Perception is associated with the brain's metabolic response to sensory stimulation

  1. Mauro DiNuzzo
  2. Silvia Mangia
  3. Marta Moraschi
  4. Daniele Mascali
  5. Gisela E Hagberg
  6. Federico Giove  Is a corresponding author
  1. Museo Storico della Fisica e Centro Studi e Ricerche Enrico Fermi, Italy
  2. University of Minnesota, United States
  3. University of Rome, Italy
  4. Università Gabriele D'Annunzio, Italy
  5. Max Planck Institute for Biological Cybernetics and Biomedical Magnetic Resonance, Germany

Abstract

Processing of incoming sensory stimulation triggers an increase of cerebral perfusion and blood oxygenation (neurovascular response) as well as an alteration of the metabolic neurochemical profile (neurometabolic response). Here we show in human primary visual cortex (V1) that perceived and unperceived isoluminant chromatic flickering stimuli designed to have similar neurovascular responses as measured by blood oxygenation level dependent functional MRI (BOLD-fMRI) have markedly different neurometabolic responses as measured by functional MRS. In particular, a significant regional buildup of lactate, an index of aerobic glycolysis, and glutamate, an index of malate-aspartate shuttle, occurred in V1 only when the flickering was perceived, without any relation with behavioral or physiological variables. Whereas the BOLD-fMRI signal in V1, a proxy for input to V1, was insensitive to flickering perception by design, the BOLD-fMRI signal in secondary visual areas was larger during perceived than unperceived flickering, indicating increased output from V1. These results demonstrate that the upregulation of energy metabolism induced by visual stimulation depends on the type of information processing taking place in V1, and that 1H-fMRS provides unique information about local input/output balance that is not measured by BOLD fMRI.

Data availability

The study was developed using SPM12 (https://www.fil.ion.ucl.ac.uk/spm/software/spm12/), LCmodel (http://s-provencher.com/lcmodel.shtml), jMRUI (http://www.jmrui.eu/) and AFNI (https://afni.nimh.nih.gov/). Data used for all the figures and for Tables 2-3 is available as source data to each element. Source data include also custom Matlab code for processing related to each figure. The raw data include sensitive data. The raw dataset cannot be made available in a public repository because of constraints originally set by the Ethics Committee and included in the informed consent signed by participants. Raw data that support the findings of this study are available from the corresponding author upon signing a MTA that would include: a list of authorized researchers; a commitment to not disclose the raw data to persons not included in the list; and a commitment to destroy the raw data when legitimate use is finished. Commercial use of the raw data is not permitted.

Article and author information

Author details

  1. Mauro DiNuzzo

    Museo Storico della Fisica e Centro Studi e Ricerche Enrico Fermi, Rome, Italy
    Competing interests
    The authors declare that no competing interests exist.
  2. Silvia Mangia

    Center for Magnetic Resonance Research, University of Minnesota, Minneapolis, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Marta Moraschi

    Department of Radiation Oncology, University of Rome, Rome, Italy
    Competing interests
    The authors declare that no competing interests exist.
  4. Daniele Mascali

    Dipartimento di Neuroscienze, Università Gabriele D'Annunzio, Chieti, Italy
    Competing interests
    The authors declare that no competing interests exist.
  5. Gisela E Hagberg

    High-Field Magnetic Resonance, Max Planck Institute for Biological Cybernetics and Biomedical Magnetic Resonance, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Federico Giove

    Museo Storico della Fisica e Centro Studi e Ricerche Enrico Fermi, Rome, Italy
    For correspondence
    federico.giove@uniroma1.it
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6934-3146

Funding

Ministero della Salute (Ricerca Corrente)

  • Federico Giove

Max Planck Institute for Biological Cybernetics (Open Access funding)

  • Gisela E Hagberg

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Human subjects: This study included human subjects and was performed by the authors in compliance with all applicable ethical standards, including the Helsinki declaration and its amendments, institutional/national standards, and international/national/institutional guidelines. The study was approved by the Ethics Committee of Fondazione Santa Lucia (Rome). All subjects gave informed consent before being enrolled in the study.

Copyright

© 2022, DiNuzzo et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 2,517
    views
  • 386
    downloads
  • 15
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Mauro DiNuzzo
  2. Silvia Mangia
  3. Marta Moraschi
  4. Daniele Mascali
  5. Gisela E Hagberg
  6. Federico Giove
(2022)
Perception is associated with the brain's metabolic response to sensory stimulation
eLife 11:e71016.
https://doi.org/10.7554/eLife.71016

Share this article

https://doi.org/10.7554/eLife.71016

Further reading

    1. Cancer Biology
    2. Neuroscience
    Jeffrey Barr, Austin Walz ... Paola D Vermeer
    Research Article

    Cancer patients often experience changes in mental health, prompting an exploration into whether nerves infiltrating tumors contribute to these alterations by impacting brain functions. Using a mouse model for head and neck cancer and neuronal tracing, we show that tumor-infiltrating nerves connect to distinct brain areas. The activation of this neuronal circuitry altered behaviors (decreased nest-building, increased latency to eat a cookie, and reduced wheel running). Tumor-infiltrating nociceptor neurons exhibited heightened calcium activity and brain regions receiving these neural projections showed elevated Fos as well as increased calcium responses compared to non-tumor-bearing counterparts. The genetic elimination of nociceptor neurons decreased brain Fos expression and mitigated the behavioral alterations induced by the presence of the tumor. While analgesic treatment restored nesting and cookie test behaviors, it did not fully restore voluntary wheel running indicating that pain is not the exclusive driver of such behavioral shifts. Unraveling the interaction between the tumor, infiltrating nerves, and the brain is pivotal to developing targeted interventions to alleviate the mental health burdens associated with cancer.

    1. Neuroscience
    Xinlin Hou, Peng Zhang ... Dandan Zhang
    Research Article

    Emotional responsiveness in neonates, particularly their ability to discern vocal emotions, plays an evolutionarily adaptive role in human communication and adaptive behaviors. The developmental trajectory of emotional sensitivity in neonates is crucial for understanding the foundations of early social-emotional functioning. However, the precise onset of this sensitivity and its relationship with gestational age (GA) remain subjects of investigation. In a study involving 120 healthy neonates categorized into six groups based on their GA (ranging from 35 and 40 weeks), we explored their emotional responses to vocal stimuli. These stimuli encompassed disyllables with happy and neutral prosodies, alongside acoustically matched nonvocal control sounds. The assessments occurred during natural sleep states using the odd-ball paradigm and event-related potentials. The results reveal a distinct developmental change at 37 weeks GA, marking the point at which neonates exhibit heightened perceptual acuity for emotional vocal expressions. This newfound ability is substantiated by the presence of the mismatch response, akin to an initial form of adult mismatch negativity, elicited in response to positive emotional vocal prosody. Notably, this perceptual shift’s specificity becomes evident when no such discrimination is observed in acoustically matched control sounds. Neonates born before 37 weeks GA do not display this level of discrimination ability. This developmental change has important implications for our understanding of early social-emotional development, highlighting the role of gestational age in shaping early perceptual abilities. Moreover, while these findings introduce the potential for a valuable screening tool for conditions like autism, characterized by atypical social-emotional functions, it is important to note that the current data are not yet robust enough to fully support this application. This study makes a substantial contribution to the broader field of developmental neuroscience and holds promise for future research on early intervention in neurodevelopmental disorders.