Abstract
Selective attention supports the prioritized processing of relevant sensory information to facilitate goal-directed behavior. Studies in human subjects demonstrate that attentional gain of cortical responses can sufficiently account for attention-related improvements in behavior. On the other hand, studies using highly trained nonhuman primates suggest that reductions in neural noise can better explain attentional facilitation of behavior. Given the importance of selective information processing in nearly all domains of cognition, we sought to reconcile these competing accounts by testing the hypothesis that extensive behavioral training alters the neural mechanisms that support selective attention. We tested this hypothesis using electroencephalography (EEG) to measure stimulus-evoked visual responses from human subjects while they performed a selective spatial attention task over the course of ~1 month. Early in training, spatial attention led to an increase in the gain of stimulus-evoked visual responses. Gain was apparent within ~100 ms of stimulus onset, and a quantitative model based on signal detection theory (SDT) successfully linked the magnitude of this gain modulation to attention-related improvements in behavior. However, after extensive training, this early attentional gain was eliminated even though there were still substantial attention-related improvements in behavior. Accordingly, the SDT-based model required noise reduction to account for the link between the stimulus-evoked visual responses and attentional modulations of behavior. These findings suggest that training can lead to fundamental changes in the way attention alters the early cortical responses that support selective information processing. Moreover, these data facilitate the translation of results across different species and across experimental procedures that employ different behavioral training regimes.
Highlights
Selective attention influences sensory processing such that relevant information is preferentially encoded at the expense of irrelevant information
With respect to behavior and perception, attentional gain of the P1 component is correlated with improved target detection [19], with improved contrast discrimination thresholds [9], and with changes in perceived contrast [31], and taken together, these findings suggest that the amount of attentional gain in the human visual cortex has a significant impact on both perception and behavior during tasks that require selective attention
Consistent with a recent report [9], early in training we found a significant increase in the maximum response of the P1-based contrast response function (CRF) in the focused target condition compared to the focused nontarget condition (p = 0.004) and a significant increase in the maximum response in the focused target condition compared to the divided attention condition (Fig 5A left and 5B top, p < 0.001, resampling tests, 2-tailed)
Summary
Selective attention influences sensory processing such that relevant information is preferentially encoded at the expense of irrelevant information. In addition to the extensive literature on attention-related gain modulations, recent electrophysiological studies in nonhuman primates demonstrate that attention can reduce the trial-by-trial variability of single neuron spike rates and the magnitude of correlated spiking between neurons [36,37,38,39,40,41,42,43,44] These modulations of neuronal noise may improve the signal-to-noise ratio of sensory codes more than attentional gain [37,40] and may be better predictors of improvements in behavioral performance [37]. Training may play a key role in shaping how selective attention impacts cortical responses to facilitate goal-directed behavior, and characterizing training effects is critical for generalizing results across tasks and species
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