Prior expectations about the visual world facilitate perception by allowing us to quickly deduce plausible interpretations from noisy and ambiguous data. The neural mechanisms of this facilitation ...remain largely unclear. Here, we used functional magnetic resonance imaging (fMRI) and multivariate pattern analysis (MVPA) techniques to measure both the amplitude and representational content of neural activity in the early visual cortex of human volunteers. We find that while perceptual expectation reduces the neural response amplitude in the primary visual cortex (V1), it improves the stimulus representation in this area, as revealed by MVPA. This informational improvement was independent of attentional modulations by task relevance. Finally, the informational improvement in V1 correlated with subjects’ behavioral improvement when the expected stimulus feature was relevant. These data suggest that expectation facilitates perception by sharpening sensory representations.
► Prior expectation facilitates visual perception ► Valid expectation leads to reduced sensory activity ► Valid expectation leads to enhanced sensory representation ► Prior expectation sharpens the stimulus representation in sensory cortex
In perception, prior expectations allow us to quickly deduce plausible interpretations from noisy and ambiguous data. Here, Kok et al. show that expectation facilitates perception by reducing the overall neural response amplitude, yet increasing the informational content in primary visual cortex.
Human perceptual decisions can be repelled away from (repulsive adaptation) or attracted towards recent visual experience (attractive serial dependence). It is currently unclear whether and how these ...repulsive and attractive biases interact during visual processing and what computational principles underlie these history dependencies. Here we disentangle repulsive and attractive biases by exploring their respective timescales. We find that perceptual decisions are concurrently attracted towards the short-term perceptual history and repelled from stimuli experienced up to minutes into the past. The temporal pattern of short-term attraction and long-term repulsion cannot be captured by an ideal Bayesian observer model alone. Instead, it is well captured by an ideal observer model with efficient encoding and Bayesian decoding of visual information in a slowly changing environment. Concurrent attractive and repulsive history biases in perceptual decisions may thus be the consequence of the need for visual processing to simultaneously satisfy constraints of efficiency and stability.
In addition to bottom-up input, the visual cortex receives large amounts of feedback from other cortical areas 1–3. One compelling example of feedback activation of early visual neurons in the ...absence of bottom-up input occurs during the famous Kanizsa illusion, where a triangular shape is perceived, even in regions of the image where there is no bottom-up visual evidence for it. This illusion increases the firing activity of neurons in the primary visual cortex with a receptive field on the illusory contour 4. Feedback signals are largely segregated from feedforward signals within each cortical area, with feedforward signals arriving in the middle layer, while top-down feedback avoids the middle layers and predominantly targets deep and superficial layers 1, 2, 5, 6. Therefore, the feedback-mediated activity increase in V1 during the perception of illusory shapes should lead to a specific laminar activity profile that is distinct from the activity elicited by bottom-up stimulation. Here, we used fMRI at high field (7 T) to empirically test this hypothesis, by probing the cortical response to illusory figures in human V1 at different cortical depths 7–14. We found that, whereas bottom-up stimulation activated all cortical layers, feedback activity induced by illusory figures led to a selective activation of the deep layers of V1. These results demonstrate the potential for non-invasive recordings of neural activity with laminar specificity in humans and elucidate the role of top-down signals during perceptual processing.
•High-field fMRI can resolve neural activity with laminar specificity in humans•Top-down and bottom-up signals lead to distinct laminar activation profiles in V1•Top-down signals selectively activate deep layers of V1•Bottom-up stimulus input activates all layers of V1
Using high-field fMRI, Kok et al. show that feedback signals evoked by a visual illusion selectively activate the deep layers of the primary visual cortex, demonstrating the potential for non-invasive in vivo recordings of neural activity with laminar specificity in humans.
Perception and behavior can be guided by predictions, which are often based on learned statistical regularities. Neural responses to expected stimuli are frequently found to be attenuated after ...statistical learning. However, whether this sensory attenuation following statistical learning occurs automatically or depends on attention remains unknown. In the present fMRI study, we exposed human volunteers to sequentially presented object stimuli, in which the first object predicted the identity of the second object. We observed a reliable attenuation of neural activity for expected compared to unexpected stimuli in the ventral visual stream. Crucially, this sensory attenuation was only apparent when stimuli were attended, and vanished when attention was directed away from the predictable objects. These results put important constraints on neurocomputational theories that cast perception as a process of probabilistic integration of prior knowledge and sensory information.
Early visual areas contain specific information about visual items maintained in working memory, suggesting a role for early visual cortex in more complex cognitive functions 1–4. It is an open ...question, however, whether these areas also underlie the ability to internally generate images de novo (i.e., mental imagery). Research on mental imagery has to this point focused mostly on whether mental images activate early sensory areas, with mixed results 5–7. Recent studies suggest that multivariate pattern analysis of neural activity patterns in visual regions can reveal content-specific representations during cognitive processes, even though overall activation levels are low 1–4. Here, we used this approach 8, 9 to study item-specific activity patterns in early visual areas (V1–V3) when these items are internally generated. We could reliably decode stimulus identity from neural activity patterns in early visual cortex during both working memory and mental imagery. Crucially, these activity patterns resembled those evoked by bottom-up visual stimulation, suggesting that mental images are indeed “perception-like” in nature. These findings suggest that the visual cortex serves as a dynamic “blackboard” 10, 11 that is used during both bottom-up stimulus processing and top-down internal generation of mental content.
