David C. Somers - US grants

Mechanisms of Attentional Selection in Human Visual Cortex
Abstract
With National Science Foundation support, Dr. Somers will conduct a three-year study to investigate the mechanisms of attentional selection in human visual cortex using functional MRI combined with psychophysics and computational modeling. Studies are proposed that will investigate 1) the spatial distribution of attention under different forms of selection, 2) the role of suppression in selection and its relationship to facilitation, and 3) the computational mechanisms by which attention facilitates or suppresses a stimulus representation in visual cortex. The human mind regularly encounters complex environments that contain more information than it can process at one instant. Attention acts as the critical gateway to perception and cognition by selecting the stimuli that will be processed. The metaphor of the spotlight, selecting a single contiguous region of space, has long been employed to describe visual attention (James, 1890). In addition to spatial selection, object-based and feature-based selection have also been inferred behaviorally. This proposal seeks to investigate the spatial patterns of modulations these differing forms of selection can exert on human visual cortex. Using fMRI, we have observed that under appropriate task demands, the attentional spotlight may be split to attend to two distinct regions of space simultaneously while leaving the intermediate region unselected (see preliminary results). The capabilities and limitations in splitting the attentional spotlight will be investigated in this proposal. Investigations of how feature-based and object-based attention operate across space in retinotopic visual cortex are also proposed. Further studies will investigate the relationship between the spatial limits of attentional resolution and the processing capabilities of different visual cortical areas. Attentional selection is a competitive process with winners, the selected stimuli, and losers, unselected stimuli. It has been argued that selection is comprised not only of facilitative processes, but also of suppressive processes. Indeed, attentional suppression of unattended stimuli in visual cortex has been observed (e.g., Somers et al, 1999). Here, it is proposed to investigate how suppression acts across space and its relationship to facilitation. Is suppression purely a passive process (e.g., withdrawal) that results when attention is directed elsewhere? Or is there an active component to suppression? Is active suppression required to split the spotlight? Is suppression uniform across non-attended space or do robust distractors receive targeted suppression? To what degree does suppression vary with task form and/or task demands? Attentional selection modulates activity even in primary visual cortex. This implies that attention directly interacts with low-level, stimulus representations. What are the computational mechanisms by which attention selects stimuli without disrupting stimulus encoding in visual cortex? Does attention primarily modulate the gain (multiplicative effect) of stimulus-driven responses? Or does attention primarily bias (additive effect) stimulus responses to give them a competitive advantage in gaining access to cognitive processes? To investigate these issues a series of parametric fMRI/psychophysical studies is proposed in which physical stimulus properties will be varied while attention is directed toward or away from the stimulus. These data will be used to construct fMRI stimulus response functions both with and without attention and will allow us to infer the primary computational effect of attention on a neuronal population. In concert with these experiments, computational modeling studies will be performed. The modeling will provide a framework to integrate not only the present experimental results, but also the primate database on single unit responses in visual cortex. It is expected that the modeling will refine understanding of selection mechanisms and help to generate future experimental questions.
The broader impact of the proposed studies includes increased understanding of cognitive brain mechanisms in normal humans. This knowledge about the relationship between mind and brain will inform future clinical studies, particularly for populations with attentional dysfunction. Computational understanding of how the brain implements attention may also aid design of future computer architectures. This research also offers training opportunities for undergraduate and graduate students, including those from underrepresented groups.

How do we remember where things are? How do we pay attention to some objects while ignoring distractions? One part of the brain that supports the processing of these and other important functions is the posterior parietal cortex. It is involved in spatial representation, attentional control, planning of eye and hand movements, number sense, and working memory. Despite the importance and diversity of the cognitive functions attributed to this region of the brain, its functional organization is not well understood. Prior studies in non-human primates suggest that this area is comprised of many small cortical areas, each with different functional roles. The goals of this project are: 1) to identify distinct functional subregions of this portion of the human cerebral cortex; 2) reveal the spatial representations that these regions use encode information; 3) reveal the different functional roles that these subregions play in visual attention and visual working memory. With support from the National Science Foundation, Dr. David Somers and colleagues at Boston University will address these questions by seeing the brain at work with functional magnetic resonance imaging. As many as fourteen distinct brain regions, each with a complete map of visual space, can now be identified in individual subjects. Activity within each of these distinct areas will be measured while human volunteers attempt to pay attention to and remember visual stimuli in different situations.

