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Deep neural networks (DNNs) optimized for visual tasks learn representations that align layer depth with the hierarchy of visual areas in the primate brain. One interpretation of this finding is that hierarchical representations are necessary to accurately predict brain activity in the primate visual system. To test this interpretation, we optimized DNNs to directly predict brain activity measured with fMRI in human visual areas V1-V4. We trained a single-branch DNN to predict activity in all four visual areas jointly, and a multi-branch DNN to predict each visual area independently. Although it was possible for the multi-branch DNN to learn hierarchical representations, only the single-branch DNN did so. This result shows that hierarchical representations are not necessary to accurately predict human brain activity in V1-V4, and that DNNs that encode brain-like visual representations may differ widely in their architecture, ranging from strict serial hierarchies to multiple independent branches.

 

Abstract Orientation selectivity in primate visual cortex is organized into cortical columns. Since cortical columns are at a finer spatial scale than the sampling resolution of standard BOLD fMRI measurements, analysis approaches have been proposed to peer past these spatial resolution limitations. It was recently found that these methods are predominantly sensitive to stimulus vignetting - a form of selectivity arising from an interaction of the oriented stimulus with the aperture edge. Beyond vignetting, it is not clear whether orientation-selective neural responses are detectable in BOLD measurements. Here, we leverage a dataset of visual cortical responses measured using high-field 7T fMRI. Fitting these responses using image-computable models, we compensate for vignetting and nonetheless find reliable tuning for orientation. Results further reveal a coarse-scale map of orientation preference that may constitute the neural basis for known perceptual anisotropies. These findings settle a long-standing debate in human neuroscience, and provide insights into functional organization principles of visual cortex. 

Converging, cross-species evidence indicates that memory for time is supported by hippocampal area CA1 and entorhinal cortex. However, limited evidence characterizes how these regions preserve temporal memories over long timescales (e.g., months). At long timescales, memoranda may be encountered in multiple temporal contexts, potentially creating interference. Here, using 7T fMRI, we measured CA1 and entorhinal activity patterns as human participants viewed thousands of natural scene images distributed, and repeated, across many months. We show that memory for an image’s original temporal context was predicted by the degree to which CA1/entorhinal activity patterns from the first encounter with an image were re-expressed during re-encounters occurring minutes to months later. Critically, temporal memory signals were dissociable from predictors of recognition confidence, which were carried by distinct medial temporal lobe expressions. These findings suggest that CA1 and entorhinal cortex preserve temporal memories across long timescales by coding for and reinstating temporal context information.

 

Experimental datasets are growing rapidly in size, scope, and detail, but the value of these datasets is limited by unwanted measurement noise. It is therefore tempting to apply analysis techniques that attempt to reduce noise and enhance signals of interest. In this paper, we draw attention to the possibility that denoising methods may introduce bias and lead to incorrect scientific inferences. To present our case, we first review the basic statistical concepts of bias and variance. Denoising techniques typically reduce variance observed across repeated measurements, but this can come at the expense of introducing bias to the average expected outcome. We then conduct three simple simulations that provide concrete examples of how bias may manifest in everyday situations. These simulations reveal several findings that may be surprising and counterintuitive: (i) different methods can be equally effective at reducing variance but some incur bias while others do not, (ii) identifying methods that better recover ground truth does not guarantee the absence of bias, (iii) bias can arise even if one has specific knowledge of properties of the signal of interest. We suggest that researchers should consider and possibly quantify bias before deploying denoising methods on important research data. 

