Multiple Scales of Stimulus Representation in the Human Brain

National Institute Of Mental Health

Investigators

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Abstract

In FY21, we continued to pursue two lines of research, focusing on 1) characterizing the representation of stimulus features in primary visual cortex and 2) studying how these stimulus representations interact with feedback signals to visual cortex associated with general arousal, emotional valence, and object-selective processes. Studies were carried out under clinical protocol NCT00001360. 1) Characterizing stimulus representations in human visual cortex. A central goal in the laboratory is to understand the neural computations that give rise to stimulus feature selectivity. Many of the studies in our group use the visual system as a model, and specifically study the computations that lead to orientation selectivity. 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. It is well established that orientation-selective V1 neurons are organized at a fine spatial scale in a pseudo-periodic, columnar structure across the cortical surface. However, 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. In FY21, we have developed a population model of V1 that provides a computational framework for investigating orientation selectivity (Gardner and Merriam, 2021). Using the model, we have demonstrated that three theoretically distinct neural mechanisms could each contribute independently to orientation biases: stimulus vignetting, neural gain fields, and asymmetric surround suppression. This modeling result shows that these mechanisms can easily be confused with one another. For example, attempts to measure surround suppression, which is thought to be a marker for excitatory/inhibitory imbalance in cortex, and implicated in a wide range of neuropsychiatric disorders, could in fact be confounded with other neural mechanisms. Another implication of the model is that it should be possible to isolate orientation-selectivity signals arising from each of these factors. However, our modeling work suggests that the relatively low signal-to-noise ratio of fMRI may limit the ability to achieve this. We are currently analyzing a very large publicly-available dataset of fMRI responses to naturalistic visual stimuli. This large dataset, collected at high-field strength with many repeated measurements from a small group of participants, may provide insights into the relative contribution of each of these mechanisms for orientation selectivity. Our work on understanding neural computations in the intact visual system is vital in determining how computations are altered in mental health and neurological disorders. 2) The role of feedback in visual processing A second theme in the laboratory is to understand the influence of non-sensory cognitive signals in visual perception. We have identified a type of brain activity that reflects a 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 spatial attention in that it is global in cortex rather than retinotopically-specific. This activity may be related to general arousal. To test this hypothesis, we systematically varied 1) task difficulty, 2) the expected reward for correct performance, and 3) the temporal predictability of the task structure. We found that a widespread fMRI response tracks arousal level in each of these task conditions, exhibiting a significance correlation with pupil size. A manuscript on this set of studies is currently under review. Understanding the neural mechanisms of 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). We have begun to use high-resolution, high-field strength fMRI to study feedback signals in individual layers in visual cortex. We have used this cutting-edge approach to study the laminar profile of responses to faces that differ with regard to emotional valence (e.g., pictures of faces with fearful or happy expressions). We are also using this approach to study feedback signals related to object perception. These studies are currently in progress and will be a focus of the lab during the coming year.