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A three-dimensional model of neural activity and phenomenal-behavioral patterns

Abstract

How phenomenal experience and behavior are related to neural activity in physiology and psychopathology represents a fundamental question in neuroscience and psychiatry. The phenomenal-behavior patterns may be deconstructed into basic dimensions, i.e., psychomotricity, affectivity, and thought, which might have distinct neural correlates. This work provides a data overview on the relationship of these phenomenal-behavioral dimensions with brain activity across physiological and pathological conditions (including major depressive disorder, bipolar disorder, schizophrenia, attention-deficit/hyperactivity disorder, anxiety disorders, addictive disorders, Parkinson’s disease, Tourette syndrome, Alzheimer’s disease, and frontotemporal dementia). Accordingly, we propose a three-dimensional model of neural activity and phenomenal-behavioral patterns. In this model, neural activity is organized into distinct units in accordance with connectivity patterns and related input/output processing, manifesting in the different phenomenal-behavioral dimensions. (1) An external neural unit, which involves the sensorimotor circuit/brain’s sensorimotor network and is connected with the external environment, processes external inputs/outputs, manifesting in the psychomotor dimension (processing of exteroception/somatomotor activity). External unit hyperactivity manifests in psychomotor excitation (hyperactivity/hyperkinesia/catatonia), while external unit hypoactivity manifests in psychomotor inhibition (retardation/hypokinesia/catatonia). (2) An internal neural unit, which involves the interoceptive-autonomic circuit/brain’s salience network and is connected with the internal/body environment, processes internal inputs/outputs, manifesting in the affective dimension (processing of interoception/autonomic activity). Internal unit hyperactivity manifests in affective excitation (anxiety/dysphoria-euphoria/panic), while internal unit hypoactivity manifests in affective inhibition (anhedonia/apathy/depersonalization). (3) An associative neural unit, which involves the brain’s associative areas/default-mode network and is connected with the external/internal units (but not with the environment), processes associative inputs/outputs, manifesting in the thought dimension (processing of ideas). Associative unit hyperactivity manifests in thought excitation (mind-wandering/repetitive thinking/psychosis), while associative unit hypoactivity manifests in thought inhibition (inattention/cognitive deficit/consciousness loss). Finally, these neural units interplay and dynamically combine into various neural states, resulting in the complex phenomenal experience and behavior across physiology and neuropsychiatric disorders.

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Fig. 1: Three-dimensional model of neural activity and phenomenal-behavioral patterns—Neural units and phenomenal-behavioral dimensions.
Fig. 2: Three-dimensional model of neural activity and phenomenal-behavioral patterns—Neural states and phenomenal-behavioral states.

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Acknowledgements

MM received support from the Taiwan National Science and Technology Council (109-2314-B-038-139-MY2; 111-2314-B-038-064), from Taipei Medical University (TMU108-AE1-B56; TMU112-F-001), and from Higher Education Sprout Project of the Taiwan Ministry of Education. PM received support from the Taiwan National Science and Technology Council (109-2314-B-038-138-MY2; 110-2628-B-038-015; 111-2628-B-038-023; 112-2628-B-038-006) and from Taipei Medical University (TMU111-AE1-B38).

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MM and PM conceived the model, performed the work, and wrote the manuscript.

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Correspondence to Matteo Martino or Paola Magioncalda.

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Martino, M., Magioncalda, P. A three-dimensional model of neural activity and phenomenal-behavioral patterns. Mol Psychiatry (2023). https://doi.org/10.1038/s41380-023-02356-w

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