Distributed neural systems for the generation of visual images

Visual perception of houses, faces, and chairs evoke differential responses in ventral temporal cortex. Using fMRI, we compared activations evoked by perception and imagery of these object categories. We found content-related activation during imagery in extrastriate cortex, but this activity was restricted to small subsets of the regions that showed category-related activation during perception. Within ventral temporal cortex, activation during imagery evoked stronger responses on the left whereas perception evoked stronger responses on the right. Additionally, visual imagery evoked activity in parietal and frontal cortex, but this activity was not content related. These results suggest that content-related activation during imagery in visual extrastriate cortex may be implemented by "top-down" mechanisms in parietal and frontal cortex that mediate the retrieval of face and object representations from long-term memory and their maintenance through visual imagery.     

Perceptual grouping of biological motion promotes binocular rivalry

Investigation of perceptual rivalry between conflicting stimuli presented one to each eye can further understanding of the neural underpinnings of conscious visual perception. During rivalry, visual awareness fluctuates between perceptions of the two stimuli. Here, we demonstrate that high-level perceptual grouping can promote rivalry between stimulus pairs that would otherwise be perceived as nonrivalrous. Perceptual grouping was generated with point-light walker stimuli that simulate human motion, visible only as lights placed on the joints. Although such walking figures are unrecognizable when stationary, recognition judgments as complex as gender and identity can accurately be made from animated displays, demonstrating the efficiency with which our visual system can group dynamic local signals into a globally coherent walking figure. We find that point-light walker stimuli presented one to each eye and in different colors and configurations results in strong rivalry. However, rivalry is minimal when the two walkers are split between the eyes or both presented to one eye. This pattern of results suggests that processing animated walker figures promotes rivalry between signals from the two eyes rather than between higher-level representations of the walkers. This leads us to hypothesize that awareness during binocular rivalry involves the integrated activity of high-level perceptual mechanisms in conjunction with lower-level ocular suppression modulated via cortical feedback.     

Contrast and Strength of Visual Memory and Imagery Differentially Affect Visual Perception

Visual short-term memory (VSTM) and visual imagery have been shown to modulate visual perception. However, how the subjective experience of VSTM/imagery and its contrast modulate this process has not been investigated. We addressed this issue by asking participants to detect brief masked targets while they were engaged either in VSTM or visual imagery. Subjective experience of memory/imagery (strength scale), and the visual contrast of the memory/mental image (contrast scale) were assessed on a trial-by-trial basis. For both VSTM and imagery, contrast of the memory/mental image was positively associated with reporting target presence. Consequently, at the sensory level, both VSTM and imagery facilitated visual perception. However, subjective strength of VSTM was positively associated with visual detection whereas the opposite pattern was found for imagery. Thus the relationship between subjective strength of memory/imagery and visual detection are qualitatively different for VSTM and visual imagery, although their impact at the sensory level appears similar. Our results furthermore demonstrate that imagery and VSTM are partly dissociable processes.     

United we sense, divided we fail: context-driven perception of ambiguous visual stimuli

Ambiguous visual stimuli provide the brain with sensory information that contains conflicting evidence for multiple mutually exclusive interpretations. Two distinct aspects of the phenomenological experience associated with viewing ambiguous visual stimuli are the apparent stability of perception whenever one perceptual interpretation is dominant, and the instability of perception that causes perceptual dominance to alternate between perceptual interpretations upon extended viewing. This review summarizes several ways in which contextual information can help the brain resolve visual ambiguities and construct temporarily stable perceptual experiences. Temporal context through prior stimulation or internal brain states brought about by feedback from higher cortical processing levels may alter the response characteristics of specific neurons involved in rivalry resolution. Furthermore, spatial or crossmodal context may strengthen the neuronal representation of one of the possible perceptual interpretations and consequently bias the rivalry process towards it. We suggest that contextual influences on perceptual choices with ambiguous visual stimuli can be highly informative about the neuronal mechanisms of context-driven inference in the general processes of perceptual decision-making.     