•Mental images can be decoded from activity patterns in human early visual cortex•Activity patterns evoked by mental images resemble stimulus-driven activity patterns•Mental imagery and working memory have shared representations in early visual cortex
Sensory signals are highly structured in both space and time. These structural regularities in visual information allow expectations to form about future stimulation, thereby facilitating decisions ...about visual features and objects. Here, we discuss how expectation modulates neural signals and behaviour in humans and other primates. We consider how expectations bias visual activity before a stimulus occurs, and how neural signals elicited by expected and unexpected stimuli differ. We discuss how expectations may influence decision signals at the computational level. Finally, we consider the relationship between visual expectation and related concepts, such as attention and adaptation.
It is widely believed that predicted tactile action outcomes are perceptually attenuated. The present experiments determined whether predictive mechanisms necessarily generate attenuation or, ...instead, can enhance perception—as typically observed in sensory cognition domains outside of action. We manipulated probabilistic expectations in a paradigm often used to demonstrate tactile attenuation. Adult participants produced actions and subsequently rated the intensity of forces on a static finger. Experiment 1 confirmed previous findings that action outcomes are perceived less intensely than passive stimulation but demonstrated more intense perception when active finger stimulation was removed. Experiments 2 and 3 manipulated prediction explicitly and found that expected touch during action is perceived more intensely than unexpected touch. Computational modeling suggested that expectations increase the gain afforded to expected tactile signals. These findings challenge a central tenet of prominent motor control theories and demonstrate that sensorimotor predictions do not exhibit a qualitatively distinct influence on tactile perception.
Visual context facilitates perception, but how this is neurally implemented remains unclear. One example of contextual facilitation is found in reading, where letters are more easily identified when ...embedded in a word. Bottom-up models explain this word advantage as a post-perceptual decision bias, while top-down models propose that word contexts enhance perception itself. Here, we arbitrate between these accounts by presenting words and nonwords and probing the representational fidelity of individual letters using functional magnetic resonance imaging. In line with top-down models, we find that word contexts enhance letter representations in early visual cortex. Moreover, we observe increased coupling between letter information in visual cortex and brain activity in key areas of the reading network, suggesting these areas may be the source of the enhancement. Our results provide evidence for top-down representational enhancement in word recognition, demonstrating that word contexts can modulate perceptual processing already at the earliest visual regions.
Recent studies claim that visual perception of stimulus features, such as orientation, numerosity, and faces, is systematically biased toward visual input from the immediate past 1–3. However, the ...extent to which these positive biases truly reflect changes in perception rather than changes in post-perceptual processes is unclear 4, 5. In the current study we sought to disentangle perceptual and decisional biases in visual perception. We found that post-perceptual decisions about orientation were indeed systematically biased toward previous stimuli and this positive bias did not strongly depend on the spatial location of previous stimuli (replicating previous work 1). In contrast, observers’ perception was repelled away from previous stimuli, particularly when previous stimuli were presented at the same spatial location. This repulsive effect resembles the well-known negative tilt-aftereffect in orientation perception 6. Moreover, we found that the magnitude of the positive decisional bias increased when a longer interval was imposed between perception and decision, suggesting a shift of working memory representations toward the recent history as a source of the decisional bias. We conclude that positive aftereffects on perceptual choice are likely introduced at a post-perceptual stage. Conversely, perception is negatively biased away from recent visual input. We speculate that these opposite effects on perception and post-perceptual decision may derive from the distinct goals of perception and decision-making processes: whereas perception may be optimized for detecting changes in the environment, decision processes may integrate over longer time periods to form stable representations.
•Recent history induces opposite biases in perception and decision•Negative adaptation repels perception away from previous stimuli•Positive serial dependence attracts decisions toward previous decisions•Serial dependence of perceptual decisions may rely on biases in working memory
Fritsche et al. show that recent history biases perception and post-perceptual decisions in opposite directions. While perception is repelled away, decisions are attracted toward the recent history. These opposite biases may enable an optimal balance between maximizing change sensitivity and maintaining stable representations.
Human agents build models of their environment, which enable them to anticipate and plan upcoming events. However, little is known about the properties of such predictive models. Recently, it has ...been proposed that hippocampal representations take the form of a predictive map-like structure, the so-called successor representation (SR). Here, we used human functional magnetic resonance imaging to probe whether activity in the early visual cortex (V1) and hippocampus adhere to the postulated properties of the SR after visual sequence learning. Participants were exposed to an arbitrary spatiotemporal sequence consisting of four items (A-B-C-D). We found that after repeated exposure to the sequence, merely presenting single sequence items (e.g., - B - -) resulted in V1 activation at the successor locations of the full sequence (e.g., C-D), but not at the predecessor locations (e.g., A). This highlights that visual representations are skewed toward future states, in line with the SR. Similar results were also found in the hippocampus. Moreover, the hippocampus developed a coactivation profile that showed sensitivity to the temporal distance in sequence space, with fading representations for sequence events in the more distant past and future. V1, in contrast, showed a coactivation profile that was only sensitive to spatial distance in stimulus space. Taken together, these results provide empirical evidence for the proposition that both visual and hippocampal cortex represent a predictive map of the visual world akin to the SR.
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