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

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 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. 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 (Fig. 1). One of the gratings was positioned over the receptive fields of recorded neurons and the other was located at an equivalent eccentricity away from the receptive fields. Trials in which attention was directed towards (attendtowards condition) and away (attend-away condition) from the receptive fields of recorded neurons were organized into blocks and cued by the colour of the central fixation dot. In a random 5% of the trials the cue instruction was invalid, such that the contrast change occurred at the unattended location. Animals were rewarded for correct detection of the contrast change in validly and invalidly cued trials. Behavioural measures of spatial attention were derived by comparisons of accuracy (percentage of trials completed correctly) and reaction times in validly and invalidly cued trials. For both monkeys, accuracy was significantly greater (P , 0.03) and reaction times were significantly faster (P , 0.05; Fig. 1b) for validly versus invalidly cued trials, indicating that animals were covertly attending to the specified location. In each animal, we implanted stimulating electrodes in the magnocellular and parvocellular layers of the LGN (Fig. 2a), so that weak electrical shocks applied to thalamocortical neurons in these layers evoked suprathreshold, shortand fixed-latency monosynaptic spikes in recorded (postsynaptic) thalamocortical-recipient (TCR) neurons, located in layer 4C of V1 (Fig. 2a, b). Importantly, stimulation levels were set so that stimulation evoked a postsynaptic spike in only a fraction of trials (Supplementary Fig. 1a). We recorded visually evoked activity in response to drifting sinusoidal gratings in order to characterize the physiological responses of all recorded TCR neurons. TCR neurons (n 5 61) were grouped into those receiving input from the magnocellular layers and from the parvocellular layers (we refer to these as magnocellular-recipient (n 5 36) and parvocellular-recipient (n 5 25) populations, respectively) based on the stimulus contrast required to evoke a half-maximum response (Fig. 2c). Magnocellularand parvocellular-recipient neurons differed across several physiological