Attention enhances synaptic efficacy and the signal-to-noise ratio in neural circuits

• Published in: Nature (London) 2013-07, Vol.499 (7459), p.476-480
• Main Authors: Briggs, Farran, Mangun, George R., Usrey, W. Martin
• Format: Article
• Language: English
• Subjects: 631/378/1697; Action Potentials; Animals; Attention; Attention - physiology; Biological and medical sciences; Brain; Electric Stimulation; Electrodes; Eye and associated structures. Visual pathways and centers. Vision; Female; Fundamental and applied biological sciences. Psychology; Geniculate Bodies - cytology; Geniculate Bodies - physiology; Humanities and Social Sciences; letter; Macaca mulatta - physiology; multidisciplinary; Neural circuitry; Neural transmission; Neurons; Neurons - physiology; Photic Stimulation; Physiological aspects; Science; Signal-To-Noise Ratio; Synapses - physiology; Synaptic Transmission; Time Factors; Vertebrates: nervous system and sense organs; Visual Cortex - cytology; Visual Cortex - physiology; Visual Pathways - cytology; Visual Pathways - physiology
• ISSN: 0028-0836; 1476-4687
• DOI: 10.1038/nature12276

In monkeys performing a visual spatial attention task, stimulation of neurons in the lateral geniculate nucleus and recording of shock-evoked responses from monosynaptically connected primary-visual-cortex neurons shows that attention enhances neuronal communication by increasing the efficacy of presynaptic input, increasing synchronous responses, and by decreasing redundant signals. Pay attention, turn down the noise Attention enhances neural processing at many points in sensory systems, but how it influences interactions between different brain areas is less well understood. Martin Usrey and colleagues probe how attention alters the functional connection between lateral geniculate nucleus and primary visual cortex, two areas modulated by attention. They find that attention not only enhances the efficacy of transmission between the areas, but also increases synchronization and reduces redundancy in primary visual cortex responses, thereby potentially reducing noise in the system. Attention is a critical component of perception 1 . However, the mechanisms by which attention modulates neuronal communication to guide behaviour are poorly understood. To elucidate the synaptic mechanisms of attention, we developed a sensitive assay of attentional modulation of neuronal communication. In alert monkeys performing a visual spatial attention task, we probed thalamocortical communication by electrically stimulating neurons in the lateral geniculate nucleus of the thalamus while simultaneously recording shock-evoked responses from monosynaptically connected neurons in primary visual cortex. We found that attention enhances neuronal communication by increasing the efficacy of presynaptic input in driving postsynaptic responses, by increasing synchronous responses among ensembles of postsynaptic neurons receiving independent input, and by decreasing redundant signals between postsynaptic neurons receiving common input. The results demonstrate that attention finely tunes neuronal communication at the synaptic level by selectively altering synaptic weights, enabling enhanced detection of salient events in the noisy sensory environment.