Testing the dorsal stream attention hypothesis: Electrophysiological correlates and the effects of ventral stream damage

The roles of dorsal and ventral processing streams in visual orienting and conscious perception were examined in two experiments. The first employed high density EEG with source localization. The second comprised a neuropsychological case study. Visual orienting was assessed with an attention procedure, where peripheral letters cued participants towards a target location. In the perception procedure participants responded to the same letters by performing an explicit conscious discrimination. In Experiment 1, the peripheral letters elicited rapid dorsal stream activation in the attention procedure, and this activation preceded top-down enhancement of target processing in occipital cortex. In the perception procedure early ventral stream activation was seen. In addition, peripheral letters elicited an “early directing attention negativity” (EDAN) over parietal recording sites in the attention procedure, but not in the perception procedure. In Experiment 2, a patient with a bilateral ventral stream lesion but preserved dorsal stream function showed clear disruption to performance in the perception procedure, whilst exhibiting a normal visual orienting effect in the attention procedure. Taken together these findings (1) highlight the distinct roles of the dorsal and ventral streams in attention and perception, and (2) suggest how these streams might interact, via reentrant effects of attention on perceptual processing.     

Are there unconscious perceptual processes?

Blindsight and vision for action seem to be exemplars of unconscious visual processes. However, researchers have recently argued that blindsight is not really a kind of unconscious vision but is rather severely degraded conscious vision. Morten Overgaard and colleagues have recently developed new methods for measuring the visibility of visual stimuli. Studies using these methods show that reported clarity of visual stimuli correlates with accuracy in both normal individuals and blindsight patients. Vision for action has also come under scrutiny. Recent findings seem to show that information processed by the dorsal stream for online action contributes to visual awareness. Some interpret these results as showing that some dorsal stream processes are conscious visual processes (e.g., Gallese, 2007; Jacob & Jeannerod, 2003). The aim of this paper is to provide new support for the more traditional view that blindsight and vision for action are genuinely unconscious perceptual processes. I argue that individuals with blindsight do not have access to the kind of purely qualitative color and size information which normal individuals do. So, even though people with blindsight have a kind of cognitive consciousness, visual information processing in blindsight patients is not associated with a distinctly visual phenomenology. I argue further that while dorsal stream processing seems to contribute to visual awareness, only information processed by the early dorsal stream (V1, V2, and V3) is broadcast to working memory. Information processed by later parts of the dorsal stream (the parietal lobe) never reaches working memory and hence does not correlate with phenomenal awareness. I conclude that both blindsight and vision for action are genuinely unconscious visual processes.     

Tracking the processes behind conscious perception: a review of event-related potential correlates of visual consciousness

Event-related potential (ERP) studies have attempted to discover the processes that underlie conscious visual perception by contrasting ERPs produced by stimuli that are consciously perceived with those that are not. Variability of the proposed ERP correlates of consciousness is considerable: the earliest proposed ERP correlate of consciousness (P1) coincides with sensory processes and the last one (P3) marks postperceptual processes. A negative difference wave called visual awareness negativity (VAN), typically observed around 200 ms after stimulus onset in occipitotemporal sites, gains strong support for reflecting the processes that correlate with, and possibly enable, aware visual perception. Research suggests that the early parts of conscious processing can proceed independently of top-down attention, although top-down attention may modulate visual processing even before consciousness. Evidence implies that the contents of consciousness are provided by interactions in the ventral stream, but indispensable contributions from dorsal regions influence already low-level visual responses.     

Interaction between endogenous and exogenous orienting in crossmodal attention

Using a cue-target paradigm, we investigated the interaction between endogenous and exogenous orienting in cross-modal attention. A peripheral (exogenous) cue was presented after a central (endogenous) cue with a variable time interval. The endogenous and exogenous cues were presented in one sensory modality (auditory in Experiment 1 and visual in Experiment 2) whereas the target was presented in another modality. Both experiments showed a significant endogenous cuing effect (longer reaction times in the invalid condition than in the valid condition). However, exogenous cuing produced a facilitatory effect in both experiments in response to the target when endogenous cuing was valid, but it elicited a facilitatory effect in Experiment 1 and an inhibitory effect in Experiment 2 when endogenous cuing was invalid. These findings indicate that endogenous and exogenous cuing can co-operate in orienting attention to the crossmodal target. Moreover, the interaction between endogenous and exogenous orienting of attention is modulated by the modality between the cue and the target.     

Conscious Vision for Action Versus Unconscious Vision for Action?

David Milner and Melvyn Goodale’s dissociation hypothesis is commonly taken to state that there are two functionally specialized cortical streams of visual processing originating in striate (V1) cortex: a dorsal, action‐related “unconscious” stream and a ventral, perception‐related “conscious” stream. As Milner and Goodale acknowledge, findings from blindsight studies suggest a more sophisticated picture that replaces the distinction between unconscious vision for action and conscious vision for perception with a tripartite division between unconscious vision for action, conscious vision for perception, and unconscious vision for perception. The combination excluded by the tripartite division is the possibility of conscious vision for action. But are there good grounds for concluding that there is no conscious vision for action? There is now overwhelming evidence that illusions and perceived size can have a significant effect on action ( Bruno & Franz, 2009 ; Dassonville & Bala, 2004 ; Franz & Gegenfurtner, 2008 ; McIntosh & Lashley, 2008 ). There is also suggestive evidence that any sophisticated visual behavior requires collaboration between the two visual streams at every stage of the process ( Schenk & McIntosh, 2010 ). I nonetheless want to make a case for the tripartite division between unconscious vision for action, conscious vision for perception, and unconscious vision for perception. My aim here is not to refute the evidence showing that conscious vision can affect action but rather to argue (a) that we cannot gain cognitive access to action‐guiding dorsal stream representations, and (b) that these representations do not correlate with phenomenal consciousness. This vindicates the semi‐conservative view that the dissociation hypothesis is best understood as a tripartite division.     

