Dissociations between top-down attention and visual awareness

Friday, May 7, 3:30 – 5:30 pm
Royal Ballroom 6-8

Organizers: Jeroen van Boxtel, California Institute of Technology and Nao Tsuchiya, California Institute of Technology, USA and Tamagawa University, Japan

Presenters: Nao Tsuchiya (California Institute of Technology, USA, Tamagawa University, Japan), Jeroen J.A. van Boxtel (California Institute of Technology, USA), Takeo Watanabe (Boston University), Joel Voss (Beckman Institute, University of Illinois Urbana-Champaign, USA), Alex Maier (National Institute of Mental Health, NIH)

Symposium Description

Historically, the pervading assumption among sensory psychologists has been that attention and awareness are intimately linked, if not identical, processes. However, a number of recent authors have argued that these are two distinct processes, with different functions and underlying neuronal mechanisms. If this position were correct, we should be able to dissociate the effects of attention and awareness with some experimental manipulation.  Furthermore, we might expect extreme cases of dissociation, such as when attention and awareness have opposing effects on some task performance and its underlying neuronal activity. In the last decade, a number of findings have been taken as support for the notion that attention and awareness are distinct cognitive processes.  In our symposium, we will review some of these results and introduce psychophysical methods to manipulate top-down attention and awareness independently.  Throughout the symposium, we showcase the successful application of these methods to human psychophysics, fMRI and EEG as well as monkey electrophysiology.

First, Nao Tsuchiya will set the stage for the symposium by offering a brief review of recent psychophysical studies that support the idea of awareness without attention as well as attention without awareness.  After discussing some of the methodological limitations of these approaches, Jeroen VanBoxtel will show direct evidence that attention and awareness can result in opposite effects for the formation of afterimages. Takeo Watanabe’s behavioral paradigm will demonstrate that subthreshold motion can be more distracting than suprathreshold motion.  He will go on to show the neuronal substrate of this counter-intuitive finding with fMRI.  Joel Voss will describe how perceptual recognition memory can occur without awareness following manipulations of attention, and how these effects result from changes in the fluency of neural processing in visual cortex measured by EEG.  Finally, Alexander Maier will link these results in the humans studies to neuronal recordings in monkeys, where the attentional state and the visibility of a stimulus are manipulated independently in order to study the neuronal basis of each.

A major theme of our symposium is that emerging evidence supports the notion that attention and awareness are two distinctive neuronal processes.  Throughout the symposium, we will discuss how dissociative paradigms can lead to new progress in the quest for the neuronal processes underlying attention and awareness.  We emphasize that it is important to separate out the effects of attention from the effects of awareness.  Our symposium would benefit most vision scientists, interested in visual attention or visual awareness because the methodologies we discuss would inform them of paradigms that can dissociate attention from awareness. Given the novelty of these findings, our symposium will cover a terrain that remains largely untouched by the main program.

Abstracts

The relationship between top-down attention and conscious awareness

Nao Tsuchiya, California Institute of Technology, USA, Tamagawa University, Japan

Although a claim that attention and awareness are different has been suggested before, it has been difficult to show clear dissociations due to their tight coupling in normal situations; top-down attention and visibility of stimulus both improve the performance in most visual tasks. As proposed in this workshop, however, putative difference in their functional and computational roles implies a possibility that attention and awareness may affect visual processing in different ways.  After brief discussion on the functional and computational roles of attention and awareness, we will introduce psychophysical methods that independently manipulate visual awareness and spatial, focal top-down attention and review the recent studies showing consciousness without attention and attention without consciousness.

Opposing effects of attention and awareness on afterimages

Jeroen J.A. van Boxtel, California Institute of Technology, USA

The brain’s ability to handle sensory information is influenced by both selective attention and awareness. There is still no consensus on the exact relationship between these two processes and whether or not they are distinct. So far, no experiment simultaneously manipulated both, which severely hampers discussions on this issue. We here describe a full factorial study of the influences of attention and awareness (as assayed by visibility) on afterimages. We investigated the duration of afterimages for all four combinations of high versus low attention and visible versus invisible grating. We demonstrate that selective attention and visual awareness have opposite effects: paying attention to the grating decreases the duration of its afterimage, while consciously seeing the grating increases afterimage duration. We moreover control for various possible confounds, including stimulus, and task changes. These data provide clear evidence for distinctive influences of selective attention and awareness on visual perception.

