Geraint Rees

Predicting the orientation of invisible stimuli from activity in human primary visual cortex

Humans can experience aftereffects from oriented stimuli that are not consciously perceived, suggesting that such stimuli receive cortical processing. Determining the physiological substrate of such effects has proven elusive owing to the low spatial resolution of conventional human neuroimaging techniques compared to the size of orientation columns in visual cortex. Here we show that even at conventional resolutions it is possible to use fMRI to obtain a direct measure of orientation-selective processing in V1. We found that many parts of V1 show subtle but reproducible biases to oriented stimuli, and that we could accumulate this information across the whole of V1 using multivariate pattern recognition. Using this information, we could then successfully predict which one of two oriented stimuli a participant was viewing, even when masking rendered that stimulus invisible. Our findings show that conventional fMRI can be used to reveal feature-selective processing in human cortex, even for invisible stimuli.

A direct quantitative relationship between the functional properties of human and macaque V5.

The nature of the quantitative relationship between single-neuron recordings in monkeys and functional magnetic resonance imaging (fMRI) measurements in humans is crucial to understanding how experiments in these different species are related, yet it remains undetermined. We measured brain activity in humans attending to moving visual stimuli, using blood oxygenation level-dependent (BOLD) fMRI. Responses in V5 showed a strong and highly linear dependence on increasing strength of motion signal (coherence). These population responses in human V5 had a remarkably simple mathematical relationship to previously observed single-cell responses in macaque V5. We provided an explicit quantitative estimate for the interspecies comparison of single-neuron activity and BOLD population responses. Our data show previously unknown dissociations between the functional properties of human V5 and other human motion-sensitive areas, thus predicting similar dissociations for the properties of single neurons in homologous areas of macaque cortex.

Neural correlates of consciousness in humans

The directness and vivid quality of conscious experience belies the complexity of the underlying neural mechanisms, which remain incompletely understood. Recent work has focused on identifying the brain structures and patterns of neural activity within the primate visual system that are correlated with the content of visual consciousness. Functional neuroimaging in humans and electrophysiology in awake mokeys indicate that there are important differences between striate and extrastriate visual cortex in how well neural activity correlates with consciousness. Moreover, recent neuroimaging studies indicate that, in addition to these ventral areas of visual cortex, dorsal prefrontal and parietal areas might contribute to conscious visual experience.

Reading Hidden Intentions in the Human Brain

When humans are engaged in goal-related processing, activity in prefrontal cortex is increased. However, it has remained unclear whether this prefrontal activity encodes a subjects current intention. Instead, increased levels of activity could reflect preparation of motor responses, holding in mind a set of potential choices, tracking the memory of previous responses, or general processes related to establishing a new task set. Here we study subjects who freely decided which of two tasks to perform and covertly held onto an intention during a variable delay. Only after this delay did they perform the chosen task and indicate which task they had prepared. We demonstrate that during the delay, it is possible to decode from activity in medial and lateral regions of prefrontal cortex which of two tasks the subjects were covertly intending to perform. This suggests that covert goals can be represented by distributed patterns of activity in the prefrontal cortex, thereby providing a potential neural substrate for prospective memory. During task execution, most information could be decoded from a more posterior region of prefrontal cortex, suggesting that different brain regions encode goals during task preparation and task execution. Decoding of intentions was most robust from the medial prefrontal cortex, which is consistent with a specific role of this region when subjects reflect on their own mental states.

The physiological basis of attentional modulation in extrastriate visual areas.

Selective attention to color or motion enhances activity in specialized areas of extrastriate cortex, but mechanisms of attentional modulation remain unclear. By dissociating modulation of visually evoked transient activity from the baseline for a particular attentional set, human functional neuroimaging was used to investigate the physiological basis of such effects. Baseline activity in motion- and color-sensitive areas of extrastriate cortex was enhanced by selective attention to these attributes, even without moving or colored stimuli. Further, visually evoked responses increased along with baseline activity. These results are consistent with the hypothesis that attention modulates sensitivity of neuronal populations to inputs by changing background activity.

Concurrent TMS-fMRI and Psychophysics Reveal Frontal Influences on Human Retinotopic Visual Cortex

BACKGROUND Regions in human frontal cortex may have modulatory top-down influences on retinotopic visual cortex, but to date neuroimaging methods have only been able to provide indirect evidence for such functional interactions between remote but interconnected brain regions. Here we combined transcranial magnetic stimulation (TMS) with concurrent functional magnetic resonance imaging (fMRI), plus psychophysics, to show that stimulation of the right human frontal eye-field (FEF) produced a characteristic topographic pattern of activity changes in retinotopic visual areas V1-V4, with functional consequences for visual perception. RESULTS FEF TMS led to activity increases for retinotopic representations of the peripheral visual field, but to activity decreases for the central field, in areas V1-V4. These frontal influences on visual cortex occurred in a top-down manner, independently of visual input. TMS of a control site (vertex) did not elicit such visual modulations, and saccades, blinks, or pupil dilation could not account for our results. Finally, the effects of FEF TMS on activity in retinotopic visual cortex led to a behavioral prediction that we confirmed psychophysically by showing that TMS of the frontal site (again compared with vertex) enhanced perceived contrast for peripheral relative to central visual stimuli. CONCLUSIONS Our results provide causal evidence that circuits originating in the human FEF can modulate activity in retinotopic visual cortex, in a manner that differentiates the central and peripheral visual field, with functional consequences for perception. More generally, our study illustrates how the new approach of concurrent TMS-fMRI can now reveal causal interactions between remote but interconnected areas of the human brain.

