Naturalistic Audio-Movies and Narrative Synchronize "Visual" Cortices across Congenitally Blind But Not Sighted Individuals.

How does developmental experience, as opposed to intrinsic physiology, shape cortical function? Naturalistic stimuli were used to elicit neural synchrony in individuals blind from birth (n = 18) and those who grew up with sight (n = 18). Blind and blindfolded sighted participants passively listened to three audio-movie clips, an auditory narrative, a sentence shuffled version of the narrative (maintaining language but lacking a plotline), and a version of the narrative backward (lacking both language and plot). For both groups, early auditory cortices were synchronized to a similar degree across stimulus types, whereas higher-cognitive temporoparietal and prefrontal areas were more synchronized by meaningful, temporally extended stimuli (i.e., audio movies and narrative). "Visual" cortices were more synchronized across blind than sighted individuals, but only for audio-movies and narrative. In the blind group, visual cortex synchrony was low for backward speech and intermediate for sentence shuffle. Meaningful auditory stimuli synchronize visual cortices of people born blind.SIGNIFICANCE STATEMENT Naturalistic stimuli engage cognitive processing at many levels. Here, we harnessed this richness to investigate the effect of experience on cortical function. We find that listening to naturalistic audio movies and narrative drives synchronized activity across "visual" cortices of blind, more so than sighted, individuals. Visual cortex synchronization varies with meaningfulness and cognitive complexity. Higher synchrony is observed for temporally extended meaningful stimuli (e.g., movies/narrative), intermediate for shuffled sentences, lowest for time varying complex noise. By contrast, auditory cortex was synchronized equally by meaningful and meaningless stimuli. In congenitally blind individuals most of visual cortex is engaged by meaningful naturalistic stimuli.

Knowledge of animal appearance among sighted and blind adults.

How does first-person sensory experience contribute to knowledge? Contrary to the suppositions of early empiricist philosophers, people who are born blind know about phenomena that cannot be perceived directly, such as color and light. Exactly what is learned and how remains an open question. We compared knowledge of animal appearance across congenitally blind (n = 20) and sighted individuals (two groups, n = 20 and n = 35) using a battery of tasks, including ordering (size and height), sorting (shape, skin texture, and color), odd-one-out (shape), and feature choice (texture). On all tested dimensions apart from color, sighted and blind individuals showed substantial albeit imperfect agreement, suggesting that linguistic communication and visual perception convey partially redundant appearance information. To test the hypothesis that blind individuals learn about appearance primarily by remembering sighted people's descriptions of what they see (e.g., "elephants are gray"), we measured verbalizability of animal shape, texture, and color in the sighted. Contrary to the learn-from-description hypothesis, blind and sighted groups disagreed most about the appearance dimension that was easiest for sighted people to verbalize: color. Analysis of disagreement patterns across all tasks suggest that blind individuals infer physical features from non-appearance properties of animals such as folk taxonomy and habitat (e.g., bats are textured like mammals but shaped like birds). These findings suggest that in the absence of sensory access, structured appearance knowledge is acquired through inference from ontological kind.

Occipital cortex of blind individuals is functionally coupled with executive control areas of frontal cortex.

In congenital blindness, the occipital cortex responds to a range of nonvisual inputs, including tactile, auditory, and linguistic stimuli. Are these changes in functional responses to stimuli accompanied by altered interactions with nonvisual functional networks? To answer this question, we introduce a data-driven method that searches across cortex for functional connectivity differences across groups. Replicating prior work, we find increased fronto-occipital functional connectivity in congenitally blind relative to blindfolded sighted participants. We demonstrate that this heightened connectivity extends over most of occipital cortex but is specific to a subset of regions in the inferior, dorsal, and medial frontal lobe. To assess the functional profile of these frontal areas, we used an n-back working memory task and a sentence comprehension task. We find that, among prefrontal areas with overconnectivity to occipital cortex, one left inferior frontal region responds to language over music. By contrast, the majority of these regions responded to working memory load but not language. These results suggest that in blindness occipital cortex interacts more with working memory systems and raise new questions about the function and mechanism of occipital plasticity.

Shindigs, brunches, and rodeos: the neural basis of event words.

Events (e.g., "running" or "eating") constitute a basic type within human cognition and human language. We asked whether thinking about events, as compared to other conceptual categories, depends on partially independent neural circuits. Indirect evidence for this hypothesis comes from previous studies showing elevated posterior temporal responses to verbs, which typically label events. Neural responses to verbs could, however, be driven either by their grammatical or by their semantic properties. In the present experiment, we separated the effects of grammatical class (verb vs. noun) and semantic category (event vs. object) by measuring neural responses to event nouns (e.g., "the hurricane"). Participants rated the semantic relatedness of event nouns, as well as of two categories of object nouns-animals (e.g., "the alligator") and plants (e.g., "the acorn")-and three categories of verbs-manner of motion (e.g., "to roll"), emission (e.g., "to sparkle"), and perception (e.g., "to gaze"). As has previously been observed, we found larger responses to verbs than to object nouns in the left posterior middle (LMTG) and superior (LSTG) temporal gyri. Crucially, we also found that the LMTG responds more to event than to object nouns. These data suggest that part of the posterior lateral temporal response to verbs is driven by their semantic properties. By contrast, a more superior region, at the junction of the temporal and parietal cortices, responded more to verbs than to all nouns, irrespective of their semantic category. We concluded that the neural mechanisms engaged when thinking about event and object categories are partially dissociable.

