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The influence of subcortical shortcuts on disordered sensory and cognitive processing

Nature Reviews Neuroscience volume 21, pages 264–276 (2020)Cite this article

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Abstract

The very earliest stages of sensory processing have the potential to alter how we perceive and respond to our environment. These initial processing circuits can incorporate subcortical regions, such as the thalamus and brainstem nuclei, which mediate complex interactions with the brain’s cortical processing hierarchy. These subcortical pathways, many of which we share with other animals, are not merely vestigial but appear to function as ‘shortcuts’ that ensure processing efficiency and preservation of vital life-preserving functions, such as harm avoidance, adaptive social interactions and efficient decision-making. Here, we propose that functional interactions between these higher-order and lower-order brain areas contribute to atypical sensory and cognitive processing that characterizes numerous neuropsychiatric disorders.

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Fig. 1: Analogous neural networks for threat responses across species.
Fig. 2: Interactions between cortical and subcortical networks during attentional allocation.
Fig. 3: Updating of beliefs using sensory evidence and prior expectations.

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Acknowledgements

R.J.D. and J.M. were supported by the Wellcome Trust (098362/A/12/Z and 091593/Z/10/Z) and M.I.G. by the University of Queensland (2016000071). The authors thank the reviewers for their insightful comments on the manuscript, J. B. Mattingley for his helpful discussions and all of the researchers who conducted the experiments discussed in this Review. Finally, they especially thank the late patient T.N., whose generosity and willingness to help has made a significant and lasting impact on our understanding of blindsight in the human brain.

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Authors and Affiliations

  1. Max Planck UCL Centre for Computational Psychiatry and Ageing Research, London, UK

    Jessica McFadyen & Raymond J. Dolan

  2. The Wellcome Trust Centre for Neuroimaging, UCL, London, UK

    Jessica McFadyen & Raymond J. Dolan

  3. Queensland Brain Institute, University of Queensland, Brisbane, Australia

    Jessica McFadyen & Marta I. Garrido

  4. Australian Research Council Centre of Excellence for Integrative Brain Function, Melbourne, Australia

    Marta I. Garrido

  5. Melbourne School of Psychological Sciences, University of Melbourne, Melbourne, Australia

    Marta I. Garrido

  6. Centre for Advanced Imaging, University of Queensland, Brisbane, Australia

    Marta I. Garrido

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J.M. researched data for article and made a substantial contribution to the discussion of content, writing and review/editing of the manuscript before submission. R.J.D and M.I.G made substantial contributions to the discussion of content and review/editing of the manuscript before submission.

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Nature Reviews Neuroscience thanks M. Tamietto, J. Lin and the other anonymous reviewer(s) for their contribution to the peer review of this work.

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Glossary

Neuroanatomical tracing

An invasive neuroimaging technique that involves injecting dye into either the cell body of a neuron (that is, anterograde tracing) or a neural synapse (that is, retrograde tracing) to visualize anatomical projections.

Diffusion imaging

A variant of MRI that measures the diffusion of water molecules that, in the brain, is restricted by the structure of biological tissue (for example, white matter tracts).

GABAergic

A description of neurons that use the neurotransmitter GABA (that is, γ-aminobutryic acid, which reduces neuronal excitability).

Fractional anisotropy

A measure derived from diffusion-weighted images that describes how restricted the diffusion process was, from 0 (isotropic, unrestricted in all directions) to 1 (anisotropic, restricted to one axis).

Tectopulvinar

Anatomical features pertaining to the tectum (that is, uppermost part of the midbrain, including the superior colliculus) and the pulvinar.

Geniculostriate

Anatomical features pertaining to the lateral geniculate nucleus and the striate cortex (that is, the primary visual cortex (V1)).

Saliency maps

Topographically organized maps of the degree to which a stimulus differs in its sensory properties from its surroundings.

Gabor patches

Striped circular stimuli that have a particular spatial frequency and orientation, created by convolving a Gaussian kernel with a sinusoidal wave.

Electroencephalography

A non-invasive functional neuroimaging method that uses scalp electrodes to measure electric activity.

Magnetoencephalography

A non-invasive functional neuroimaging method that uses sensitive external sensors to measure the magnetic fields emitted by electrical currents within the brain.

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McFadyen, J., Dolan, R.J. & Garrido, M.I. The influence of subcortical shortcuts on disordered sensory and cognitive processing. Nat Rev Neurosci 21, 264–276 (2020). https://doi.org/10.1038/s41583-020-0287-1

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