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.     

Reference,perception, and attention

I examine John Campbell’s claim that the determination of the reference of a perceptual demonstrative requires conscious visual object-based selective attention. I argue that although Campbell’s claim to the effect that, first, a complex binding parameter is needed to establish the referent of a perceptual demonstrative, and, second, that this referent is determined independently of, and before, the application of sortals is correct, this binding parameter does not require object-based attention for its construction. If object-based attention were indeed required then the determination of the referent would necessarily involve the application of sortal concepts, since object-based attention initiates top-down cognitive effects on visual processing. I also examine Mohan Matthen’s claim that reference to objects is established only through the visual processing in the dorsal visual stream and argue that although it is true that processing in the dorsal stream can determine reference, a thesis that goes against Campbell’s view that the determination of the referent requires conscious attention, processing along the ventral visual stream can also establish the reference of perceptual demonstratives. It also claim that Matthen’s account of dorsal processing underestimates the kind of information processed along the dorsal stream and this has some implications regarding perceptual demonstratives reference fixing.

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.     

Conscious Vision in Action

It is natural to assume that the fine‐grained and highly accurate spatial information present in visual experience is often used to guide our bodily actions. Yet this assumption has been challenged by proponents of the Two Visual Systems Hypothesis (TVSH), according to which visuomotor programming is the responsibility of a “zombie” processing stream whose sources of bottom‐up spatial information are entirely non‐conscious (Clark, 2007, 2009; Goodale & Milner, 1992, 2004a; Milner & Goodale, 1995/2006, 2008). In many formulations of TVSH, the role of conscious vision in action is limited to “recognizing objects, selecting targets for action, and determining what kinds of action, broadly speaking, to perform” (Clark, 2007, p. 570). Our aim in this study is to show that the available evidence not only fails to support this dichotomous view but actually reveals a significant role for conscious vision in motor programming, especially for actions that require deliberate attention.     

Sub-threshold cuing: Saccadic responses to low-contrast,peripheral, transient visual landmark cues

Dorsal stream visual encoding was studied in three experiments, by examining effects of peripheral landmark cues on eye movements. Stimulus features and task structure were tailored to physiological and functional characterisations of the dorsal visual stream. Sub-discriminable peripheral stimuli served as landmark cue stimuli. In Experiments 1 and 2, orienting behaviour in response to cues and targets differed for participants with relatively low and relatively high peripheral contrast thresholds. In Experiment 1, low, but not high-threshold participants oriented towards landmark cues that could not be discriminated consciously. However, in Experiment 3, high-, but not low-threshold participants oriented towards near threshold cues. Hence, under appropriate conditions both groups of participants oriented in response to brief, low-contrast, peripheral information. We propose that landmark cueing may provide a useful tool for measuring individual differences in dorsal stream processing and dynamic aspects of visual functioning and awareness.     

Spatial attention and conscious perception: the role of endogenous and exogenous orienting

Attention has often been considered to be a gateway to consciousness (Posner, Proceedings of the National Academy of Sciences of the United States of America, 91(16), 7398–7403, 1994). However, its relationship with conscious perception (CP) remains highly controversial. While theoretical models and experimental data support the role of attention in CP (Chica, Lasaponara, Lupiáñez, Doricchi, &; Bartolomeo, NeuroImage, 51, 1205–1212, 2010; Dehaene, Changeux, Naccache, Sackur, &; Sergent, Trends in Cognitive Sciences, 10, 204–211, 2006; Mack &; Rock, Inattentional blindness, 1998), recent studies have claimed that at least some forms of attention—endogenous or top-down spatial attention—are neither sufficient nor necessary for CP (Koch &; Tsuchiya, Trends in Cognitive Sciences, 11, 16–22, 2007). In the present experiments, we demonstrate the importance of exogenously triggered attention for the modulation of CP. Weak or null effects were instead observed when attention was triggered endogenously. Our data are discussed in the framework of recent neuropsychological models (Dehaene et al., Trends in Cognitive Sciences, 10, 204–211, 2006), postulating that activity within reverberating frontoparietal networks, as colocalized with spatial--orienting systems, is the brain correlate of consciously processed information.     