This work will reveal a more comprehensive picture of the functional organization of human posterior parietal cortex and of the brain mechanisms that support visual perception, visual attention, and visual working memory. This research also could identify new distinct regions of the cerebral cortex. These investigations have broad implications for the study of neurological diseases and disorders that involve posterior parietal cortex, including Alzheimer's Disease, Williams Syndrome, and a variety of attentional disorders. This research also offers cognitive neuroscience and brain imaging research training opportunities for both undergraduate and graduate students, including those from underrepresented groups.

DESCRIPTION (provided by applicant): The overarching goal of this research is to reveal the brain mechanisms by which visual attention, visual short- term memory (STM) and retrieval from visual long-term memory (LTM) integrate their functioning to support cognition and perception. Performance of healthy humans in visual tasks exceeds the performance of supercomputers, yet the capacity of the human visual system is profoundly limited; people can only attend to or hold in visual STM about four objects at one time. Retrieval from long-term memory into visual working memory (VWM) contributes greatly to visual performance in familiar contexts. However, diseases, including Alzheimer's and schizophrenia, traumatic brain injuries, stroke, and normal aging all can lead to reductions in the capacity of visual attention and STM and result in severe impairments in the performance of vision-related cognitive and perceptual tasks. In order to help guide therapeutic interventions, it is critical to have a detailed understanding of the neural substrates and mechanisms of visual attention, STM and LTM retrieval. A series of human functional magnetic resonance imaging (fMRI) and behavioral studies is proposed to identify the shared and dissociated neural substrates of visual attention, visual STM and retrieval from visual LTM. Research has shown that portions of the frontal and parietal lobes work together as a network to support each of these tasks, but currently the precise identity and functional role of these brain areas in the different tasks is not well understood. Functional localizer fMRI methods and within-subject analysis will be performed in order to obtain precise localization of these brain regions. STM load and several attentional factors will be manipulated in order to identify the functional contributions of different brain regions to capacity limits under different forms of task demands. Event-related analysis will be performed in order to identify network components of visual LTM retrieval and their relationship to components of the visual STM, attentional & default mode networks. Experiments employing functional connectivity fMRI methods will focus on network interactions that may play a role in the symptoms of Hemispatial Neglect and in the post-stroke mechanisms that accompany restoration of spatial processing. This knowledge can guide the development of assays that can refine diagnosis and treatment of psychiatric illnesses and may help maintain cognitive function in persons who experience disease- related or age-related decline. As the specific contributions of different brain regions are characterized, research can focus on identifying particular network subcomponents that may be differentially impaired in different clinical populations. PUBLIC HEALTH RELEVANCE: Cognitive performance is limited by the restricted capacity of the brain's attention and short-term memory systems. Diseases including Alzheimer's and schizophrenia, brain damage caused by stroke or traumatic brain injury, and normal aging are all associated with diminished attention and short-term memory capacity and can result in severe impairments of cognitive performance. In order to speed the development of pharmaceutical and other therapeutic methods, it is critical to understand the normal functioning of the brain circuits supporting attention and memory and the goal of this project is to reveal the specific roles of a network of brain regions in the frontal and parietal lobes in visual attention, visual short-term memory, and retrieval from visual long-term memory.