Attention driven phantom vision: measuring the sensory strength of attentional templates and their relation to visual mental imagery and aphantasia

When we search for an object in an array or anticipate attending to a future object, we create an ‘attentional template'' of the object. The definitions of attentional templates and visual imagery share many similarities as well as many of the same neural characteristics. However, the phenomenology of these attentional templates and their neural similarities to visual imagery and perception are rarely, if ever discussed. Here, we investigate the relationship between these two forms of non-retinal phantom vision through the use of the binocular rivalry technique, which allows us to measure the sensory strength of attentional templates in the absence of concurrent perceptual stimuli. We find that attentional templates correlate with both feature-based attention and visual imagery. Attentional templates, like imagery, were significantly disrupted by the presence of irrelevant visual stimuli, while feature-based attention was not. We also found that a special population who lack the ability to visualize (aphantasia), showed evidence of feature-based attention when measured using the binocular rivalry paradigm, but not attentional templates. Taken together, these data suggest functional similarities between attentional templates and visual imagery, advancing the theory of visual imagery as a general simulation tool used across cognition.This article is part of the theme issue ‘Offline perception: voluntary and spontaneous perceptual experiences without matching external stimulation’.     

Neural representation of visual objects: encoding and top-down activation

Knowledge or experiences are voluntarily recalled from memory by reactivation of their neural representations in the association cortex. Mnemonic representations of visual objects, located in the ventral processing stream of visual perception, provide the best indication of how neuronal codes are created, organized and reactivated. Associative codes are created by neurons that have the ability to link the representations of temporally associated stimuli. Recent experiments suggest that not only bottom-up signals from the retina but also top-down signals from the prefrontal cortex can trigger the retrieval of associative codes, which may serve as a neural basis for conscious recall.     

Single units and conscious vision.

Figures that can be seen in more than one way are invaluable tools for the study of the neural basis of visual awareness, because such stimuli permit the dissociation of the neural responses that underlie what we perceive at any given time from those forming the sensory representation of a visual pattern. To study the former type of responses, monkeys were subjected to binocular rivalry, and the response of neurons in a number of different visual areas was studied while the animals reported their alternating percepts by pulling levers. Perception-related modulations of neural activity were found to occur to different extents in different cortical visual areas. The cells that were affected by suppression were almost exclusively binocular, and their proportion was found to increase in the higher processing stages of the visual system. The strongest correlations between neural activity and perception were observed in the visual areas of the temporal lobe. A strikingly large number of neurons in the early visual areas remained active during the perceptual suppression of the stimulus, a finding suggesting that conscious visual perception might be mediated by only a subset of the cells exhibiting stimulus selective responses. These physiological findings, together with a number of recent psychophysical studies, offer a new explanation of the phenomenon of binocular rivalry. Indeed, rivalry has long been considered to be closely linked with binocular fusion and stereopsis, and the sequences of dominance and suppression have been viewed as the result of competition between the two monocular channels. The physiological data presented here are incompatible with this interpretation. Rather than reflecting interocular competition, the rivalry is most probably between the two different central neural representations generated by the dichoptically presented stimuli. The mechanisms of rivalry are probably the same as, or very similar to, those underlying multistable perception in general, and further physiological studies might reveal much about the neural mechanisms of our perceptual organization.     

Mental imagery and visual working memory

Visual working memory provides an essential link between past and future events. Despite recent efforts, capacity limits, their genesis and the underlying neural structures of visual working memory remain unclear. Here we show that performance in visual working memory--but not iconic visual memory--can be predicted by the strength of mental imagery as assessed with binocular rivalry in a given individual. In addition, for individuals with strong imagery, modulating the background luminance diminished performance on visual working memory and imagery tasks, but not working memory for number strings. This suggests that luminance signals were disrupting sensory-based imagery mechanisms and not a general working memory system. Individuals with poor imagery still performed above chance in the visual working memory task, but their performance was not affected by the background luminance, suggesting a dichotomy in strategies for visual working memory: individuals with strong mental imagery rely on sensory-based imagery to support mnemonic performance, while those with poor imagery rely on different strategies. These findings could help reconcile current controversy regarding the mechanism and location of visual mnemonic storage.     