Dorsal and ventral visual streams: Typical and atypical development

The literature on visuospatial processing describes two distinct pathways within the brain: a dorsal route extending from the visual cortex into the parietal lobes that is critical for spatial processing and a ventral route extending from the visual cortex into the temporal lobes that is critical for form perception. These visual streams appear to differ in their developmental trajectories and their vulnerabilities to diverse neurodevelopmental conditions. The present work aims to investigate development and vulnerability in two aspects of dorsal and ventral visual-stream function, namely attention to location and attention to identity. In Study 1, we compare typically-developing (TD) youth aged 9 to 16 years with young adults aged 18 to 22 years on computerized location and identity tasks. In Study 2, we compare children and adolescents who have congenital hypothyroidism (CH), a pediatric endocrine disorder, with age-matched TD controls on the same tasks. The results from Study 1 show that the youths were less accurate than the adults at judging identity, whereas both groups were equally accurate at judging location. The results from Study 2 show that the youths with CH were slower but not less accurate than the TD youths in making both identity and location judgments. The results are interpreted as signifying later development of ventral (identity) stream functions compared to dorsal (location) but equal vulnerability of both functions in CH.     

Face and location processing in children with early unilateral brain injury

Human visuospatial functions are commonly divided into those dependent on the ventral visual stream (ventral occipitotemporal regions), which allows for processing the ‘what’ of an object, and the dorsal visual stream (dorsal occipitoparietal regions), which allows for processing ‘where’ an object is in space. Information about the development of each of the two streams has been accumulating, but very little is known about the effects of injury, particularly very early injury, on this developmental process. Using a set of computerized dorsal and ventral stream tasks matched for stimuli, required response, and difficulty (for typically-developing individuals), we sought to compare the differential effects of injury to the two systems by examining performance in individuals with perinatal brain injury (PBI), who present with selective deficits in visuospatial processing from a young age. Thirty participants (mean = 15.1 years) with early unilateral brain injury (15 right hemisphere PBI, 15 left hemisphere PBI) and 16 matched controls participated. On our tasks children with PBI performed more poorly than controls (lower accuracy and longer response times), and this was particularly prominent for the ventral stream task. Lateralization of PBI was also a factor, as the dorsal stream task did not seem to be associated with lateralized deficits, with both PBI groups showing only subtle decrements in performance, while the ventral stream task elicited deficits from RPBI children that do not appear to improve with age. Our findings suggest that early injury results in lesion-specific visuospatial deficits that persist into adolescence. Further, as the stimuli used in our ventral stream task were faces, our findings are consistent with what is known about the neural systems for face processing, namely, that they are established relatively early, follow a comparatively rapid developmental trajectory (conferring a vulnerability to early insult), and are biased toward the right hemisphere.     

Mapping the similarity space of paintings: Image statistics and visual perception

What makes two images look similar? Here we test the hypothesis that perceived similarity of artwork is related to basic image statistics to which the early visual system is attuned. In two experiments, we employ multidimensional scaling (MDS) analysis of paired-image similarity ratings from observers for paintings. Two sets of images, classified as “landscapes” and “portraits/still-life”, are tested separately. For the landscapes, we find that one of the first two MDS scales of similarity is strongly correlated with a basic greyscale image statistic, whereas the other dimension can be accounted for by a semantic variable (representation of people). For portrait/still-life, the first two MDS scales of similarity are most highly correlated with semantic variables. Linear combinations of statistical and nonstatistical features achieve improved predictive values for the first two MDS scales for both sets. The statistics that play the largest role in shaping similarity judgements in our tests are the activity fraction measure of sparseness and the log-log slope of the spatial frequency amplitude spectrum. We discuss these results in the context of scene perception and in terms of efficient coding of statistical regularities in scenes.     

Flexible cue combination in the guidance of attention in visual search

Hodsoll and Humphreys (2001) have assessed the relative contributions of stimulus-driven and user-driven knowledge on linearly- and nonlinearly separable searches. However, the target feature used to determine linear separability in their task (i.e., target size) was required to locate the target. In the present work, we investigated the contributions of stimulus-driven and user-driven knowledge when a linearly- or a nonlinearly-separable feature is available but not required for target identification. We asked observers to complete a series of standard color × orientation conjunction searches in which target size was either linearly- or nonlinearly separable from the size of the distractors. When guidance by color × orientation and guidance by size information are both available, observers rely on whichever information results in the best search efficiency. This is the case irrespective of whether we provide target foreknowledge by blocking stimulus conditions, suggesting that feature information is used in both a stimulus-driven and a user-driven fashion.     

The development and learning of the visual control of movement: An ecological perspective

We compare development and learning of the visual control of movement from an ecological perspective. It is argued that although the constraints that are imposed upon development and learning are vastly different, both are best characterised as a change towards the use of more useful and specifying optic variables. Implicit learning, in which awareness is drawn away from movement execution, is most appropriate to accomplish this change in optic variable use, although its contribution in development is more contentious. Alternatively, learning can also be affected by explicit processes. We propose that explicit learning would typically invoke vision for perception processes instead of the designated vision for action processes. It is for that reason that after explicit learning performance is more easily compromised in the face of pressure or disorders. We present a way to deal with the issue of explicit learning during infancy.     

