Apparent thinning of human visual cortex during childhood is associated with myelination.

Human cortex appears to thin during childhood development. However, the underlying microstructural mechanisms are unknown. Using functional magnetic resonance imaging (fMRI), quantitative MRI (qMRI), and diffusion MRI (dMRI) in children and adults, we tested what quantitative changes occur to gray and white matter in ventral temporal cortex (VTC) from childhood to adulthood, and how these changes relate to cortical thinning. T1 relaxation time from qMRI and mean diffusivity (MD) from dMRI provide independent and complementary measurements of microstructural properties of gray and white matter tissue. In face- and character-selective regions in lateral VTC, T1 and MD decreased from age 5 to adulthood in mid and deep cortex, as well as in their adjacent white matter. T1 reduction also occurred longitudinally in children's brain regions. T1 and MD decreases 1) were consistent with tissue growth related to myelination, which we verified with adult histological myelin stains, and 2) were correlated with apparent cortical thinning. In contrast, in place-selective cortex in medial VTC, we found no development of T1 or MD after age 5, and thickness was related to cortical morphology. These findings suggest that lateral VTC likely becomes more myelinated from childhood to adulthood, affecting the contrast of MR images and, in turn, the apparent gray-white boundary. These findings are important because they suggest that VTC does not thin during childhood but instead gets more myelinated. Our data have broad ramifications for understanding both typical and atypical brain development using advanced in vivo quantitative measurements and clinical conditions implicating myelin.

Differential sustained and transient temporal processing across visual streams.

How do high-level visual regions process the temporal aspects of our visual experience? While the temporal sensitivity of early visual cortex has been studied with fMRI in humans, temporal processing in high-level visual cortex is largely unknown. By modeling neural responses with millisecond precision in separate sustained and transient channels, and introducing a flexible encoding framework that captures differences in neural temporal integration time windows and response nonlinearities, we predict fMRI responses across visual cortex for stimuli ranging from 33 ms to 20 s. Using this innovative approach, we discovered that lateral category-selective regions respond to visual transients associated with stimulus onsets and offsets but not sustained visual information. Thus, lateral category-selective regions compute moment-to-moment visual transitions, but not stable features of the visual input. In contrast, ventral category-selective regions process both sustained and transient components of the visual input. Our model revealed that sustained channel responses to prolonged stimuli exhibit adaptation, whereas transient channel responses to stimulus offsets are surprisingly larger than for stimulus onsets. This large offset transient response may reflect a memory trace of the stimulus when it is no longer visible, whereas the onset transient response may reflect rapid processing of new items. Together, these findings reveal previously unconsidered, fundamental temporal mechanisms that distinguish visual streams in the human brain. Importantly, our results underscore the promise of modeling brain responses with millisecond precision to understand the underlying neural computations.

Learning to Read Increases the Informativeness of Distributed Ventral Temporal Responses.

Becoming a proficient reader requires substantial learning over many years. However, it is unknown how learning to read affects development of distributed visual representations across human ventral temporal cortex (VTC). Using fMRI and a data-driven, computational approach, we quantified the development of distributed VTC responses to characters (pseudowords and numbers) versus other domains in children, preteens, and adults. Results reveal anatomical- and hemisphere-specific development. With development, distributed responses to words and characters became more distinctive and informative in lateral but not medial VTC, and in the left but not right hemisphere. While the development of voxels with both positive and negative preference to words affected distributed information, only development of voxels with positive preference to words (i.e., word-selective) was correlated with reading ability. These data show that developmental increases in informativeness of distributed left lateral VTC responses are related to proficient reading and have important implications for both developmental theories and for elucidating neural mechanisms of reading disabilities.

Development of population receptive fields in the lateral visual stream improves spatial coding amid stable structural-functional coupling.