Closing the mind's eye: incoming luminance signals disrupt visual imagery

Mental imagery has been associated with many cognitive functions, both high and low-level. Despite recent scientific advances, the contextual and environmental conditions that most affect the mechanisms of visual imagery remain unclear. It has been previously shown that the greater the level of background luminance the weaker the effect of imagery on subsequent perception. However, in these experiments it was unclear whether the luminance was affecting imagery generation or storage of a memory trace. Here, we report that background luminance can attenuate both mental imagery generation and imagery storage during an unrelated cognitive task. However, imagery generation was more sensitive to the degree of luminance. In addition, we show that these findings were not due to differential dark adaptation. These results suggest that afferent visual signals can interfere with both the formation and priming-memory effects associated with visual imagery. It follows that background luminance may be a valuable tool for investigating imagery and its role in various cognitive and sensory processes.     

Emergence and transmission of visual awareness through optical coding in the brain: A redox molecular hypothesis on visual mental imagery

Does the primary visual cortex mediate consciousness for higher-level stages of information processing by providing an outlet for mental imagery? Evidence based on neural electrical activity is inconclusive as reflected in the “imagery debate” in cognitive science. Neural information and activity, however, also depend on regulated biophoton (optical) signaling. During encoding and retrieval of visual information, regulated electrical (redox) signals of neurons are converted into synchronized biophoton signals by bioluminescent radical processes. That is, visual information may be represented by regulated biophotons of mitochondrial networks in retinotopically organized cytochrome oxidase-rich neural networks within early visual areas. Therefore, we hypothesize that regulated biophotons can generate intrinsic optical representations in the primary visual cortex and then propagate variably degraded versions along cytochrome oxidase pathways during both perception and imagery. Testing this hypothesis requires to establish a methodology for measurement of in vivo and/or in vitro increases of biophoton emission in humans' brain during phosphene inductions by transcranial magnetic stimulation and to compare the decrease in phosphene thresholds during transcranial magnetic stimulation and imagery. Our hypothesis provides a molecular mechanism for the visual buffer and for imagery as the prevalent communication mode (through optical signaling) within the brain. If confirmed empirically, this hypothesis could resolve the imagery debate and the underlying issue of continuity between perception and abstract thought.     

Attribute Pair-Based Visual Recognition and Memory

Background

In the human visual system, different attributes of an object, such as shape, color, and motion, are processed separately in different areas of the brain. This raises a fundamental question of how are these attributes integrated to produce a unified perception and a specific response. This “binding problem” is computationally difficult because all attributes are assumed to be bound together to form a single object representation. However, there is no firm evidence to confirm that such representations exist for general objects.

Methodology/Principal Findings

Here we propose a paired-attribute model in which cognitive processes are based on multiple representations of paired attributes. In line with the model''s prediction, we found that multiattribute stimuli can produce an illusory perception of a multiattribute object arising from erroneous integration of attribute pairs, implying that object recognition is based on parallel perception of paired attributes. Moreover, in a change-detection task, a feature change in a single attribute frequently caused an illusory perception of change in another attribute, suggesting that multiple pairs of attributes are stored in memory.

Conclusions/Significance

The paired-attribute model can account for some novel illusions and controversial findings on binocular rivalry and short-term memory. Our results suggest that many cognitive processes are performed at the level of paired attributes rather than integrated objects, which greatly facilitates the binding problem and provides simpler solutions for it.     

Is object search mediated by object-based or image-based representations?