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.     

When believing is seeing: The role of predictions in shaping visual perception

The study investigated the influence of predictions on perception—in particular, how strong but erroneous prediction coupled with poor sensory data can trigger misperceptions. Using signal detection, we tested whether predictions induced by a semantic cue change the recognition threshold (criterion) or the subjectively perceived differences between stimuli (sensitivity). In a series of 3 experiments, participants observed pictures of (a) real objects distorted to various extents (targets), (b) noise with elements corresponding to meaningful objects (foils), or (c) nonsense images (noise). Stimuli were preceded either by a semantic cue or by a blank screen with equal probability. Presence of the cue resulted in a more liberal criterion, but only for targets and foils. The cue decreased sensitivity between the distorted targets, but increased sensitivity between the targets and noise—that is, the cue increased between-class differences, but decreased within-class differences. When there was no correspondence between prediction and the sensory input, prediction actually increased the chances of correctly rejecting noise. The influence of the cue was strongest for the moderately distorted targets and foils—when uncertainty related to the bottom-up input was the highest.     

Language-guided visual processing affects reasoning: The role of referential and spatial anchoring

Language is more than a source of information for accessing higher-order conceptual knowledge. Indeed, language may determine how people perceive and interpret visual stimuli. Visual processing in linguistic contexts, for instance, mirrors language processing and happens incrementally, rather than through variously-oriented fixations over a particular scene. The consequences of this atypical visual processing are yet to be determined. Here, we investigated the integration of visual and linguistic input during a reasoning task. Participants listened to sentences containing conjunctions or disjunctions (Nancy examined an ant and/or a cloud) and looked at visual scenes containing two pictures that either matched or mismatched the nouns. Degree of match between nouns and pictures (referential anchoring) and between their expected and actual spatial positions (spatial anchoring) affected fixations as well as judgments. We conclude that language induces incremental processing of visual scenes, which in turn becomes susceptible to reasoning errors during the language-meaning verification process.     

The influence of visual short-term memory on size perception

We show that perceived size of visual stimuli can be altered by matches between the contents of visual short-term memory and stimuli in the scene. Observers were presented with a colour cue (to hold in working memory or to merely identify) and subsequently had to indicate which of the two different-coloured objects presented simultaneously on the screen appeared bigger (or smaller). One of the two objects for size judgements had the same colour as the cue (matching stimulus) and the other did not (mismatching stimulus). Perceived object size was decreased by the reappearance of the recently seen cue, as there were more size judgement errors on trials where the matching stimulus was physically bigger (relative to the mismatching stimulus) than on trials where the matching stimulus was physically smaller. The effect occurred regardless of whether the visual cue was actively maintained in working memory or was merely identified. The effect was unlikely generated by the allocation of attention, because shifting attention to a visual stimulus actually increased its perceived size. The findings suggest that visual short-term memory, whether explicit or implicit, can decrease the perceived size of subsequent visual stimuli.     

Visual orienting in response to attentional cues: Spatial correspondence is critical,conscious awareness is not

Three experiments examined visual orienting in response to spatial precues. In Experiments 1 and 2, attentional effects of central letters were stimulus driven: Orienting was dependent on the spatial layout of the cue display. When there were no correspondences between spatial features of the cue display and target location, attentional effects were absent, despite a conscious intention to orient in response to the symbolic information carried by the cue letters. In Experiment 3 clear orienting effects were observed when target location corresponded with spatial features of the cue display, but the magnitude of these effects was unaffected by whether participants were aware or unaware of the cue–target relationship. These findings are consistent with the view that (1) spatial correspondences between cues and targets are a critical factor driving visual orienting in cueing paradigms, and (2) attentional effects of spatial precues are largely independent of participants’ conscious awareness of the cue–target relationship.     

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.     

Neuronal correlates of full and partial visual conscious perception

Stimuli may induce only partial consciousness—an intermediate between null and full consciousness—where the presence but not identity of an object can be reported. The differences in the neuronal basis of full and partial consciousness are poorly understood. We investigated if evoked and oscillatory activity could dissociate full from partial conscious perception. We recorded human cortical activity with magnetoencephalography (MEG) during a visual perception task in which stimulus could be either partially or fully perceived. Partial consciousness was associated with an early increase in evoked activity and theta/low-alpha-band oscillations while full consciousness was also associated with late evoked activity and beta-band oscillations. Full from partial consciousness was dissociated by stronger evoked activity and late increase in theta oscillations that were localized to higher-order visual regions and posterior parietal and prefrontal cortices. Our results reveal both evoked activity and theta oscillations dissociate partial and full consciousness.     

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.