Attentional load modulates responses of human primary visual cortex to invisible stimuli.
ABSTRACT: Visual neuroscience has long sought to determine the extent to which stimulus-evoked activity in visual cortex depends on attention and awareness. Some influential theories of consciousness maintain that the allocation of attention is restricted to conscious representations [1, 2]. However, in the load theory of attention , competition between task-relevant and task-irrelevant stimuli for limited-capacity attention does not depend on conscious perception of the irrelevant stimuli. The critical test is whether the level of attentional load in a relevant task would determine unconscious neural processing of invisible stimuli. Human participants were scanned with high-field fMRI while they performed a foveal task of low or high attentional load. Irrelevant, invisible monocular stimuli were simultaneously presented peripherally and were continuously suppressed by a flashing mask in the other eye . Attentional load in the foveal task strongly modulated retinotopic activity evoked in primary visual cortex (V1) by the invisible stimuli. Contrary to traditional views [1, 2, 5, 6], we found that availability of attentional capacity determines neural representations related to unconscious processing of continuously suppressed stimuli in human primary visual cortex. Spillover of attention to cortical representations of invisible stimuli (under low load) cannot be a sufficient condition for their awareness.
Project description:A growing number of studies suggest that early visual processing is not only affected by low-level perceptual attributes but also by higher order cognitive factors such as attention or emotion. Using high-density electroencephalography, we recently demonstrated that attentional load of a task at fixation reduces the response of primary visual cortex to irrelevant peripheral stimuli, as indexed by the C1 component. In the latter study, peripheral stimuli were always presented during intervals without task-relevant stimuli. Here, we use a similar paradigm but present central task stimuli and irrelevant peripheral stimuli simultaneously while keeping all other stimulus characteristics constant. Results show that rather than to suppress responses to peripheral stimulation, high attentional load elicits higher C1 amplitudes under these conditions. These findings suggest that stimulus timing can profoundly alter the effects of attentional load on the earliest stages of processing in human visual cortex.
Project description:When a behaviorally relevant stimulus has been previously associated with reward, behavioral responses are faster and more accurate compared to equally relevant but less valuable stimuli. Conversely, task-irrelevant stimuli that were previously associated with a high reward can capture attention and distract processing away from relevant stimuli (e.g., seeing a chocolate bar in the pantry when you are looking for a nice, healthy apple). Although increasing the value of task-relevant stimuli systematically up-regulates neural responses in early visual cortex to facilitate information processing, it is not clear whether the value of task-irrelevant distractors influences behavior via competition in early visual cortex or via competition at later stages of decision-making and response selection. Here, we measured functional magnetic resonance imaging (fMRI) in human visual cortex while subjects performed a value-based learning task, and we applied a multivariate inverted encoding model (IEM) to assess the fidelity of distractor representations in early visual cortex. We found that the fidelity of neural representations related to task-irrelevant distractors increased when the distractors were previously associated with a high reward. This finding suggests that value-driven attentional capture begins with sensory modulations of distractor representations in early areas of visual cortex.
Project description:Task Irrelevant Perceptual Learning (TIPL) shows that the brain's discriminative capacity can improve also for invisible and unattended visual stimuli. It has been hypothesized that this form of "unconscious" neural plasticity is mediated by an endogenous reward mechanism triggered by the correct task performance. Although this result has challenged the mandatory role of attention in perceptual learning, no direct evidence exists of the hypothesized link between target recognition, reward and TIPL. Here, we manipulated the reward value associated with a target to demonstrate the involvement of reinforcement mechanisms in sensory plasticity for invisible inputs. Participants were trained in a central task associated with either high or low monetary incentives, provided only at the end of the experiment, while subliminal stimuli were presented peripherally. Our results showed that high incentive-value targets induced a greater degree of perceptual improvement for the subliminal stimuli, supporting the role of reinforcement mechanisms in TIPL.
