Prior Expectations Evoke Stimulus Templates in the Primary Visual Cortex

Kok, Peter; Failing, Michel; Lange, Floris P. de

doi:10.1162/jocn_a_00562

Cited by 236 publications

(248 citation statements)

References 64 publications

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“…This is especially surprising, considering that an expected stimulus elicits a sustained cortical visual representation (Kok et al, 2014) akin to a stimulus maintained in VWM. Future research is needed to investigate how stimulus-specific delay activity can sometimes elicit an enhanced neural response (as is the case for VWM), and sometimes elicit a reduced neural response to matching visual input (as is the case for expectancy).…”

Section: Discussionmentioning

confidence: 99%

Visual Working Memory Enhances the Neural Response to Matching Visual Input

et al. 2017

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Visual working memory (VWM) is used to maintain visual information available for subsequent goal-directed behavior. The content of VWM has been shown to affect the behavioral response to concurrent visual input, suggesting that visual representations originating from VWM and from sensory input draw upon a shared neural substrate (i.e., a sensory recruitment stance on VWM storage). Here, we hypothesized that visual information maintained in VWM would enhance the neural response to concurrent visual input that matches the content of VWM. To test this hypothesis, we measured fMRI BOLD responses to task-irrelevant stimuli acquired from 15 human participants (three males) performing a concurrent delayed match-to-sample task. In this task, observers were sequentially presented with two shape stimuli and a retro-cue indicating which of the two shapes should be memorized for subsequent recognition. During the retention interval, a task-irrelevant shape (the probe) was briefly presented in the peripheral visual field, which could either match or mismatch the shape category of the memorized stimulus. We show that this probe stimulus elicited a stronger BOLD response, and allowed for increased shape-classification performance, when it matched rather than mismatched the concurrently memorized content, despite identical visual stimulation. Our results demonstrate that VWM enhances the neural response to concurrent visual input in a content-specific way. This finding is consistent with the view that neural populations involved in sensory processing are recruited for VWM storage, and it provides a common explanation for a plethora of behavioral studies in which VWMmatching visual input elicits a stronger behavioral and perceptual response.

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Section: Discussionmentioning

confidence: 99%

Visual Working Memory Enhances the Neural Response to Matching Visual Input

et al. 2017

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“…Previous research has shown that these orientation-specific patterns may embody prior expectations. For example, in the absence of a stimulus, expectations evoke patterns of activity in early visual cortex similar to those evoked by actual stimuli (SanMiguel et al, 2013;Kok et al, 2014). Such complex and regular spatiotemporal patterns have also been characterized in spontaneous brain fluctuations (Fox et al, 2005), where they are thought to embody prior expectations about the immediate, directly relevant future (Schacter et al, 2007).…”

Section: Discussionmentioning

confidence: 99%

“…We aggregated the data according to voxel preference and block orientation: activity in 45°voxels during 45°blocks and activity in 135°voxels during 135°blocks were averaged together as "voxels tuned to expected orientation" and activity in 45°voxels during 135°blocks and activity in 135°voxels during 45°blocks were averaged together as "voxels tuned to nonexpected orientation" (Kok et al, 2014). Differences in orientation-specific activity between trial types were assessed by a threeway repeated-measures ANOVA with the factors "voxel tuning" (levels: expected orientation and nonexpected orientation), "trial type" (levels: CRs and FAs), and "time" (levels: t ϭ Ϫ2 s and t ϭ 0 s).…”

Section: Experimental Designmentioning

confidence: 99%

“…Conversely, prior expectations about sen-sory events may be embodied in the specific patterns of prestimulus spontaneous activity in the relevant sensory regions (Berkes et al, 2011). Indeed, sensory expectations evoke patterns of activity that resemble those evoked by actual stimuli in early sensory cortices (SanMiguel et al, 2013;Kok et al, 2014) and such stimulus-like patterns have also been observed in spontaneous cortical activity (Kenet et al, 2003). Spontaneous fluctuations in neural patterns of activity may thus embody fluctuations in the content and strength of perceptual expectations.…”