Do hands attract attention?

Social stimuli, like faces (Kanwisher, McDermott, & Chun, 1997) or bodies (Downing, Jiang, Shuman, & Kanwisher, 2001), engage specific areas within the visual cortex. Behavioural research reveals an attentional bias to these same stimuli (Ro, Friggel, & Lavie, 2007). The current study examined whether there is an attentional bias towards hands, and whether such a bias is distinct from any bias towards human bodies. In a two-alternative, forced-choice dot-probe task, participants saw two side-by-side pictures for 500 ms. A probe dot then appeared on either side and participants indicated where the dot appeared. Participants were significantly faster to respond when the probe location coincided with the location of pictures of bodies, hands, or feet, compared to dogs, starfish, hand tools, toaster ovens, inverted hands, or inverted bodies. Results suggest an attentional bias to bodies and body parts but found no evidence of a difference in attentional advantage of hands over bodies or feet.     

Differences in visual orienting between persons with Down or fragile X syndrome

The voluntary and reflexive orienting abilities of persons with Down syndrome and fragile X syndrome, at average MA levels of approximately 4 and 7 years, were compared with an RT task. Reflexive orienting abilities appeared to develop in accordance with MA for the participants with Down syndrome but not for those with fragile X syndrome. However, both groups showed delayed voluntary orienting. The group differences in reflexive orienting at the low MA level reinforce the practice of separating etiologies and highlight the contribution of rudimentary attentional processes in the study of individuals with mental retardation.     

Effects of background color on detecting spot stimuli in the upper and lower visual fields

Participants were required to detect spot stimuli briefly presented to the upper, central, or lower visual fields. The stimuli were presented either on a green or a red background. Results showed that reaction time (RT) was shorter for the lower visual field (LVF) compared to the upper visual field (UVF). Furthermore, this LVF advantage was significantly reduced in the red background condition compared to the green one. A red light is known to suppress activity of the magno-dominated stream. Therefore, the LVF advantage in RT can be explained as resulting from the biased representation of the magno-dominated stream in the LVF.     

Action control: independent effects of memory and monocular viewing on reaching accuracy

Evidence suggests that perceptual networks in the ventral visual pathway are necessary for action control when targets are viewed with only one eye, or when the target must be stored in memory. We tested whether memory-linked (i.e., open-loop versus memory-guided actions) and monocular-linked effects (i.e., binocular versus monocular actions) on action arise from a common mechanism as suggested by evidence from neuropsychology and psychophysics. Participants viewed targets with either one eye or two (vision: monocular versus binocular) and then reached to touch targets in open-loop and memory-guided conditions (condition: open-loop versus 0, 500, 1000, and 1500 ms delays). Results showed that memory-linked and monocular-linked increases in radial and variable movement error were additive (i.e., main effects of vision and condition, but no interaction). This suggests that the two effects on visuomotor control arise from separate mechanisms, in contrast to evidence from psychophysics and neuropsychology suggesting a common underlying mechanism.     

Altered vision near the hands

The present study explored the manner in which hand position may affect visual processing. We studied three classic visual attention tasks (visual search, inhibition of return, and attentional blink) during which the participants held their hands either near the stimulus display, or far from the display. Remarkably, the hands altered visual processing: people shifted their attention between items more slowly when their hands were near the display. The same results were observed for both visible and invisible hands. This enhancement in vision for objects near the hands reveals a mechanism that could facilitate the detailed evaluation of objects for potential manipulation, or the assessment of potentially dangerous objects for a defensive response.     

The development of exogenous orienting: mechanisms of control

The present study examined exogenous orienting in children ages 6 years (n=14), 10 years (n=13), 14 years (n=14), and adults (n=13). The main purpose was to identify which of the attentional operations underlying exogenous orienting (disengaging, shifting, and/or engaging) improves with age. A simple detection task was used in which single targets were correctly (80%) or incorrectly (20%) cued. The main finding was that disengaging attention alone distinguished the performance of younger children from that of older children and adults, regardless of whether attention alone (covert attention) or attention and associated sensory and motor systems (overt attention) were involved. In addition, our data, in contrast to those reported previously, raise the possibility that even the youngest children tested were able to use the predictability of the cue to enhance their performance. These and related neuroanatomical findings are taken as evidence for the development with age of more flexible control in orienting visual attention.     

Low-level visual attention and its relation to joint attention in autism spectrum disorder

Visual attention is integral to social interaction and is a critical building block for development in other domains (e.g., language). Furthermore, atypical attention (especially joint attention) is one of the earliest markers of autism spectrum disorder (ASD). The current study assesses low-level visual attention and its relation to social attentional processing in youth with ASD and typically developing (TD) youth, aged 7 to 18 years. The findings indicate difficulty overriding incorrect attentional cues in ASD, particularly with non-social (arrow) cues relative to social (face) cues. The findings also show reduced competition in ASD from cues that remain on-screen. Furthermore, social attention, autism severity, and age were all predictors of competing cue processing. The results suggest that individuals with ASD may be biased towards speeded rather than accurate responding, and further, that reduced engagement with visual information may impede responses to visual attentional cues. Once attention is engaged, individuals with ASD appear to interpret directional cues as meaningful. These findings from a controlled, experimental paradigm were mirrored in results from an ecologically valid measure of social attention. Attentional difficulties may be exacerbated during the complex and dynamic experience of actual social interaction. Implications for intervention are discussed.