In contrast to the traditional idea that the processing of visual information consists of a sequence of feedforward operations, with neuronal functional properties taking on increasing complexity as the information progresses through a hierarchy of cortical areas, increasing evidence points towards a reverse process, with higher-order cognitive influences interacting with information coming from the retina.
Thus, rather than having a fixed functional role, neurons should be thought of as adaptive processors, changing their function according to the behavioural context.
Vision is an active process in which higher-order cognitive influences affect the operations performed by cortical neurons.
Visual pathways operate bidirectionally, with each feedforward connection being matched by feedback or re-entrant connections going from higher- to lower-order cortical areas.
Top-down influences include various forms of attention, such as spatial, object oriented and feature oriented attention.
Top-down influences are not limited to attention but mediate a much broader range of functional roles, including perceptual task, object expectation, scene segmentation, efference copy, working memory and the encoding and recall of learned information.
The effect of top-down influences is to change the information conveyed by neurons, both by altering the tuning of their responses to stimulus attributes and by changing the structure of correlations over neuronal ensembles.
All areas of the visual pathway, except for the retina, are subject to top-down influences, including early cortical stages of visual processing such as the primary visual cortex and the lateral geniculate nucleus, and all areas along the dorsal and ventral visual cortical pathways. Each area contains an association field of potential interactions, and expresses a subset of these interactions to execute different functions.
The sources of top-down influences are widespread, with each area providing information reflecting the functional properties of that area. As a consequence, even a single neuron can be viewed as a microcosm of activity occurring throughout the visual pathway.
We propose that the circuit mechanism of top-down control and adaptive processing involves a gating of intrinsic cortical circuits within an area mediated by long-range feedback connections to that area. By selecting a subset of inputs, a neuron can express different components of its association field, and as a result take on different functional roles.
Re-entrant or feedback pathways between cortical areas carry rich and varied information about behavioural context, including attention, expectation, perceptual tasks, working memory and motor commands. Neurons receiving such inputs effectively function as adaptive processors that are able to assume different functional states according to the task being executed. Recent data suggest that the selection of particular inputs, representing different components of an association field, enable neurons to take on different functional roles. In this Review, we discuss the various top-down influences exerted on the visual cortical pathways and highlight the dynamic nature of the receptive field, which allows neurons to carry information that is relevant to the current perceptual demands.
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This work was supported by US National Institutes of Health grant EY007968 (C.D.G.), a grant from the James S. McDonnell Foundation (C.D.G.), the National Natural Science Foundation of China grant 31125014 (W.L.) and the 111 Project B07008 (W.L.).
The authors declare no competing financial interests.
- Re-entrant or feedback pathways
Processing strategy in which the product of an ongoing computation at one cortical level is analysed by the next level. The resultant information is then sent back to the initial level to influence its further computation. This is also sometimes referred to as countercurrent processing streams.
- Visual cortical hierarchy
The hierarchy of cortical areas in the classical model of the cortical representation of visual information beginning with the primary visual cortex and ascending through two pathways: a ventral pathway extending into the temporal lobe, which is involved with object recognition, and a dorsal pathway extending into the parietal lobe, which is involved with visually directed movement and spatial attention.
- Intermediate-level vision
Visual processing that involves contour integration and surface segmentation.
In a complex visual scene, some objects are attended (the targets) and others (the distracters) are unattended, but the distracters can compete with the target for attentional resources.
One-half of the visual field.
- Line label
The property or information represented by a neuron. Different neurons represent different values, and the strength of their firing indicates how close the stimulus is to that value.
The variability in neurons' responses to a given stimulus. If different neurons with similar functional properties have independent noise, an ensemble of such neurons can carry more information about a stimulus than a single neuron.
- Local field potentials
(LFPs). The electrical fields generated by a population of neurons, with signals having components spanning a spectrum of frequencies. LFPs originate from the integrated currents coming from synaptic activation and from action potentials in dendrites, cell somata and axons.
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Gilbert, C., Li, W. Top-down influences on visual processing. Nat Rev Neurosci 14, 350–363 (2013). https://doi.org/10.1038/nrn3476
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