorter timescales. (i) The background layer comprises longer and more powerful timescales mediating topographic-dynamic similarities between different subjects' brains. (ii) The intermediate layer includes a mixture of medium-scaled timescales allowing for stochastic matching between environmental inputs and neuronal activity through the brain's intrinsic neuronal timescales and temporal receptive windows. (iii) The foreground layer comprises shorter and less powerful timescales for neuronal entrainment of stimuli temporal onset through neuronal phase shifting and resetting. Second, we elaborate on how the three neuronal layers of temporo-spatial alignment correspond to their respective phenomenal layers of consciousness. (i) The inter-subjectively shared contextual background of consciousness. (ii) An intermediate layer that mediates the relationship between different contents of consciousness. (iii) A foreground layer that includes specific fast-changing contents of consciousness. Overall, temporo-spatial alignment may provide a mechanism whose different neuronal layers modulate corresponding phenomenal layers of consciousness. Temporo-spatial alignment can provide a bridging principle for linking physical-energetic (free energy), dynamic (symmetry), neuronal (three layers of distinct time-space scales) and phenomenal (form featured by background-intermediate-foreground) mechanisms of consciousness.

Keywords: consciousness; spatio-temporal neuroscience; temporo-spatial dynamics.

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Conflict of interest statement

We declare we have no competing interests.

Figures

Figure 1.
Figure 1.
Temporo-spatial alignment between environment and brain in a three-layer model. Alignment describes the interaction of the brain's ongoing spontaneous activity with interoceptive bodily and exteroceptive environmental stimuli. The (1) background layer refers to inter-individually shared cortical topography and neuronal dynamics of low-frequency high-amplitude timescales. The (2) intermediate layer refers to a stochastic alignment of INT to environmental dynamics measurable by stimuli- or task-related TRWs. Finally, the (3) foreground layer of high-frequency low-amplitude timescales considers entrainment as phase-locking of neuronal activity by exteroceptive and interoceptive stimuli.
Figure 2.
Figure 2.
ISC of the BOLD time-series standard deviation (s.d.) in the resting state. (a) Variability of the spontaneous BOLD signal measured in 360 regions across 974 subjects on days one and two. (b) Spatial or topographic correlation of the BOLD s.d. between days one and two. (c) Statistical comparison between regional differences into three groups: low, mid and highly shared s.d. The accompanying boxplots display the difference between the three group-based regions. (d) s.d. topography at the single subject level. The mean s.d. correlation between days one and two across all subjects yielded a high Pearson correlation (r = 0.84). The correlation of each subject's s.d. topography to the rest of the group on both days yielded high Pearson correlations (day 1: r = 0.74; day 2: r = 0.74). Finally, the correlation between the topography of each subject to every other subject yielded moderate results (day 1: r = 0.56; day 2: r = 0.55).
Figure 3.
Figure 3.
The background layer is constituted by low-frequency high-amplitude timescales. These long timescales show a high degree of inter-individual overlap across the brain's topography in rest and task states. The background layer thus provides a common shared ground between subjects for alignment with the social and natural world.
Figure 4.
Figure 4.
The intermediate layer provides stochastic alignment by modulating a repertoire of the brain's INT, measured in the resting state, to a range of environmental dynamics resulting in TRWs, measured in naturalistic stimuli paradigms.
Figure 5.
Figure 5.
The foreground layer focuses on fast timescales (high-frequency low-amplitude) by stimulus- or task-evoked activity. Interoceptive bodily and exteroceptive environmental stimuli can entrain the brain's neuronal activity by phase-locking the intrinsic spontaneous activity's oscillatory phase angles to the extrinsic stimuli's oscillations, establishing alignment on rapid timescales.
Figure 6.
Figure 6.
The summary of the three-layer organization displays temporo-spatial alignment starting from environmental stimuli or inputs over the interaction with the three layers of the neuronal activity's ongoing spontaneous activity to stimulus-induced activity associated with the contents of consciousness.

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References

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