Recent research suggests that visually specific memory representations for previously fixated objects are maintained during scene perception. Here we investigate the degree of visual specificity by asking whether the memory representations are image-based or object-based. To that end we measured the effects of object orientation on the time to search for a familiar object from amongst a set of 7 familiar distractors arranged in a circular array. Search times were found to depend on the relative orientations of the target object and the probe object for both familiar and novel objects. This effect was found to be partly an image matching effect but there was also an advantage shown for the object's canonical view for familiar objects. Orientation effects were maintained even when the target object was specified as having unique or similar shape properties relative to the distractors. Participants' eye movements were monitored during two of the experiments. Eye movement patterns revealed selection for object shape and object orientation during the search process. Our findings provide evidence for object representations during search that are detailed and share image-based characteristics with more high-level characteristics from object memory.     

Imagine Jane and identify John: face identity aftereffects induced by imagined faces

It is not known whether prolonged exposure to perceived and imagined complex visual images produces similar shifts in subsequent perception through selective adaptation. This question is important because a positive finding would suggest that perception and imagery of visual stimuli are mediated by shared neural networks. In this study, we used a selective adaptation procedure designed to induce high-level face-identity aftereffects--a phenomenon in which extended exposure to a particular face facilitates recognition of subsequent faces with opposite features while impairing recognition of all other faces. We report here that adaptation to either real or imagined faces produces a similar shift in perception and that identity boundaries represented in real and imagined faces are equivalent. Together, our results show that identity information contained in imagined and real faces produce similar behavioral outcomes. Our findings of high-level visual aftereffects induced by imagined stimuli can be taken as evidence for the involvement of shared neural networks that mediate perception and imagery of complex visual stimuli.     

Tracking the mind's image in the brain I: time-resolved fMRI during visuospatial mental imagery

Mental imagery, the generation and manipulation of mental representations in the absence of sensory stimulation, is a core element of numerous cognitive processes. We investigate the cortical mechanisms underlying imagery and spatial analysis in the visual domain using event-related functional magnetic resonance imaging during the mental clock task. The time-resolved analysis of cortical activation from auditory perception to motor response reveals a sequential activation of the left and right posterior parietal cortex, suggesting that these regions perform distinct functions in this imagery task. This is confirmed by a trial-by-trial analysis of correlations between reaction time and onset, width, and amplitude of the hemodynamic response. These findings pose neurophysiological constraints on cognitive models of mental imagery.     

Color and luminance influence, but can not explain, binocular rivalry onset bias

When an observer is presented with dissimilar images to the right and left eye, the images will alternate every few seconds in a phenomenon known as binocular rivalry. During sustained viewing, the timing of these switches appears to be unpredictable. Recent research has suggested that the initial 'onset' period of rivalry is not random and may be different in its neural mechanism than subsequent dominance periods. It is known that differences in luminance and contrast have a significant influence on the average dominance during sustained rivalry and that perception of luminance can vary between individuals and across the visual field. We therefore investigated whether perception of luminance contrast plays a role in onset rivalry. Observers viewed rival targets of equal brightness for brief presentations in eight locations of the near periphery and reported the color that was first dominant in each location. Results show that minimizing differences in brightness and contrast yields a stronger pattern of onset dominance bias and reveals evidence of monocular dominance. The results suggest that both contrast and monocular dominance play a role in onset dominance, though neither can fully explain the effect.     

On the perception of probable things: neural substrates of associative memory, imagery, and perception

Perception is influenced both by the immediate pattern of sensory inputs and by memories acquired through prior experiences with the world. Throughout much of its illustrious history, however, study of the cellular basis of perception has focused on neuronal structures and events that underlie the detection and discrimination of sensory stimuli. Relatively little attention has been paid to the means by which memories interact with incoming sensory signals. Building upon recent neurophysiological/behavioral studies of the cortical substrates of visual associative memory, I propose a specific functional process by which stored information about the world supplements sensory inputs to yield neuronal signals that can account for visual perceptual experience. This perspective represents a significant shift in the way we think about the cellular bases of perception.     