Section: Introductionmentioning

confidence: 98%

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Spontaneous Activity Patterns in Primary Visual Cortex Predispose to Visual Hallucinations

et al. 2015

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According to theoretical frameworks casting perception as inference, vision results from the integration of bottom-up visual input with top-down expectations. Under conditions of strongly degraded sensory input, this may occasionally result in false perceptions in the absence of a sensory signal, also termed "hallucinations." Here, we investigated whether spontaneous prestimulus activity patterns in sensory circuits, which may embody a participant's prior expectations, predispose the observer toward false perceptions. Specifically, we used fMRI to investigate whether the representational content of prestimulus activity in early visual cortex is linked to subsequent perception during a challenging detection task. Human participants were asked to detect oriented gratings of a particular orientation that were embedded in noise. We found two characteristics of prestimulus activity that predisposed participants to hallucinations: overall lower prestimulus activity and a bias in the prestimulus activity patterns toward the to-be-detected (expected) grating. These results suggest that perceptual hallucinations may be due to an imprecise and biased state of sensory circuits preceding sensory evidence collection.

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“…Because there is no sensory input during stimulus omission, the response cannot be due to recovery from repetition suppression, and, if the effect is localized (i.e., does not occur in all cortical regions), it cannot be due to nonspecific surprise. This stimulus-omission paradigm has been used with mice to record from V1 with multielectrode arrays (8), with human adults to record from auditory and frontal areas with magnetoencephalography (MEG) (7), from V1 using fMRI (26), and with presurgical epilepsy patients to record from temporal-parietal areas with cortical electrodes (27). A particularly impressive variation is the ability of a recently learned cross-modal association (e.g., audiovisual stimuli) to generate responses to the unexpected omission of one of the previously paired stimuli, as recently demonstrated in human adults (5,28).…”

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confidence: 99%

Top-down modulation in the infant brain: Learning-induced expectations rapidly affect the sensory cortex at 6 months

Emberson

Richards

Aslin

2015

Proc. Natl. Acad. Sci. U.S.A.

162

210

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Recent theoretical work emphasizes the role of expectation in neural processing, shifting the focus from feed-forward cortical hierarchies to models that include extensive feedback (e.g., predictive coding). Empirical support for expectation-related feedback is compelling but restricted to adult humans and nonhuman animals. Given the considerable differences in neural organization, connectivity, and efficiency between infant and adult brains, it is a crucial yet open question whether expectation-related feedback is an inherent property of the cortex (i.e., operational early in development) or whether expectation-related feedback develops with extensive experience and neural maturation. To determine whether infants' expectations about future sensory input modulate their sensory cortices without the confounds of stimulus novelty or repetition suppression, we used a cross-modal (audiovisual) omission paradigm and used functional near-infrared spectroscopy (fNIRS) to record hemodynamic responses in the infant cortex. We show that the occipital cortex of 6-month-old infants exhibits the signature of expectation-based feedback. Crucially, we found that this region does not respond to auditory stimuli if they are not predictive of a visual event. Overall, these findings suggest that the young infant's brain is already capable of some rudimentary form of expectation-based feedback.O ver the past two decades, theoretical focus has shifted from predominantly feed-forward hierarchies of cortical function, where sensory cortex propagates information to higher level analyzers on the way to decision and motor control areas, to models in which feedback connections to lower-level cortical regions allow extensive top-down functional modulation based on expectation (1). An influential model for incorporating feedback is predictive coding, which compares expectations or predictions to input at each level of the processing hierarchy (2-4). There is extensive and compelling evidence for expectation-based modulation even at the earliest levels of sensory processing in both humans (5-7) and nonhuman animals (8). Because complex, naturalistic sensory input is characterized by temporal, spatial, and contextual regularities, the ability to modulate early sensory function as a result of expectations is believed to support adaptive perceptual abilities (4).Empirical evidence for expectation-based feedback, however, is restricted to adult humans and nonhuman animals. With their extensive experience, adults already have developed sophisticated internal models of the environment and have a highly interconnected brain and efficient neural processing. Comparatively, human infants are born with a demonstratively immature behavioral repertoire, have underdeveloped sensorimotor and cognitive capacities, and lack sophisticated internal models of the environment. These internal models undergo substantial postnatal development even in the early sensory cortex. For example, spontaneous activity of primary visual cortex (V1) in ferrets converges with e...

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Prior Expectations Evoke Stimulus Templates in the Primary Visual Cortex

Cited by 236 publications

References 64 publications

Visual Working Memory Enhances the Neural Response to Matching Visual Input

Visual Working Memory Enhances the Neural Response to Matching Visual Input

Spontaneous Activity Patterns in Primary Visual Cortex Predispose to Visual Hallucinations

Top-down modulation in the infant brain: Learning-induced expectations rapidly affect the sensory cortex at 6 months

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