People can understand descriptions of motion without activating visual motion brain regions.

What is the relationship between our perceptual and linguistic neural representations of the same event? We approached this question by asking whether visual perception of motion and understanding linguistic depictions of motion rely on the same neural architecture. The same group of participants took part in two language tasks and one visual task. In task 1, participants made semantic similarity judgments with high motion (e.g., "to bounce") and low motion (e.g., "to look") words. In task 2, participants made plausibility judgments for passages describing movement ("A centaur hurled a spear … ") or cognitive events ("A gentleman loved cheese …"). Task 3 was a visual motion localizer in which participants viewed animations of point-light walkers, randomly moving dots, and stationary dots changing in luminance. Based on the visual motion localizer we identified classic visual motion areas of the temporal (MT/MST and STS) and parietal cortex (inferior and superior parietal lobules). We find that these visual cortical areas are largely distinct from neural responses to linguistic depictions of motion. Motion words did not activate any part of the visual motion system. Motion passages produced a small response in the right superior parietal lobule, but none of the temporal motion regions. These results suggest that (1) as compared to words, rich language stimuli such as passages are more likely to evoke mental imagery and more likely to affect perceptual circuits and (2) effects of language on the visual system are more likely in secondary perceptual areas as compared to early sensory areas. We conclude that language and visual perception constitute distinct but interacting systems.

Theory of mind performance in children correlates with functional specialization of a brain region for thinking about thoughts.

Thinking about other people's thoughts recruits a specific group of brain regions, including the temporo-parietal junctions (TPJ), precuneus (PC), and medial prefrontal cortex (MPFC). The same brain regions were recruited when children (N=20, 5-11 years) and adults (N=8) listened to descriptions of characters' mental states, compared to descriptions of physical events. Between ages 5 and 11 years, responses in the bilateral TPJ became increasingly specific to stories describing mental states as opposed to people's appearance and social relationships. Functional activity in the right TPJ was related to children's performance on a high level theory of mind task. These findings provide insights into the origin of neural mechanisms of theory of mind, and how behavioral and neural changes can be related in development.

A sensitive period for language in the visual cortex: distinct patterns of plasticity in congenitally versus late blind adults.

Recent evidence suggests that blindness enables visual circuits to contribute to language processing. We examined whether this dramatic functional plasticity has a sensitive period. BOLD fMRI signal was measured in congenitally blind, late blind (blindness onset 9-years-old or later) and sighted participants while they performed a sentence comprehension task. In a control condition, participants listened to backwards speech and made match/non-match to sample judgments. In both congenitally and late blind participants BOLD signal increased in bilateral foveal-pericalcarine cortex during response preparation, irrespective of whether the stimulus was a sentence or backwards speech. However, left occipital areas (pericalcarine, extrastriate, fusiform and lateral) responded more to sentences than backwards speech only in congenitally blind people. We conclude that age of blindness onset constrains the non-visual functions of occipital cortex: while plasticity is present in both congenitally and late blind individuals, recruitment of visual circuits for language depends on blindness during childhood.

Sensitive period for a multimodal response in human visual motion area MT/MST.

The middle temporal complex (MT/MST) is a brain region specialized for the perception of motion in the visual modality. However, this specialization is modified by visual experience: after long-standing blindness, MT/MST responds to sound. Recent evidence also suggests that the auditory response of MT/MST is selective for motion. The developmental time course of this plasticity is not known. To test for a sensitive period in MT/MST development, we used fMRI to compare MT/MST function in congenitally blind, late-blind, and sighted adults. MT/MST responded to sound in congenitally blind adults, but not in late-blind or sighted adults, and not in an individual who lost his vision between ages of 2 and 3 years. All blind adults had reduced functional connectivity between MT/MST and other visual regions. Functional connectivity was increased between MT/MST and lateral prefrontal areas in congenitally blind relative to sighted and late-blind adults. These data suggest that early blindness affects the function of feedback projections from prefrontal cortex to MT/MST. We conclude that there is a sensitive period for visual specialization in MT/MST. During typical development, early visual experience either maintains or creates a vision-dominated response. Once established, this response profile is not altered by long-standing blindness.

Neuroanatomically separable effects of imageability and grammatical class during single-word comprehension.

The present study characterizes the neural correlates of noun and verb imageability and addresses the question of whether components of the neural network supporting word recognition can be separately modified by variations in grammatical class and imageability. We examined the effect of imageability on BOLD signal during single-word comprehension of nouns and verbs. Subjects made semantic similarity judgments while undergoing functional magnetic resonance imaging (fMRI). Nouns and verbs were matched on imageability, and imageability varied continuously within a grammatical category. We observed three anatomically separable effects: a main effect of grammatical class, a main effect of imageability, and an imageability by grammatical class cross-over interaction. The left superior parietal lobule and a region in the left fusiform responded similarly to increases in noun and verb imageability; the left superior temporal gyrus showed greater activity for verbs than nouns after imageability was matched across grammatical class; and, in both the left middle temporal gyrus and the left inferior frontal lobe, a decrease in noun but not verb imageability resulted in higher BOLD signal. The presence of reliable and anatomically separable main effects of both imageability and grammatical class renders unlikely the hypothesis that previously reported dissociations between nouns and verbs can be dismissed as imageability effects. However, some regions previously thought to respond to grammatical class or imageability instead respond to the interaction of these variables.