Touch Interacts with Vision during Binocular Rivalry with a Tight Orientation Tuning

Multisensory integration is a common feature of the mammalian brain that allows it to deal more efficiently with the ambiguity of sensory input by combining complementary signals from several sensory sources. Growing evidence suggests that multisensory interactions can occur as early as primary sensory cortices. Here we present incompatible visual signals (orthogonal gratings) to each eye to create visual competition between monocular inputs in primary visual cortex where binocular combination would normally take place. The incompatibility prevents binocular fusion and triggers an ambiguous perceptual response in which the two images are perceived one at a time in an irregular alternation. One key function of multisensory integration is to minimize perceptual ambiguity by exploiting cross-sensory congruence. We show that a haptic signal matching one of the visual alternatives helps disambiguate visual perception during binocular rivalry by both prolonging the dominance period of the congruent visual stimulus and by shortening its suppression period. Importantly, this interaction is strictly tuned for orientation, with a mismatch as small as 7.5° between visual and haptic orientations sufficient to annul the interaction. These results indicate important conclusions: first, that vision and touch interact at early levels of visual processing where interocular conflicts are first detected and orientation tunings are narrow, and second, that haptic input can influence visual signals outside of visual awareness, bringing a stimulus made invisible by binocular rivalry suppression back to awareness sooner than would occur without congruent haptic input.     

Olfaction spontaneously highlights visual saliency map

Attention is intrinsic to our perceptual representations of sensory inputs. Best characterized in the visual domain, it is typically depicted as a spotlight moving over a saliency map that topographically encodes strengths of visual features and feedback modulations over the visual scene. By introducing smells to two well-established attentional paradigms, the dot-probe and the visual-search paradigms, we find that a smell reflexively directs attention to the congruent visual image and facilitates visual search of that image without the mediation of visual imagery. Furthermore, such effect is independent of, and can override, top-down bias. We thus propose that smell quality acts as an object feature whose presence enhances the perceptual saliency of that object, thereby guiding the spotlight of visual attention. Our discoveries provide robust empirical evidence for a multimodal saliency map that weighs not only visual but also olfactory inputs.     

Negative BOLD differentiates visual imagery and perception

Recent studies emphasize the overlap between the neural substrates of visual perception and visual imagery. However, the subjective experiences of imagining and seeing are clearly different. Here we demonstrate that deactivation of auditory cortex (and to some extent of somatosensory and subcortical visual structures) as measured by BOLD functional magnetic resonance imaging unequivocally differentiates visual imagery from visual perception. During visual imagery, auditory cortex deactivation negatively correlates with activation in visual cortex and with the score in the subjective vividness of visual imagery questionnaire (VVIQ). Perception of the world requires the merging of multisensory information so that, during seeing, information from other sensory systems modifies visual cortical activity and shapes experience. We suggest that pure visual imagery corresponds to the isolated activation of visual cortical areas with concurrent deactivation of "irrelevant" sensory processing that could disrupt the image created by our "mind's eye."     

Non-Attended Representations are Perceptual Rather than Unconscious in Nature

Introspectively we experience a phenomenally rich world. In stark contrast, many studies show that we can only report on the few items that we happen to attend to. So what happens to the unattended objects? Are these consciously processed as our first person perspective would have us believe, or are they – in fact – entirely unconscious? Here, we attempt to resolve this question by investigating the perceptual characteristics of visual sensory memory. Sensory memory is a fleeting, high-capacity form of memory that precedes attentional selection and working memory. We found that memory capacity benefits from figural information induced by the Kanizsa illusion. Importantly, this benefit was larger for sensory memory than for working memory and depended critically on the illusion, not on the stimulus configuration. This shows that pre-attentive sensory memory contains representations that have a genuinely perceptual nature, suggesting that non-attended representations are phenomenally experienced rather than unconscious.