Scientific Understanding of Consciousness
Consciousness as an Emergent Property of Thalamocortical Activity

Attention Modulated Top-Down, Selectively Processes Information


Science 8 August 2014:  Vol. 345  no. 6197  pp. 660-665 

Long-range and local circuits for top-down modulation of visual cortex processing

Siyu Zhang,

Division of Neurobiology, Department of Molecular and Cell Biology, Helen Wills Neuroscience Institute, Howard Hughes Medical Institute, University of California, Berkeley, CA 94720, USA.

Department of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, CA 94305, USA.


Top-down modulation of sensory processing allows the animal to select inputs most relevant to current tasks. We found that the cingulate (Cg) region of the mouse frontal cortex powerfully influences sensory processing in the primary visual cortex (V1) through long-range projections that activate local γ-aminobutyric acid–ergic (GABAergic) circuits. Optogenetic activation of Cg neurons enhanced V1 neuron responses and improved visual discrimination. Focal activation of Cg axons in V1 caused a response increase at the activation site but a decrease at nearby locations (center-surround modulation). Whereas somatostatin-positive GABAergic interneurons contributed preferentially to surround suppression, vasoactive intestinal peptide-positive interneurons were crucial for center facilitation. Long-range corticocortical projections thus act through local microcircuits to exert spatially specific top-down modulation of sensory processing.

Sensory processing is strongly modulated by the animal’s behavioral state. A well-known example is top-down attention, a powerful mechanism for selective processing of behaviorally relevant information and filtering out irrelevant stimuli. In visual cortical areas, many neurons exhibit enhanced responses to attended stimuli. Several frontal and parietal cortical regions have been implicated as the sources of top-down modulation signals, especially the dorsolateral prefrontal cortex and frontal eye field (FEF). Electrical stimulation of the FEF enhanced V4 neuron responses at the retinotopically corresponding location and suppressed responses at other locations, resembling the center-surround profile of attentional modulation. Beyond identifying the signal sources, however, the synaptic circuits mediating top-down modulation are largely unknown. In addition to corticocortical projections, FEF also projects to the thalamus and other subcortical circuits that modulate cortical processing. The role of each pathway has not been clearly delineated. Furthermore, because long-range corticocortical projections are primarily glutamatergic, whether and how they provide center-surround modulation is unknown.

To examine the circuit mechanism of top-down modulation in mouse brain, we first identified neurons in the frontal cortex that directly project to visual cortex by injecting fluorescent latex microspheres (Retrobeads) into V1. We found numerous retrogradely labeled neurons in the cingulate (Cg) area. To visualize the axonal projections from Cg excitatory neurons, we injected adeno-associated virus [AAV-CaMKIIα-hChR2(H134R)-EYFP] into Cg. We found enhanced yellow fluorescent protein (EYFP)–labeled axons in both V1 and surrounding visual areas, with the axons in V1 preferentially distributed in layers 1 and 6. Cg neurons also project to the superior colliculus.

We identified a region of mouse frontal cortex that can exert spatially specific top-down modulation of visual processing, which is a hallmark of selective attention. The spatial pattern of Cg projections and its powerful modulation of visual processing indicate functional similarity between mouse Cg and primate FEF (although the FEF projects primarily to higher visual areas rather than V1). In primate visual cortex, top-down attention enhances the firing rates of putative inhibitory interneurons. In our study, the three subtypes of interneurons were all innervated by Cg, but they play different roles in top-down modulation. SOM+ neurons strongly inhibit pyramidal neurons in response to Cg input 200 μm away. That they also mediate suppression by visual stimuli outside of the receptive field suggests that both bottom-up visual processing and top-down attentional modulation use a common mechanism for surround suppression. Disinhibition of pyramidal neurons by VIP+ neurons has also been shown in somatosensory, visual, auditory, and medial prefrontal cortices, mediating firing rate increases induced by motor activity or reinforcement signals. In the top-down modulation studied here, the disinhibition is highly localized at the site of Cg axon activation.

Whereas spatial attention involves center-surround modulation in the space domain, feature attention also biases the competition between attended and unattended stimuli, perhaps via circuit mechanisms similar to those described here but operating in higher visual areas in stimulus feature space. Enhancing neuronal representation of relevant input and filtering out irrelevant stimuli are two equally important aspects of selective attention. Long-range glutamatergic projections can exert both types of modulation by activating local circuits that contain distinct subtypes of GABAergic interneurons.

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