Emotion processing and the amygdala: from a 'low road' to 'many roads' of evaluating biological significance

Abstract

A subcortical pathway through the superior colliculus and pulvinar to the amygdala is commonly assumed to mediate the non-conscious processing of affective visual stimuli. We review anatomical and physiological data that argue against the notion that such a pathway plays a prominent part in processing affective visual stimuli in humans. Instead, we propose that the primary role of the amygdala in visual processing, like that of the pulvinar, is to coordinate the function of cortical networks during evaluation of the biological significance of affective visual stimuli. Under this revised framework, the cortex has a more important role in emotion processing than is traditionally assumed.

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Figure 1: Visual pathways.
Figure 2: Intact non-conscious processing of fearful faces in the absence of the amygdala.
Figure 3: Schematic layout of the pulvinar.
Figure 4: Pulvinar and amygdala during processing of affective stimuli.

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Acknowledgements

The authors thank A. Anticevic, L. Oliveira, M. Pereira, R. Todd, and S. Wang for feedback on the manuscript. They also thank L. Barrett and two anonymous reviewers for comments. The authors' research is supported by grants from the National Institute of Mental Health (R01 MH071589 to L.P. and R01 MH080721 to R.A.), the National Institute of Neurological Disorders and Stroke (P01 NS019632 to R.A.), the Simons Foundation Autism Research Initiative and the National Science Foundation (NSF 0926,544).

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Glossary

Attentional blink

A phenomenon that occurs in experiments in which a rapid stream of visual items is presented to an observer whose task is to detect two targets within the stream. When the two targets are separated in time by a brief interval (for example, 200–500ms), the successful detection of the first target impairs detection of the second one (as if the participant blinked) owing to limited processing capacity.

Backward masking

A phenomenon that occurs in experimental paradigms in which a target visual stimulus is followed by another salient visual stimulus that 'masks' the perception of the target stimulus, making its detection or recognition difficult or impossible. Visual masking is commonly used to manipulate visual awareness.

Blindsight

The ability, in humans or monkeys, to respond to visual stimuli without consciously perceiving them — a situation that may ensue following a lesion to the primary visual cortex.

Continuous flash suppression

A technique in which a fixed image shown to one eye is suppressed by a stream of rapidly changing images flashed to the other eye. The technique is used to manipulate visual awareness.

Labelled line

A processing architecture in which a separate pathway conveys information that is specific to a class of sensory stimuli owing to, for example, receptor specificity (for example, pain and touch conveyed by particular somatosensory channels).

Magnocellular system

A visual pathway from the retina to the cortex that conveys relatively fast, transient and wavelength-insensitive information.

Path analysis

A statistical method to investigate the relationship between multiple variables.

Source modelling

A set of techniques that attempt to estimate the neural 'sources' of the electrical or magnetic signals that are measured at external sensors (for example, at the scalp in the case of electroencephalography).

Visual search

An experimental paradigm in which subjects are asked to indicate the presence or absence of a 'target' item (for example, a fearful face) among an array of distractor items (for example, neutral faces).

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Pessoa, L., Adolphs, R. Emotion processing and the amygdala: from a 'low road' to 'many roads' of evaluating biological significance. Nat Rev Neurosci 11, 773–782 (2010). https://doi.org/10.1038/nrn2920

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