Advances in artificial intelligence have inspired a paradigm shift in human neuroscience, yielding large-scale functional magnetic resonance imaging (fMRI) datasets that provide high-resolution brain responses to thousands of naturalistic visual stimuli. Because such experiments necessarily involve brief stimulus durations and few repetitions of each stimulus, achieving sufficient signal-to-noise ratio can be a major challenge. We address this challenge by introducing GLMsingle , a scalable, user-friendly toolbox available in MATLAB and Python that enables accurate estimation of single-trial fMRI responses ( glmsingle.org ). Requiring only fMRI time-series data and a design matrix as inputs, GLMsingle integrates three techniques for improving the accuracy of trial-wise general linear model (GLM) beta estimates. First, for each voxel, a custom hemodynamic response function (HRF) is identified from a library of candidate functions. Second, cross-validation is used to derive a set of noise regressors from voxels unrelated to the experiment. Third, to improve the stability of beta estimates for closely spaced trials, betas are regularized on a voxel-wise basis using ridge regression. Applying GLMsingle to the Natural Scenes Dataset and BOLD5000, we find that GLMsingle substantially improves the reliability of beta estimates across visually-responsive cortex in all subjects. Comparable improvements in reliability are also observed in a smaller-scale auditory dataset from the StudyForrest experiment. These improvements translate into tangible benefits for higher-level analyses relevant to systems and cognitive neuroscience. We demonstrate that GLMsingle: (i) helps decorrelate response estimates between trials nearby in time; (ii) enhances representational similarity between subjects within and across datasets; and (iii) boosts one-versus-many decoding of visual stimuli. GLMsingle is a publicly available tool that can significantly improve the quality of past, present, and future neuroimaging datasets sampling brain activity across many experimental conditions. 

The brain mechanisms of memory consolidation remain elusive. Here, we examine blood-oxygen-level-dependent (BOLD) correlates of image recognition through the scope of multiple influential systems consolidation theories. We utilize the longitudinal Natural Scenes Dataset, a 7-Tesla functional magnetic resonance imaging human study in which ∼135,000 trials of image recognition were conducted over the span of a year among eight subjects. We find that early- and late-stage image recognition associates with both medial temporal lobe (MTL) and visual cortex when evaluating regional activations and a multivariate classifier. Supporting multiple-trace theory (MTT), parts of the MTL activation time course show remarkable fit to a 20-y-old MTT time-dynamical model predicting early trace intensity increases and slight subsequent interference ( R 2 > 0.90). These findings contrast a simplistic, yet common, view that memory traces are transferred from MTL to cortex. Next, we test the hypothesis that the MTL trace signature of memory consolidation should also reflect synaptic “desaturation,” as evidenced by an increased signal-to-noise ratio. We find that the magnitude of relative BOLD enhancement among surviving memories is positively linked to the rate of removal (i.e., forgetting) of competing traces. Moreover, an image-feature and time interaction of MTL and visual cortex functional connectivity suggests that consolidation mechanisms improve the specificity of a distributed trace. These neurobiological effects do not replicate on a shorter timescale (within a session), implicating a prolonged, offline process. While recognition can potentially involve cognitive processes outside of memory retrieval (e.g., re-encoding), our work largely favors MTT and desaturation as perhaps complementary consolidative memory mechanisms. 

How variable is the functionally defined structure of early visual areas in human cortex and how much variability is shared between twins? Here we quantify individual differences in the best understood functionally defined regions of cortex: V1, V2, V3. The Human Connectome Project 7T Retinotopy Dataset includes retinotopic measurements from 181 subjects (109 female, 72 male), including many twins. We trained four “anatomists” to manually define V1-V3 using retinotopic features. These definitions were more accurate than automated anatomical templates and showed that surface areas for these maps varied more than threefold across individuals. This threefold variation was little changed when normalizing visual area size by the surface area of the entire cerebral cortex. In addition to varying in size, we find that visual areas vary in how they sample the visual field. Specifically, the cortical magnification function differed substantially among individuals, with the relative amount of cortex devoted to central vision varying by more than a factor of 2. To complement the variability analysis, we examined the similarity of visual area size and structure across twins. Whereas the twin sample sizes are too small to make precise heritability estimates (50 monozygotic pairs, 34 dizygotic pairs), they nonetheless reveal high correlations, consistent with strong effects of the combination of shared genes and environment on visual area size. Collectively, these results provide the most comprehensive account of individual variability in visual area structure to date, and provide a robust population benchmark against which new individuals and developmental and clinical populations can be compared.

SIGNIFICANCE STATEMENTAreas V1, V2, and V3 are among the best studied functionally defined regions in human cortex. Using the largest retinotopy dataset to date, we characterized the variability of these regions across individuals and the similarity between twin pairs. We find that the size of visual areas varies dramatically (up to 3.5×) across healthy young adults, far more than the variability of the cerebral cortex size as a whole. Much of this variability appears to arise from inherited factors, as we find very high correlations in visual area size between monozygotic twin pairs, and lower but still substantial correlations between dizygotic twin pairs. These results provide the most comprehensive assessment of how functionally defined visual cortex varies across the population to date.