Project description:Directing visual attention toward a particular feature or location in the environment suppresses processing of nearby stimuli [1-4]. Echoing the center-surround organization of retinal ganglion cell receptive fields , and biasing of competitive local neuronal dynamics in favor of task-relevant stimuli , this "inhibitory surround" attention mechanism accentuates the demarcation between task-relevant and irrelevant items. Here, we show that internally maintaining a color stimulus in working memory (WM), rather than visually attending the stimulus in the external environment, produces an analogous pattern of inhibition for stimuli that are nearby in color space. Replicating a well-known effect of attentional capture by stimuli that match WM content , visual attention was biased toward (task-irrelevant) stimuli that exactly matched a WM item. This bias was curtailed, however, for stimuli that were very similar to the WM content (i.e., within the inhibitory zone surrounding the focus of WM) and recovered for less similar stimuli (i.e., beyond the bounds of the inhibitory surround). Moreover, the expression of this inhibition effect was positively associated with WM performance across observers. In a second experiment, inhibition also occurred between two similar items simultaneously held in WM. This suggests that maintenance in WM is characterized by an excitatory peak centered on the focus of (internal) attention, surrounded by an inhibitory zone to limit interference by irrelevant and confusable representations. Here, thus, we show for the first time that the same center-surround selection mechanism that focuses visual attention on sensory stimuli also selectively maintains internally activated representations in WM.
Project description:Our daily behavior is dynamically influenced by conscious and unconscious processes. Although the neural bases of conscious experience have been extensively investigated over the past several decades, how unconscious information impacts neural circuitry and behavior remains unknown. Here, we recorded populations of neurons in macaque primary visual cortex (V1) to find that perceptually unidentifiable stimuli repeatedly presented in the absence of awareness are encoded by neural populations in a way that facilitates their future processing in the context of a behavioral task. Such exposure increases stimulus sensitivity and information encoded in cell populations, even though animals are unaware of stimulus identity. This phenomenon is consistent with a Hebbian mechanism underlying an increase in functional connectivity specifically for the neurons activated by subthreshold stimuli. This form of unsupervised adaptation may constitute a vestigial pre-attention system using the mere frequency of stimulus occurrence to change stimulus representations even when sensory inputs are perceptually invisible.
Project description:Theories of object-based attention often make two assumptions: that attentional resources are facilitatory, and that they spread automatically within grouped objects. Consistent with this, ignored visual stimuli can be easier to process, or more distracting, when perceptually grouped with an attended target stimulus. But in past studies, the ignored stimuli often shared potentially relevant features or locations with the target. In this fMRI study, we measured the effects of attention and grouping on Blood Oxygenation Level Dependent (BOLD) responses in the human brain to entirely task-irrelevant events. Two checkerboards were displayed each in opposite hemifields, while participants responded to check-size changes in one pre-cued hemifield, which varied between blocks. Grouping (or segmentation) between hemifields was manipulated between blocks, using common (vs. distinct) motion cues. Task-irrelevant transient events were introduced by randomly changing the color of either checkerboard, attended or ignored, at unpredictable intervals. The above assumptions predict heightened BOLD signals for irrelevant events in attended vs. ignored hemifields for ungrouped contexts, but less such attentional modulation under grouping, due to automatic spreading of facilitation across hemifields. We found the opposite pattern, in primary visual cortex. For ungrouped stimuli, BOLD signals associated with task-irrelevant changes were lower, not higher, in the attended vs. ignored hemifield; furthermore, attentional modulation was not reduced but actually inverted under grouping, with higher signals for events in the attended vs. ignored hemifield. These results challenge two popular assumptions underlying object-based attention. We consider a broader biased-competition framework: task-irrelevant stimuli are suppressed according to how strongly they compete with task-relevant stimuli, with intensified competition when the irrelevant features or locations comprise the same object.