Relating Introspective Accuracy to Individual Differences in Brain Structure

Naval Gazing Simple perceptual tasks, such as detecting the contrast between light and dark bars in a grating, have been a mainstay of psychophysical research for decades. This kind of task makes it possible to obtain both an objective measure of how accurate subjects are and a subjective measure of how confident they are in their judgments. Fleming et al. (p. 1541; see the Perspective by Lau and Maniscalco) have taken this approach one step further by constructing a measure of how accurate subjects are in their confidence judgments. This capacity for introspection, which can be regarded as one facet of metacognition (thinking about thinking), is shown to vary across individuals and to correlate positively with the gray matter volume of the frontopolar cortex (the frontmost region of the brain) and also with white matter in the tracts of the corpus callosum that connect these regions in the left and right hemispheres. Individual differences in the capacity for introspection are reflected in structural variation in the frontal lobe. The ability to introspect about self-performance is key to human subjective experience, but the neuroanatomical basis of this ability is unknown. Such accurate introspection requires discriminating correct decisions from incorrect ones, a capacity that varies substantially across individuals. We dissociated variation in introspective ability from objective performance in a simple perceptual-decision task, allowing us to determine whether this interindividual variability was associated with a distinct neural basis. We show that introspective ability is correlated with gray matter volume in the anterior prefrontal cortex, a region that shows marked evolutionary development in humans. Moreover, interindividual variation in introspective ability is also correlated with white-matter microstructure connected with this area of the prefrontal cortex. Our findings point to a focal neuroanatomical substrate for introspective ability, a substrate distinct from that supporting primary perception.

Neural correlates of change detection and change blindness

Functional magnetic resonance imaging (fMRI) of subjects attempting to detect a visual change occurring during a screen flicker was used to distinguish the neural correlates of change detection from those of change blindness. Change detection resulted in enhanced activity in the parietal and right dorsolateral prefrontal cortex as well as category-selective regions of the extrastriate visual cortex (for example, fusiform gyrus for changing faces). Although change blindness resulted in some extrastriate activity, the dorsal activations were clearly absent. These results demonstrate the importance of parietal and dorsolateral frontal activations for conscious detection of changes in properties coded in the ventral visual pathway, and thus suggest a key involvement of dorsal–ventral interactions in visual awareness.

Characterizing Stimulus-Response Functions Using Nonlinear Regressors in Parametric fMRI Experiments

Parametric study designs proved very useful in characterizing the relationship between experimental parameters (e.g., word presentation rate) and regional cerebral blood flow in positron emission tomography studies. In a previous paper we presented a method that fits nonlinear functions of stimulus or task parameters to hemodynamic responses, using second-order polynomial expansions. Here we expand this approach to model nonlinear relationships between BOLD responses and experimental parameters, using fMRI. We present a framework that allows this technique to be implemented in the context of the general linear model employed by statistical parametric mapping (SPM). Statistical inferences, in this instance, are based on F statistics and in this respect we emphasize the use of corrected P values for F fields (i.e., SPM¿F¿). The approach is illustrated with a fMRI study that looked at the effect of increasing auditory word-presentation rate. Our parametric design allowed us to characterize different forms of rate-dependent responses in three critical regions: (i) bilateral frontal regions showed a categorical response to the presence of words irrespective of rate, suggesting a role for this region in establishing cognitive (e.g., attentional) set; (ii) in bilateral occipitotemporal regions activations increased linearly with increasing word rate; and (iii) posterior auditory association cortex exhibited a nonlinear (inverted U) relationship to word rate.

Eye-specific effects of binocular rivalry in the human lateral geniculate nucleus.

When dissimilar images are presented to the two eyes, they compete for perceptual dominance so that each image is visible in turn for a few seconds while the other is suppressed. Such binocular rivalry is associated with relative suppression of local, eye-based representations that can also be modulated by high-level influences such as perceptual grouping. However, it is currently unclear how early in visual processing the suppression of eye-based signals can occur. Here we use high-resolution functional magnetic resonance imaging (fMRI) in conjunction with a new binocular rivalry stimulus to show that signals recorded from the human lateral geniculate nucleus (LGN) exhibit eye-specific suppression during rivalry. Regions of the LGN that show strong eye-preference independently show strongly reduced activity during binocular rivalry when the stimulus presented in their preferred eye is perceptually suppressed. The human LGN is thus the earliest stage of visual processing that reflects eye-specific dominance and suppression.