Visual context affects the perceived timing of tactile sensations elicited through intra-cortical microstimulation.

Intra-cortical microstimulation (ICMS) is a technique to provide tactile sensations for a somatosensory brain-machine interface (BMI). A viable BMI must function within the rich, multisensory environment of the real world, but how ICMS is integrated with other sensory modalities is poorly understood. To investigate how ICMS percepts are integrated with visual information, ICMS and visual stimuli were delivered at varying times relative to one another. Both visual context and ICMS current amplitude were found to bias the qualitative experience of ICMS. In two tetraplegic participants, ICMS and visual stimuli were more likely to be experienced as occurring simultaneously when visual stimuli were more realistic, demonstrating an effect of visual context on the temporal binding window. The peak of the temporal binding window varied but was consistently offset from zero, suggesting that multisensory integration with ICMS can suffer from temporal misalignment. Recordings from primary somatosensory cortex (S1) during catch trials where visual stimuli were delivered without ICMS demonstrated that S1 represents visual information related to ICMS across visual contexts.

S1 represents multisensory contexts and somatotopic locations within and outside the bounds of the cortical homunculus.

Recent literature suggests that tactile events are represented in the primary somatosensory cortex (S1) beyond its long-established topography; in addition, the extent to which S1 is modulated by vision remains unclear. To better characterize S1, human electrophysiological data were recorded during touches to the forearm or finger. Conditions included visually observed physical touches, physical touches without vision, and visual touches without physical contact. Two major findings emerge from this dataset. First, vision strongly modulates S1 area 1, but only if there is a physical element to the touch, suggesting that passive touch observation is insufficient to elicit neural responses. Second, despite recording in a putative arm area of S1, neural activity represents both arm and finger stimuli during physical touches. Arm touches are encoded more strongly and specifically, supporting the idea that S1 encodes tactile events primarily through its topographic organization but also more generally, encompassing other areas of the body.

Temporal dynamics of the neural representation of hue and luminance polarity.

Hue and luminance contrast are basic visual features. Here we use multivariate analyses of magnetoencephalography data to investigate the timing of the neural computations that extract them, and whether they depend on common neural circuits. We show that hue and luminance-contrast polarity can be decoded from MEG data and, with lower accuracy, both features can be decoded across changes in the other feature. These results are consistent with the existence of both common and separable neural mechanisms. The decoding time course is earlier and more temporally precise for luminance polarity than hue, a result that does not depend on task, suggesting that luminance contrast is an updating signal that separates visual events. Meanwhile, cross-temporal generalization is slightly greater for representations of hue compared to luminance polarity, providing a neural correlate of the preeminence of hue in perceptual grouping and memory. Finally, decoding of luminance polarity varies depending on the hues used to obtain training and testing data. The pattern of results is consistent with observations that luminance contrast is mediated by both L-M and S cone sub-cortical mechanisms.

The Neurophysiological Representation of Imagined Somatosensory Percepts in Human Cortex.

Intracortical microstimulation (ICMS) in human primary somatosensory cortex (S1) has been used to successfully evoke naturalistic sensations. However, the neurophysiological mechanisms underlying the evoked sensations remain unknown. To understand how specific stimulation parameters elicit certain sensations we must first understand the representation of those sensations in the brain. In this study we record from intracortical microelectrode arrays implanted in S1, premotor cortex, and posterior parietal cortex of a male human participant performing a somatosensory imagery task. The sensations imagined were those previously elicited by ICMS of S1, in the same array of the same participant. In both spike and local field potential recordings, features of the neural signal can be used to classify different imagined sensations. These features are shown to be stable over time. The sensorimotor cortices only encode the imagined sensation during the imagery task, while posterior parietal cortex encodes the sensations starting with cue presentation. These findings demonstrate that different aspects of the sensory experience can be individually decoded from intracortically recorded human neural signals across the cortical sensory network. Activity underlying these unique sensory representations may inform the stimulation parameters for precisely eliciting specific sensations via ICMS in future work.SIGNIFICANCE STATEMENT Electrical stimulation of human cortex is increasingly more common for providing feedback in neural devices. Understanding the relationship between naturally evoked and artificially evoked neurophysiology for the same sensations will be important in advancing such devices. Here, we investigate the neural activity in human primary somatosensory, premotor, and parietal cortices during somatosensory imagery. The sensations imagined were those previously elicited during intracortical microstimulation (ICMS) of the same somatosensory electrode array. We elucidate the neural features during somatosensory imagery that significantly encode different aspects of individual sensations and demonstrate feature stability over almost a year. The correspondence between neurophysiology elicited with or without stimulation for the same sensations will inform methods to deliver more precise feedback through stimulation in the future.

