Compressive Temporal Summation in Human Visual Cortex

• Published in: The Journal of neuroscience Vol. 38; no. 3; pp. 691 - 709
• Main Authors: Zhou, Jingyang, Benson, Noah C., Kay, Kendrick N., Winawer, Jonathan
• Format: Journal Article
• Language: English
• Published: United States Society for Neuroscience 17.01.2018
• Subjects: Adult; Brain; Brain mapping; Brain Mapping - methods; Cortex (somatosensory); Cortex (temporal); Female; Functional magnetic resonance imaging; Humans; Information processing; Linear prediction; Magnetic Resonance Imaging; Male; Medical imaging; Middle Aged; Models, Neurological; Neuroimaging; Neurology; Nonlinear systems; Receptive field; Sensory stimulation; Signal processing; Spatial distribution; Temporal resolution; Time; Visual cortex; Visual Cortex - physiology; Visual pathways; Visual Perception - physiology; Visual signals; Visual stimuli; Young Adult; fMRI; adaptation; temporal summation; population receptive fields; visual cortex; visual hierarchy
• ISSN: 0270-6474; 1529-2401; 1529-2401
• DOI: 10.1523/JNEUROSCI.1724-17.2017

Combining sensory inputs over space and time is fundamental to vision. Population receptive field models have been successful in characterizing spatial encoding throughout the human visual pathways. A parallel question, how visual areas in the human brain process information distributed over time, has received less attention. One challenge is that the most widely used neuroimaging method, fMRI, has coarse temporal resolution compared with the time-scale of neural dynamics. Here, via carefully controlled temporally modulated stimuli, we show that information about temporal processing can be readily derived from fMRI signal amplitudes in male and female subjects. We find that all visual areas exhibit subadditive summation, whereby responses to longer stimuli are less than the linear prediction from briefer stimuli. We also find fMRI evidence that the neural response to two stimuli is reduced for brief interstimulus intervals (indicating adaptation). These effects are more pronounced in visual areas anterior to V1-V3. Finally, we develop a general model that shows how these effects can be captured with two simple operations: temporal summation followed by a compressive nonlinearity. This model operates for arbitrary temporal stimulation patterns and provides a simple and interpretable set of computations that can be used to characterize neural response properties across the visual hierarchy. Importantly, compressive temporal summation directly parallels earlier findings of compressive spatial summation in visual cortex describing responses to stimuli distributed across space. This indicates that, for space and time, cortex uses a similar processing strategy to achieve higher-level and increasingly invariant representations of the visual world. SIGNIFICANCE STATEMENT Combining sensory inputs over time is fundamental to seeing. Two important temporal phenomena are summation, the accumulation of sensory inputs over time, and adaptation, a response reduction for repeated or sustained stimuli. We investigated these phenomena in the human visual system using fMRI. We built predictive models that operate on arbitrary temporal patterns of stimulation using two simple computations: temporal summation followed by a compressive nonlinearity. Our new temporal compressive summation model captures (1) subadditive temporal summation, and (2) adaptation. We show that the model accounts for systematic differences in these phenomena across visual areas. Finally, we show that for space and time, the visual system uses a similar strategy to achieve increasingly invariant representations of the visual world.