Multiple Scales of Stimulus Representation in the Human Brain

National Institute Of Mental Health

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Abstract

During the past year, we have focused on 1) characterizing the representation of stimulus features in primary visual cortex and 2) studying how these representations interact with endogenous brain states, such as spatial attention and arousal. 1) Characterizing stimulus representations in human visual cortex. Stimulus orientation is one of the most basic stimulus features represented in primary visual cortex (V1). Yet, after more than 50 years of research, the representation of orientation is inadequately understood. Orientation-selective V1 neurons are organized at a fine spatial scale in a pseudo-periodic, columnar structure across the cortical surface. Using functional magnetic resonance imaging (fMRI), we have previously discovered an additional level of organization, a coarse-scale orientation bias in which each fMRI voxel in V1 exhibits an orientation preference that depends on the region of space that it represents. Over the past year, we have investigated the neural computations that give rise to the coarse-scale orientation bias. We developed a computational model of neural activity in V1. The modeling results indicate that three theoretically distinct neural mechanisms could give rise to the coarse-scale orientation bias: stimulus vignetting, neural gain fields, and asymmetric surround suppression. We tested predictions of the computational model using high-resolution fMRI at 7 Tesla (7T) under NCT00001360. We found that the coarse-scale orientation bias is entirely determined by stimulus vignetting, and that there was no evidence for fine-scale orientation biases in the fMRI measurements (Roth et al., eLife, 2018). Our results provide a framework for reinterpreting a wide-range of imaging results in the visual system. Our ongoing work on this topic has focused on two questions. First, we are applying these theoretical and empirical findings to guide studies of visual recovery following stroke. Second, we are using the computational model in conjunction with fMRI to measure visual surround suppression, which is an important step in characterizing excitatory/inhibitory interactions in the visual system. Our work on understanding neural computations in the intact visual system is vital in determining how these computations are altered in mental health and neurological disorders. 2) Endogenous brain states. Visual perception arises from dynamic interactions between feedforward sensory information and top-down modulatory signals. In the past year, we have studied two types of top-down modulation. First, we used a novel spatial cuing protocol to isolate fMRI activity associated with endogenous spatial attention. We discovered specific sub-regions of the temporal-parietal junction are involved in directing attention to locations in space (Dugu et al., Cerebral Cortex, 2017). Second, we identified a type of brain activity that reflects the subject's general engagement in a task. This task-related activity contributes prominently to brain hemodynamic responses measured with fMRI, is independent of external visual stimuli, and instead reflects internal brain states. Task-related activity appears to be distinct from spatially-localized endogenous attention in that it is spatially global in cortex rather than retinotopically specific. This activity may be related to general arousal. We found that fluctuations in task-related brain activity correlate with fluctuations in behavioral performance. Our experiments in the past year have focused on simple visual discrimination tasks, and we have more recently begun to extend these experiments to investigate the relationship between task-related activity and task difficulty and reward processing. We are also collaborating with members of the Functional Magnetic Resonance Imaging Core Facility at NIMH to use high resolution fMRI methods to test the hypothesis that task-related hemodynamic signals have a laminar profile that is distinct from that of spatial attention. Understanding the neural mechanisms of attention and global brain states has implications for the study of a number of neurological and psychiatric disorders, including schizophrenia, autism and Attention Deficit Hyperactivity Disorder (ADHD).