Color Space Geometry Uncovered with Magnetoencephalography.

The geometry that describes the relationship among colors, and the neural mechanisms that support color vision, are unsettled. Here, we use multivariate analyses of measurements of brain activity obtained with magnetoencephalography to reverse-engineer a geometry of the neural representation of color space. The analyses depend upon determining similarity relationships among the spatial patterns of neural responses to different colors and assessing how these relationships change in time. We evaluate the approach by relating the results to universal patterns in color naming. Two prominent patterns of color naming could be accounted for by the decoding results: the greater precision in naming warm colors compared to cool colors evident by an interaction of hue and lightness, and the preeminence among colors of reddish hues. Additional experiments showed that classifiers trained on responses to color words could decode color from data obtained using colored stimuli, but only at relatively long delays after stimulus onset. These results provide evidence that perceptual representations can give rise to semantic representations, but not the reverse. Taken together, the results uncover a dynamic geometry that provides neural correlates for color appearance and generates new hypotheses about the structure of color space.

Deconstructing Theory-of-Mind Impairment in High-Functioning Adults with Autism.

Inferring the beliefs, desires, and intentions of other people ("theory of mind," ToM) requires specialized psychological processes that represent the minds of others as distinct from our own [1-3]. ToM is engaged ubiquitously in our everyday social behavior and features a specific developmental trajectory [4] that is notably delayed in children with autism spectrum disorder (ASD) [5, 6]. In healthy individuals, model-based analyses of social learning and decision-making have successfully elucidated specific computational components of ToM processing [7-11]. However, the use of this approach to study ToM impairment in ASD has been extremely limited [10, 12]. To better characterize specific ToM impairment in ASD, we developed a novel learning task and applied model-based analyses in high-functioning adults with ASD and matched healthy controls. After completing a charitable donation task, participants performed a "mentalizer" task in which they observed another person (the agent) complete the same charity task. The mentalizer task probed the participants' ability to acquire and use ToM representations. To accurately predict agent behavior, participants needed to dynamically track the agent's beliefs (true or false) about an experimental context that varied over time and use that information to infer the agent's intentions from their actions. ASD participants were specifically impaired at using their estimates of agent belief to learn agent intentions, though their ability to track agent belief was intact and their reasoning about belief and intentions was rational. Furthermore, model parameters correlated with aspects of social functioning, e.g., ADOS severity scores [13]. Together, these results identify novel, and more specific, targets for future research.

Color statistics of objects, and color tuning of object cortex in macaque monkey.

We hypothesized that the parts of scenes identified by human observers as "objects" show distinct color properties from backgrounds, and that the brain uses this information towards object recognition. To test this hypothesis, we examined the color statistics of naturally and artificially colored objects and backgrounds in a database of over 20,000 images annotated with object labels. Objects tended to be warmer colored (L-cone response > M-cone response) and more saturated compared to backgrounds. That the distinguishing chromatic property of objects was defined mostly by the L-M post-receptoral mechanism, rather than the S mechanism, is consistent with the idea that trichromatic color vision evolved in response to a selective pressure to identify objects. We also show that classifiers trained using only color information could distinguish animate versus inanimate objects, and at a performance level that was comparable to classification using shape features. Animate/inanimate is considered a fundamental superordinate category distinction, previously thought to be computed by the brain using only shape information. Our results show that color could contribute to animate/inanimate, and likely other, object-category assignments. Finally, color-tuning measured in two macaque monkeys with functional magnetic resonance imaging (fMRI), and confirmed by fMRI-guided microelectrode recording, supports the idea that responsiveness to color reflects the global functional organization of inferior temporal cortex, the brain region implicated in object vision. More strongly in IT than in V1, colors associated with objects elicited higher responses than colors less often associated with objects.