Performance on visual perception and visual cognition tasks depends critically on precise spatiotemporal deployment of attention. In order to help guide therapeutic interventions for patients with perceptual and/or cognitive deficits, it is critical to develop a detailed understanding of the brain circuits and mechanisms that support attentional function. Although cerebellar dysfunction has been implicated in attention-deficit / hyperactivity disorder (ADHD), potential contributions of the cerebellum to visual attentional functions have largely been overlooked. Cerebellar dysfunction is also implicated in other neurological disorders such as schizophrenia, obsessive-compulsive disorder and autism. In the motor system, the cerebellum is known to play a key role in fine temporal coordination of movements. Moreover, the cerebellum appears to form `internal models' of learned tasks that can be used to correct errors `on the fly,' and thus support efficient task performance. Recent evidence indicates that specific sub-regions of the human cerebellum exhibit functional connectivity with specific cortical networks, forming cerebro-cerebellar networks. Although the motor cerebro- cerebellar network has been well studied, the functional properties of cerebro-cerebellar networks linked to cognition have received only modest scientific attention. Our preliminary results demonstrate that cerebellar lobules VIIb/VIIIa are a component of a cerebro-cerebellar `dorsal attention network' that supports sustained visual attention and visual working memory. Here, we plan to explore this network and other potential cerebellar sub-region contributions to established cortical attention networks, including the ventral attention network and the cognitive control network. The demonstration of the existence of multiple cerebro-cerebellar attention networks and the elucidation of distinct cerebellar functional contributions to different forms of attention would significantly advance both our understanding of attention networks in the brain and our understanding of the functional roles of the cerebellum in these networks. We will also examine specific hypotheses regarding the mechanisms by which cerebellar lobules VIIb/VIIIa contribute to visual attention and visual working memory performance. This knowledge can guide the development of assays that can refine diagnosis and treatment of neurological disorders in which visual attention and cognition are impaired. It may also help to identify approaches for maintaining cognitive function in persons experiencing disease-related or age-related decline.

Abstract

Humans experience the world via multiple sensory modalities -- we see, we hear, and we touch. Each sensory modality has unique strengths and weaknesses in its ability to represent the world around us. Our minds are able to flexibly recruit visual or auditory brain structures when their strengths correspond to the task at hand. In addition, our experience at any moment depends both on sensory input and on working memory and attention mechanisms in the brain. These mechanisms have very limited capacities, which in turn limit cognition. The overarching goal of this project is to examine the human brain mechanisms that support attention and working memory in vision, hearing, and touch. The research team will perform functional MRI experiments to study the brain activity of healthy adults while they perform demanding sensory working memory tasks. Preliminary studies by the research group suggest that there are extensive brain networks, extending into the frontal lobes of the cerebral cortex, that are specialized for each sensory modality, as well as a shared network that supports and unifies these three senses. The current research program will examine individual differences in working memory performance and brain network organization. It will also develop advanced computational models that can predict the functional organization of an individual's brain from their unique pattern or 'fingerprint' of brain connectivity. The project will facilitate other research efforts through the dissemination of new models and computational tools, and will recruit and train young scientists, including members of groups that are under-represented in STEM, in cognitive neuroscience research.

This proposal has 4 primary intellectual goals: (1) identify the fine-scale organization of tactile, visual, auditory, and modality-independent attention & working memory (WM) regions within human cerebral cortex; (2) reveal the specificity of coding of WM information across cortical regions for each modality; (3) detail the network organization of attention & WM circuits; and (4) test hypotheses about content-specific WM mechanisms and cross-modality WM coding. Individual subject fMRI analyses permit fine-scale observation of distinct functional regions. Drawing on subject-specific maps of cortical organization, the research group will re-examine the highly debated question of which brain structures support stimulus-specific working memory for each modality. It will investigate the specificity of sensory modality biased regions by examining functional networks in the resting-state within individual participants. The research team will leverage its findings to probe these networks in 1200 subjects from the Human Connectome Project dataset. The research group will also test and validate a machine-learning approach, Connectome Fingerprinting, for predicting the location of modality-specific working memory regions in individual brains from their unique functional connectome. Vision excels in coding spatial information, but codes timing less reliably; conversely, the auditory system performs high-fidelity temporal coding but coarse spatial coding. The research team has observed cross-modal recoding of WM information into cortical structures that prefer the 'appropriate modality' - auditory spatial WM recruits visual-biased regions and visual temporal WM recruits auditory-biased regions. To probe content-specific WM mechanisms, the researchers will examine interactions between sensory modality WM and space/time WM. The research group hypothesizes that visual and spatial WM stores are distinct, but that auditory and timing WM stores are shared. Collectively, these studies will elucidate the human brain networks and mechanisms that support sensory working memory.

This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.