Project description:Load theory of attention proposes that distractor processing is reduced in tasks with high perceptual load that exhaust attentional capacity within task-relevant processing. In contrast, tasks of low perceptual load leave spare capacity that spills over, resulting in the perception of task-irrelevant, potentially distracting stimuli. Tsal and Benoni (2010) find that distractor response competition effects can be reduced under conditions with a high search set size but low perceptual load (due to a singleton color target). They claim that the usual effect of search set size on distractor processing is not due to attentional load but instead attribute this to lower level visual interference. Here, we propose an account for their findings within load theory. We argue that in tasks of low perceptual load but high set size, an irrelevant distractor competes with the search nontargets for remaining capacity. Thus, distractor processing is reduced under conditions in which the search nontargets receive the spillover of capacity instead of the irrelevant distractor. We report a new experiment testing this prediction. Our new results demonstrate that, when peripheral distractor processing is reduced, it is the search nontargets nearest to the target that are perceived instead. Our findings provide new evidence for the spare capacity spillover hypothesis made by load theory and rule out accounts in terms of lower level visual interference (or mere "dilution") for cases of reduced distractor processing under low load in displays of high set size. We also discuss additional evidence that discounts the viability of Tsal and Benoni's dilution account as an alternative to perceptual load.
Project description:Attention modulates visual perception and is generally considered inextricably linked with conscious awareness: we become aware of stimuli as we attend to them, and we attend to stimuli as we become aware of them. Recent evidence suggests that attention can also modulate the effects of stimuli that remain invisible, and a natural explanation is that attention enhances weak perceptual representations, bringing them closer to conscious threshold even if they do not reach that threshold. However, there is also the possibility that attention may modulate neural processes that are entirely separate from those supporting conscious perception: sensorimotor mechanisms that do not create awareness however much they are enhanced. Here we provide evidence in support of this second hypothesis by showing that attentional cueing can modulate the behavioral response to invisible stimuli in a way that is distinct from enhancing their visibility. We used a masked-prime paradigm that produces a negative or positive compatibility effect depending on the perceptual strength (duration or brightness) of the prime. We found that attention enhanced the effect of both visible and invisible primes and also increased the likelihood of detecting the prime (i.e., boosted perceptual strength). Crucially, the pattern of attentional influence on priming could not be explained by attentional modulation of the prime's perceptual strength but was predicted by a direct attentional influence on the nonconscious priming process itself. Therefore, in addition to regulating what we perceive, attention seems to influence our behavior through sensorimotor processes that are not involved in conscious awareness.
Project description:For individuals with autism spectrum disorder (ASD), salient behaviorally-relevant information often fails to capture attention, while subtle behaviorally-irrelevant details commonly induce a state of distraction. The present study used functional magnetic resonance imaging (fMRI) to investigate the neurocognitive networks underlying attentional capture in sixteen high-functioning children and adolescents with ASD and twenty-one typically developing (TD) individuals. Participants completed a rapid serial visual presentation paradigm designed to investigate activation of attentional networks to behaviorally-relevant targets and contingent attention capture by task-irrelevant distractors. In individuals with ASD, target stimuli failed to trigger bottom-up activation of the ventral attentional network and the cerebellum. Additionally, the ASD group showed no differences in behavior or occipital activation associated with contingent attentional capture. Rather, results suggest that to-be-ignored distractors that shared either task-relevant or irrelevant features captured attention in ASD. Results indicate that individuals with ASD may be under-reactive to behaviorally-relevant stimuli, unable to filter irrelevant information, and that both top-down and bottom-up attention networks function atypically in ASD. Lastly, deficits in target-related processing were associated with autism symptomatology, providing further support for the hypothesis that non-social attentional processes and their neurofunctional underpinnings may play a significant role in the development of sociocommunicative impairments in ASD.
Project description:Practice improves perception and enhances neural representations of trained visual stimuli, a phenomenon known as visual perceptual learning (VPL). While attention to task-relevant stimuli plays an important role in such learning, Pavlovian stimulus-reinforcer associations are sufficient to drive VPL, even subconsciously. It has been proposed that reinforcement facilitates perceptual learning through the activation of neuromodulatory centers, but this has not been directly confirmed in primates. Here, we paired task-irrelevant visual stimuli with microstimulation of a dopaminergic center, the ventral tegmental area (VTA), in macaques. Pairing VTA microstimulation with a task-irrelevant visual stimulus increased fMRI activity and improved classification of fMRI activity patterns selectively for the microstimulation-paired stimulus. Moreover, pairing VTA microstimulation with a task-irrelevant visual stimulus improved the subject's capacity to discriminate that stimulus. This is the first causal demonstration of the role of neuromodulatory centers in VPL in primates.