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Subcortical face processing

Key Points

  • Recent functional imaging, neuropsychological and electrophysiological studies on adults have provided evidence for a fast, low-spatial-frequency (LSF), subcortical face-detection pathway that might also modulate the responses of certain cortical areas to faces and other social stimuli. This route involves the superior colliculus, the pulvinar and the amygdala.

  • Evidence from human depth electrode studies, and from event-related potential and magnetoencephalographic studies, supports a fast pathway for face detection that can produce a face-selective response before early visual cortical areas are activated.

  • Functional MRI studies indicate that the subcortical route processes LSF information about faces, in contrast to the mid- and high-spatial-frequencies that are processed by the cortical route.

  • In many face perception tasks, activity in the two routes is correlated, and functional connections between the subcortical route and cortical regions increases. Together with the shorter-latency activity in the subcortical route, this raises the hypothesis that the subcortical route can modulate activity in face-sensitive cortical regions before the arrival of visual information through the cortical route.

  • Although the amygdala route has commonly been associated with fear detection, various lines of evidence indicate that it has a broader function. Alternative proposals include that the pathway is maximally sensitive to LSF aspects of faces (and that this selectively differentiates expressions such as fear), and that the route is most responsive to the eyes of a stimulus face.

  • Evidence has accrued from many studies that human newborns are biased to attend towards face-relevant stimuli. Although there is a continuing debate about the mechanisms underlying this bias, it is generally agreed that it is sufficient for newborns to attend to real faces in the natural environment.

  • Converging evidence leads to the hypothesis that the subcortical route described in adults supports the face bias in newborns. This suggests an important role for the subcortical route in establishing the specialization of cortical regions involved in face processing during development.

  • The proposed role for the subcortical route in typical development leads to the postulation that disturbance of this route could account for patterns of deficit in some developmental disorders, particularly autism and developmental prosopagnosia.

Abstract

Recent functional imaging, neuropsychological and electrophysiological studies on adults have provided evidence for a fast, low-spatial-frequency, subcortical face-detection pathway that modulates the responses of certain cortical areas to faces and other social stimuli. These findings shed light on an older literature on the face-detection abilities of newborn infants, and the hypothesis that these newborn looking preferences are generated by a subcortical route. Converging lines of evidence indicate that the subcortical face route provides a developmental foundation for what later becomes the adult cortical 'social brain' network, and that disturbances to this pathway might contribute to certain developmental disorders.

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Figure 1: The dual route model of face processing in adults.
Figure 2: Both schematic and realistic stimuli have been used to test newborns' preferences for face-related stimuli.
Figure 3: Schematic illustration of the stimuli that might be optimal for eliciting a face-related preference in newborns.
Figure 4: How newborns see faces.

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Acknowledgements

I acknowledge financial support from the Medical Research Council, and helpful discussions with G. Csibra, M. Eimer, T. Farroni, G. Horn and M. Spratling.

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DATABASES

OMIM

Autism

FURTHER INFORMATION

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Glossary

NEGLECT

A neurological syndrome (often involving damage to the right parietal cortex) in which patients show a marked difficulty in detecting or responding to information in the contralesional field.

BLINDSIGHT

The ability of a person with a lesion in the primary visual cortex to reach towards or guess at the orientation of objects projected on the part of the visual field that corresponds to this lesion, even though they report that they can see nothing in that part of their visual field.

PROSOPAGNOSIA

The inability to visually recognize faces that were previously familiar, usually after a brain injury.

VISUAL EXTINCTION

This is often associated with damage to the parietal cortex. The patient can see a stimulus presented alone in the contralateral visual field, but cannot see it if it is presented at the same time as a stimulus in the ipsilateral visual field.

EVENT-RELATED POTENTIALS

(ERPs). Electrical potentials that are generated in the brain as a consequence of the synchronized activation of neuronal networks by external stimuli. These evoked potentials are recorded at the scalp and consist of precisely timed sequences of waves or 'components'.

MAGNETOENCEPHALOGRAPHY

(MEG). A non-invasive technique that allows the detection of the changing magnetic fields that are associated with brain activity. As the magnetic fields of the brain are weak, extremely sensitive magnetic detectors, known as superconducting quantum interference devices, that work at low, superconducting temperatures (−269 °C) are used to pick up the signal.

N170/M170

The N170 is a well-studied ERP component, the latency and amplitude of which are modulated by the presence of faces in the visual input to the participant. It is a negative peak that is usually recorded at 170 ms after stimulus onset over lateral occipital and temporal recording sites. The M170 is a similar component recorded during MEG studies of face processing, and might share common generators with the N170.

VENTRAL VISUAL PATHWAY

Visual information coming from the primary visual cortex is processed in two interconnected but partly dissociable visual pathways, a 'ventral' pathway, which extends into the temporal lobe and is thought to be primarily involved in visual object recognition, and a 'dorsal' pathway, which extends into the parietal lobes and is thought to be more involved in extracting information about 'where' an object is or 'how' to execute visually guided actions towards it.

GAP EFFECT

A commonly observed phenomenon is that a saccade to a peripheral target is significantly slower when a central fixation stimulus is still present, compared with when the fixation point is removed at, or just before, the onset of the peripheral target. One explanation for this gap effect is that participants have to disengage from the fixation point before initiating their saccade to the target.

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Johnson, M. Subcortical face processing. Nat Rev Neurosci 6, 766–774 (2005). https://doi.org/10.1038/nrn1766

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