The integration of bottom-up and top-down signals in human perception in health and disease

To extract a meaningful visual experience from the information falling on the retina, the visual system must integrate signals from multiple levels. Bottom-up signals provide input relating to local features while top-down signals provide contextual feedback and reflect internal states of the organism. In this thesis I will explore the nature and neural basis of this integration in two key areas. I will examine perceptual filling-in of artificial scotomas to investigate the bottom-up signals causing changes in perception when filling-in takes place. I will then examine how this perceptual filling-in is modified by top-down signals reflecting attention and working memory. I will also investigate hemianopic completion, an unusual form of filling-in, which may reflect a breakdown in top-down feedback from higher visual areas. The second part of the thesis will explore a different form of top-down control of visual processing. While the effects of cognitive mechanisms such as attention on visual processing are well-characterised, other types of top-down signal such as reward outcome are less well explored. I will therefore study whether signals relating to reward can influence visual processing. To address these questions, I will employ a range of methodologies including functional MRI, magnetoencephalography and behavioural testing in healthy participants and patients with cortical damage. I will demonstrate that perceptual filling-in of artificial scotomas is largely a bottom-up process but that higher cognitive functions can modulate the phenomenon. I will also show that reward modulates activity in higher visual areas in the absence of concurrent visual stimulation and that receiving reward leads to enhanced activity in primary visual cortex on the next trial. These findings reveal that integration occurs across multiple levels even for processes rooted in early retinotopic regions, and that higher cognitive processes such as reward can influence the earliest stages of cortical visual processing

Gamma oscillatory activity in autism spectrum disorder during a face cueing task

Joint attention is a social interaction skill that normally develops in infancy and involves following another’s gaze to a stimulus. This skill is absent or developmentally delayed in autism spectrum disorders (ASD), causing cascading effects on development. Neural synchrony in the gamma frequency band is thought to be involved in cognitive functions such as joint attention. The current study investigated differences in gamma power between neurotypicals and ASD as measured by magnetoencephalography (MEG) while performing a gaze cueing task simulating joint attention. Results support lower frontal gamma power in ASD, suggesting that impaired generation of gamma activity in the prefrontal cortex may be involved in impairments in social cognitive functions such as joint attention in ASD. In contrast to previous research, findings did not support higher posterior gamma power in ASD, indicating a need for further research to clarify the nature of gamma oscillatory activity in posterior brain regions in ASD

The role of oscillatory brain activity in object processing and figure-ground segmentation in human vision

The perception of an object as a single entity within a visual scene requires that its features are bound together and segregated from the background and/or other objects. Here, we used magnetoencephalography (MEG) to assess the hypothesis that coherent percepts may arise from the synchronized high frequency (gamma) activity between neurons that code features of the same object. We also assessed the role of low frequency (alpha, beta) activity in object processing. The target stimulus (i.e. object) was a small patch of a concentric grating of 3. c/°, viewed eccentrically. The background stimulus was either a blank field or a concentric grating of 3. c/° periodicity, viewed centrally. With patterned backgrounds, the target stimulus emerged - through rotation about its own centre - as a circular subsection of the background. Data were acquired using a 275-channel whole-head MEG system and analyzed using Synthetic Aperture Magnetometry (SAM), which allows one to generate images of task-related cortical oscillatory power changes within specific frequency bands. Significant oscillatory activity across a broad range of frequencies was evident at the V1/V2 border, and subsequent analyses were based on a virtual electrode at this location. When the target was presented in isolation, we observed that: (i) contralateral stimulation yielded a sustained power increase in gamma activity; and (ii) both contra- and ipsilateral stimulation yielded near identical transient power changes in alpha (and beta) activity. When the target was presented against a patterned background, we observed that: (i) contralateral stimulation yielded an increase in high-gamma (> 55. Hz) power together with a decrease in low-gamma (40-55. Hz) power; and (ii) both contra- and ipsilateral stimulation yielded a transient decrease in alpha (and beta) activity, though the reduction tended to be greatest for contralateral stimulation. The opposing power changes across different regions of the gamma spectrum with 'figure/ground' stimulation suggest a possible dual role for gamma rhythms in visual object coding, and provide general support of the binding-by-synchronization hypothesis. As the power changes in alpha and beta activity were largely independent of the spatial location of the target, however, we conclude that their role in object processing may relate principally to changes in visual attention. © 2010 Elsevier B.V

Top-down effects on early visual processing in humans: a predictive coding framework

An increasing number of human electroencephalography (EEG) studies examining the earliest component of the visual evoked potential, the so-called C1, have cast doubts on the previously prevalent notion that this component is impermeable to top-down effects. This article reviews the original studies that (i) described the C1, (ii) linked it to primary visual cortex (V1) activity, and (iii) suggested that its electrophysiological characteristics are exclusively determined by low-level stimulus attributes, particularly the spatial position of the stimulus within the visual field. We then describe conflicting evidence from animal studies and human neuroimaging experiments and provide an overview of recent EEG and magnetoencephalography (MEG) work showing that initial V1 activity in humans may be strongly modulated by higher-level cognitive factors. Finally, we formulate a theoretical framework for understanding top-down effects on early visual processing in terms of predictive coding