Role of subthreshold stimuli in task-performance and its underlying mechanism

Takeo Watanabe, Boston University

Considerable evidence exists indicating that a stimulus which is subthreshold and thus consciously invisible, influences brain activity and behavioral performance. However, it is not clear how subthreshold stimuli are processed in the brain. We found that a task-irrelevant subthreshold coherent motion leads to stronger disturbance in task performance than suprathreshold motion. With the subthreshold motion, fMRI activity in the visual cortex was higher, but activity in the dorsolateral prefrontal cortex (DLPFC) was lower, than with suprathreshold motion. The results of the present study demonstrate two important points. First, a weak task-irrelevant stimulus feature which is below but near the perceptual threshold more strongly activates visual area (MT+) which is highly related to the stimulus feature and more greatly disrupts task performance. This contradicts the general view that irrelevant signals that are stronger in stimulus properties more greatly influence the brain and performance and that the influence of a subthreshold stimulus is smaller than that of suprathreshold stimuli. Second, the results may reveal important bidirectional interactions between a cognitive controlling system and the visual system. LPFC, which has been suggested to provide inhibitory control on task-irrelevant signals, may have a higher detection threshold for incoming signals than the visual cortex. Task-irrelevant signals around the threshold level may be sufficiently strong to be processed in the visual system but not strong enough for LPFC to “notice” and, therefore, to provide effective inhibitory control on the signals. In this case, such signals may remain uninhibited, take more resources for a task-irrelevant distractor, and leave fewer resources for a given task, and disrupt task performance more than a suprathreshold signal. On the other hand, suprathreshold coherent motion may be “noticed”, given successful inhibitory control by LPFC, and leave more resources for a task. This mechanism may underlie the present paradoxical finding that subthreshold task-irrelevant stimuli activate the visual area strongly and disrupt task performance more and could also be one of the reasons why subthreshold stimuli tend to lead to relatively robust effects.

Implicit recognition: Implications for the study of attention and awareness

Joel Voss, Beckman Institute, University of Illinois Urbana-Champaign, USA

Recognition memory is generally accompanied by awareness, such as when a person recollects details about a prior event or feels that a previously encountered face is familiar. Moreover, recognition is usually benefited by attention. I will describe a set of experiments that yielded unprecedented dissociations between recognition, attention, and awareness. These effects were produced by carefully selecting experimental parameters to minimize contributions from memory encoding and retrieval processes that normally produce awareness, such as semantic elaboration. Fractal images were viewed repeatedly, and repeat images could be discriminated from novel images that were perceptually similar. Discrimination responses were highly accurate even when subjects reported no awareness of having seen the images previously, a phenomenon we describe as implicit recognition. Importantly, implicit recognition was dissociated from recognition accompanied by awareness based on differences in the relationship between confidence and accuracy for each memory type. Diversions of attention at encoding greatly increased the prevalence of implicit recognition. Electrophysiological responses obtained during memory testing showed that implicit recognition was based on similar neural processes as implicit priming. Both implicit recognition and implicit priming for fractal images included repetition-induced reductions in the magnitude of neural activity in visual cortex, an indication of visual processing fluency.  These findings collectively indicate that attention during encoding biases the involvement of different memory systems. High attention recruits medial temporal structures that promote memory with awareness whereas low attention yields cortical memory representations that are independent from medial temporal contributions, such that implicit recognition can result.

Selective attention and perceptual suppression independently modulate contrast change detection.

Alex Maier, National Institute of Mental Health, NIH

Visual awareness bears a complex relationship to selective attention, with some evidence suggesting they can be operationally dissociated (Koch & Tsuchiya 2007). As a first step in the neurophysiological investigation of this dissociation, we developed a novel paradigm that allows for the independent manipulation of visual attention and stimulus awareness in nonhuman primates using a cued perceptual suppression paradigm. We trained two macaque monkeys to detect a slight decrement in stimulus contrast occurring at random time intervals. This change was applied to one of eight isoeccentric sinusoidal grating stimuli with equal probability. In 80% of trials a preceding cue at the fixation spot indicated the correct position of the contrast change. Previous studies in humans demonstrated that such cuing leads to increased selective attention under similar conditions (Posner et al. 1984). In parallel with behavioral cuing, we used binocular rivalry flash suppression (Wolfe 1984) to render the attended stimuli invisible on half the trials. The combined paradigm allows for independent assessment of the effects of spatial attention and perceptual suppression on the detection threshold of the contrast decrement, as well as on neural responses. Our behavioral results suggest that the visibility of the decrement is affected independently by attention and perceptual state. We will present preliminary electrophysiological data from early visual cortex that suggest independent contributions of these two factors to the modulation of neural responses to a visual stimulus.