Human visual cortex encompasses more than a dozen visual field maps across three major processing streams. One of these streams is the lateral visual stream, which extends from V1 to lateral-occipital (LO) and temporal-occipital (TO) visual field maps and plays a prominent role in shape as well as motion perception. However, it is unknown if and how population receptive fields (pRFs) in the lateral visual stream develop from childhood to adulthood, and what impact this development may have on spatial coding. Here, we used functional magnetic resonance imaging and pRF modeling in school-age children and adults to investigate the development of the lateral visual stream. Our data reveal four main findings: 1) The topographic organization of eccentricity and polar angle maps of the lateral stream is stable after age five. 2) In both age groups there is a reliable relationship between eccentricity map transitions and cortical folding: the middle occipital gyrus predicts the transition between the peripheral representation of LO and TO maps. 3) pRFs in LO and TO maps undergo differential development from childhood to adulthood, resulting in increasing coverage of the central visual field in LO and of the peripheral visual field in TO. 4) Model-based decoding shows that the consequence of pRF and visual field coverage development is improved spatial decoding from LO and TO distributed responses in adults vs. children. Together, these results explicate both the development and topography of the lateral visual stream. Our data show that the general structural-functional organization is laid out early in development, but fine-scale properties, such as pRF distribution across the visual field and consequently, spatial precision, become fine-tuned across childhood development. These findings advance understanding of the development of the human visual system from childhood to adulthood and provide an essential foundation for understanding developmental deficits.

A preference for mathematical processing outweighs the selectivity for Arabic numbers in the inferior temporal gyrus.

A region in the posterior inferior temporal gyrus (ITG), referred to as the number form area (NFA, here ITG-numbers) has been implicated in the visual processing of Arabic numbers. However, it is unknown if this region is specifically involved in the visual encoding of Arabic numbers per se or in mathematical processing more broadly. Using functional magnetic resonance imaging (fMRI) during experiments that systematically vary tasks and stimuli, we find that mathematical processing, not preference to Arabic numbers, consistently drives both mean and distributed responses in the posterior ITG. While we replicated findings of higher responses in ITG-numbers to numbers than other visual stimuli during a 1-back task, this preference to numbers was abolished when participants engaged in mathematical processing. In contrast, an ITG region (ITG-math) that showed higher responses during an adding task vs. other tasks maintained this preference for mathematical processing across a wide range of stimuli including numbers, number/letter morphs, hands, and dice. Analysis of distributed responses across an anatomically-defined posterior ITG expanse further revealed that mathematical task but not Arabic number form can be successfully and consistently decoded from these distributed responses. Together, our findings suggest that the function of neuronal regions in the posterior ITG goes beyond the specific visual processing of Arabic numbers. We hypothesize that they ascribe numerical content to the visual input, irrespective of the format of the stimulus.

Development differentially sculpts receptive fields across early and high-level human visual cortex.

Receptive fields (RFs) processing information in restricted parts of the visual field are a key property of visual system neurons. However, how RFs develop in humans is unknown. Using fMRI and population receptive field (pRF) modeling in children and adults, we determine where and how pRFs develop across the ventral visual stream. Here we report that pRF properties in visual field maps, from the first visual area, V1, through the first ventro-occipital area, VO1, are adult-like by age 5. However, pRF properties in face-selective and character-selective regions develop into adulthood, increasing the foveal coverage bias for faces in the right hemisphere and words in the left hemisphere. Eye-tracking indicates that pRF changes are related to changing fixation patterns on words and faces across development. These findings suggest a link between face and word viewing behavior and the differential development of pRFs across visual cortex, potentially due to competition on foveal coverage.

Encoding model of temporal processing in human visual cortex.

How is temporal information processed in human visual cortex? Visual input is relayed to V1 through segregated transient and sustained channels in the retina and lateral geniculate nucleus (LGN). However, there is intense debate as to how sustained and transient temporal channels contribute to visual processing beyond V1. The prevailing view associates transient processing predominately with motion-sensitive regions and sustained processing with ventral stream regions, while the opposing view suggests that both temporal channels contribute to neural processing beyond V1. Using fMRI, we measured cortical responses to time-varying stimuli and then implemented a two temporal channel-encoding model to evaluate the contributions of each channel. Different from the general linear model of fMRI that predicts responses directly from the stimulus, the encoding approach first models neural responses to the stimulus from which fMRI responses are derived. This encoding approach not only predicts cortical responses to time-varying stimuli from milliseconds to seconds but also, reveals differential contributions of temporal channels across visual cortex. Consistent with the prevailing view, motion-sensitive regions and adjacent lateral occipitotemporal regions are dominated by transient responses. However, ventral occipitotemporal regions are driven by both sustained and transient channels, with transient responses exceeding the sustained. These findings propose a rethinking of temporal processing in the ventral stream and suggest that transient processing may contribute to rapid extraction of the content of the visual input. Importantly, our encoding approach has vast implications, because it can be applied with fMRI to decipher neural computations in millisecond resolution in any part of the brain.