Perceptual organization and consciousness

With chapter written by leading researchers in the field, this is the state-of-the-art reference work on this topic, and will be so for many years to come

Boundary completion is automatic and dissociable from shape discrimination

Normal visual perception readily overcomes suboptimal or degraded viewing conditions through perceptual filling-in processes, enhancing object recognition and discrimination abilities. This study used visual evoked potential (VEP) recordings in conjunction with electrical neuroimaging analyses to determine the spatiotemporal brain dynamics of boundary completion and shape discrimination processes in healthy humans performing the so-called "thin/fat" discrimination task (Ringach and Shapley, 1996) with stimuli producing illusory contours. First, results suggest that boundary completion processes occur independent of subjects' accuracy on the discrimination task. Modulation of the VEP to the presence versus absence of illusory contours [the IC effect (Murray et al., 2002)] was indistinguishable in terms of response magnitude and scalp topography over the 124-186 ms poststimulus period, regardless of whether task performance was correct. This suggests that failure on this discrimination task is not primarily a consequence of failed boundary completion. Second, the electrophysiological correlates of thin/fat shape discrimination processes are temporally dissociable from those of boundary completion, occurring during a substantially later phase of processing (approximately 330-406 ms). The earlier IC effect was unaffected by whether the perceived contour produced a thin or fat shape. In contrast, later time periods of the VEP modulated according to perceived shape only in the case of stimuli producing illusory contours, but not for control stimuli for which performance was at near-chance levels. Collectively, these data provide further support for a multistage model of object processing under degraded viewing conditions

Illusions of Visual Motion Elicited by Electrical Stimulation of Human MT Complex

Human cortical area MT+ (hMT+) is known to respond to visual motion stimuli, but its causal role in the conscious experience of motion remains largely unexplored. Studies in non-human primates demonstrate that altering activity in area MT can influence motion perception judgments, but animal studies are inherently limited in assessing subjective conscious experience. In the current study, we use functional magnetic resonance imaging (fMRI), intracranial electrocorticography (ECoG), and electrical brain stimulation (EBS) in three patients implanted with intracranial electrodes to address the role of area hMT+ in conscious visual motion perception. We show that in conscious human subjects, reproducible illusory motion can be elicited by electrical stimulation of hMT+. These visual motion percepts only occurred when the site of stimulation overlapped directly with the region of the brain that had increased fMRI and electrophysiological activity during moving compared to static visual stimuli in the same individual subjects. Electrical stimulation in neighboring regions failed to produce illusory motion. Our study provides evidence for the sufficient causal link between the hMT+ network and the human conscious experience of visual motion. It also suggests a clear spatial relationship between fMRI signal and ECoG activity in the human brain

SENSORY AND PERCEPTUAL CODES IN CORTICAL AUDITORY PROCESSING

A key aspect of human auditory cognition is establishing efficient and reliable representations about the acoustic environment, especially at the level of auditory cortex. Since the inception of encoding models that relate sound to neural response, three longstanding questions remain open. First, on the apparently insurmountable problem of fundamental changes to cortical responses depending on certain categories of sound (e.g. simple tones versus environmental sound). Second, on how to integrate inner or subjective perceptual experiences into sound encoding models, given that they presuppose existing, direct physical stimulation which is sometimes missed. And third, on how does context and learning fine-tune these encoding rules, as adaptive changes to improve impoverished conditions particularly important for communication sounds. In this series, each question is addressed by analysis of mappings from sound stimuli delivered-to and/or perceived-by a listener, to large-scale cortically-sourced response time series from magnetoencephalography. It is first shown that the divergent, categorical modes of sensory coding may unify by exploring alternative acoustic representations other than the traditional spectrogram, such as temporal transient maps. Encoding models of either of artificial random tones, music, or speech stimulus classes, were substantially matched in their structure when represented from acoustic energy increases –consistent with the existence of a domain-general common baseline processing stage. Separately, the matter of the perceptual experience of sound via cortical responses is addressed via stereotyped rhythmic patterns normally entraining cortical responses with equal periodicity. Here, it is shown that under conditions of perceptual restoration, namely cases where a listener reports hearing a specific sound pattern in the midst of noise nonetheless, one may access such endogenous representations in the form of evoked cortical oscillations at the same rhythmic rate. Finally, with regards to natural speech, it is shown that extensive prior experience over repeated listening of the same sentence materials may facilitate the ability to reconstruct the original stimulus even where noise replaces it, and to also expedite normal cortical processing times in listeners. Overall, the findings demonstrate cases by which sensory and perceptual coding approaches jointly continue to expand the enquiry about listeners’ personal experience of the communication-rich soundscape