Scientific Understanding of Consciousness
Attention Enhances Synaptic Efficacy and Signal-to-Noise Ratio
Nature 499, 476–480 (25 July 2013)
Attention enhances synaptic efficacy and the signal-to-noise ratio in neural circuits
Center for Neuroscience, University of California, Davis, 1544 Newton Court, Davis, California 95618, USA
Farran Briggs & W. Martin Usrey
Department of Physiology and Neurobiology, Geisel School of Medicine at Dartmouth, 1 Medical Center Drive, Lebanon, New Hampshire 03756, USA
Center for Mind and Brain, University of California, Davis, 267 Cousteau Place, Davis, California 95618, USA
George R. Mangun
Department of Psychology, University of California, Davis, 1 Shields Avenue, Davis, California 95616, USA
George R. Mangun
Department of Neurology, University of California, Davis, 4860 Y Street, Sacramento, California 95817, USA
George R. Mangun & W. Martin Usrey
Department of Neurobiology, Physiology and Behavior, University of California, Davis, 1 Shields Avenue, Davis, California 95616, USA
W. Martin Usrey
Attention is a critical component of perception. 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 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.
Selective attention is a powerful brain mechanism that enables enhanced processing of relevant information while preventing interference from distracting events. Many studies in humans and animals have established that visual attention can influence sensory information processing in visual cortex and subcortical visual areas. Attention directed towards stimuli within the receptive field of a neuron in visual cortex generally results in increases in neuronal firing rate and synchrony. More recent work indicates that visual attention can also alter the correlation structure, variability and/or response gain of neuronal activity. However, the fundamental mechanisms by which visual attention alters communication in neural circuits, at the synaptic level, remain a mystery. Moreover, it is unclear how attention-mediated alterations in neuronal population activity translate into improvements in perception.
To elucidate the synaptic mechanisms of attention, we developed a sensitive electrophysiological assay of neuronal communication involving stimulation of thalamocortical neurons in the lateral geniculate nucleus (LGN) of the thalamus and simultaneous recordings from monosynaptically connected (that is, postsynaptic) neurons in primary visual cortex (V1) of macaque monkeys performing a spatial attention task. First, we tested whether visual attention alters the efficacy of synaptic communication between the LGN and V1, defined here as the probability that presynaptic stimulation evokes a postsynaptic action potential. Second, we examined whether attention alters both signal and noise in correlated activity among ensembles of postsynaptic target neurons.
Two monkeys were trained to maintain central fixation while covertly focusing their attention on one of two drifting gratings in order to report a contrast change in the attended stimulus.
Taken together, the results of this study provide multiple insights into the mechanisms by which attention alters neuronal communication. First, attention modulates signal transmission by enhancing synaptic efficacy. This finding represents the first evidence that attention acts at the synaptic level. Second, attention modulates afferent signal transmission with fine temporal precision. Third, attention serves to increase the signal-to-noise ratio in neural circuits by simultaneously enhancing the transmission of signal and reducing the transmission of noise. These results suggest strongly that attention modulates synaptic inputs in a highly selective manner, such that inputs that carry salient sensory information (through independent channels) are enhanced and inputs carrying potentially redundant information (through common channels) are suppressed. Each of these results has significant implications for our understanding of attentional modulation of sensory information processing.
Attentional modulation of synaptic efficacy in thalamocortical circuits was robust and displayed temporal precision. Attention-related improvements in spike-timing precision in V1 resulted in part from fast disynaptic feedforward inhibition. Interestingly, the temporal precision of attentional modulation of V1 activity did not correlate strongly with more global changes in firing rate (represented by an attention index calculated from peri-stimulus spiking activity). This lack of correspondence suggests that attention alters brain activity through multiple mechanisms, including more global alterations in neuronal firing rate, as well as finer-scale dynamic alterations in synaptic communication operating at the level of individual neural circuits. Moreover, our results support the idea that attentional modulations involving fine-scale dynamics may not manifest in more global alterations in neuronal firing rate. At the local circuit level, this effect may serve to enhance spatial and temporal precision, but at the more global level, these effects may average out. In V1 (and other sensory cortices), attention may make use of fine-scale dynamics to accommodate depressing synapses, a known property of thalamocortical afferents. It would be interesting to know whether or not attention affects synaptic weights in higher visual cortical areas and, if so, whether the effects of attention on synaptic weights underlie the influence of attention on neuronal firing-rate dynamics.
Our data support the idea that attention enhances sensory information processing directly by increasing the ratio of signal to noise in neural-circuit communication. Simultaneous signal enhancement and noise reduction in the same neural circuit suggests that attention modulates correlated synaptic activity in a highly selective manner. Select synaptic connections that originate from independent inputs and carrying feature-specific information about a sensory stimulus are more strongly weighted with attention, leading to better processing of salient stimulus features by downstream neurons. Synaptic connections that originate from common inputs are weighted less with attention, so that false positives are less likely to be communicated to downstream decoding neurons. Such asymmetric synaptic weighting with attention hints at a presynaptic locus for modulation, because a postsynaptic locus, such as altering the membrane potential threshold of cortical recipient neurons, would be difficult to reconcile with asymmetric synaptic weights. Furthermore, the finding that attention does not increase the overall firing rate of cortical neurons that receive direct LGN input indicates that the measured changes in thalamocortical communication are unlikely to be due to a generalized depolarization among target neurons with attention. To determine the structural basis for presynaptic modulation is beyond the scope of the current study, but one possible candidate is differential modulation by acetylcholine. Acetylcholine has been implicated in attention effects in V1, and a particular class of cholinergic receptors are localized to the presynaptic terminals of LGN axons that innervate cortical layer 4C neurons. These cholinergic synapses could therefore provide a route for attention to alter synaptic weights selectively.
Feedforward subcortical–cortical and cortico–cortical connections often must convey information with speed and precision, but anatomical wiring constraints on these connections can introduce unreliable information. Here we demonstrate that attention alters synaptic communication in a dynamic and highly selective manner that could be uniquely adapted for signal transmission in sensory cortex. Specifically, attention selectively enhances inputs carrying salient sensory information while simultaneously suppressing inputs carrying potentially redundant information. These findings suggest that attention could represent a critical mechanism by which anatomical wiring limitations are overcome in order to optimize communication across neural circuits, thereby permitting the most behaviourally relevant information to influence perception and performance.
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