Transfer of Tactile Learning from Trained to Untrained Body Parts Supported by Cortical Coactivation in Primary Somatosensory Cortex.

A pioneering study by Volkmann (1858) revealed that training on a tactile discrimination task improved task performance, indicative of tactile learning, and that such tactile learning transferred from trained to untrained body parts. However, the neural mechanisms underlying tactile learning and transfer of tactile learning have remained unclear. We trained groups of human subjects (female and male) in daily sessions on a tactile discrimination task either by stimulating the palm of the right hand or the sole of the right foot. Task performance before training was similar between the palm and sole. Posttraining transfer of tactile learning was greater from the trained right sole to the untrained right palm than from the trained right palm to the untrained right sole. Functional magnetic resonance imaging (fMRI) and multivariate pattern classification analysis revealed that the somatotopic representation of the right palm in contralateral primary somatosensory cortex (SI) was coactivated during tactile stimulation of the right sole. More pronounced coactivation in the cortical representation of the right palm was associated with lower tactile performance for tactile stimulation of the right sole and more pronounced subsequent transfer of tactile learning from the trained right sole to the untrained right palm. In contrast, coactivation of the cortical sole representation during tactile stimulation of the palm was less pronounced and no association with tactile performance and subsequent transfer of tactile learning was found. These results indicate that tactile learning may transfer to untrained body parts that are coactivated to support tactile learning with the trained body part.SIGNIFICANCE STATEMENT Perceptual skills such as the discrimination of tactile cues can improve by means of training, indicative of perceptual learning and sensory plasticity. However, it has remained unclear whether and if so, how such perceptual learning can occur if the training task is very difficult. Here, we show for tactile perceptual learning that the representation of the palm of the hand in primary somatosensory cortex (SI) is coactivated to support learning of a difficult tactile discrimination task with tactile stimulation of the sole of the foot. Such cortical coactivation of an untrained body part to support tactile learning with a trained body part might be critically involved in the subsequent transfer of tactile learning between the trained and untrained body parts.

Hierarchical categorization learning is associated with representational changes in the dorsal striatum and posterior frontal and parietal cortex.

Learning and recognition can be improved by sorting novel items into categories and subcategories. Such hierarchical categorization is easy when it can be performed according to learned rules (e.g., "if car, then automatic or stick shift" or "if boat, then motor or sail"). Here, we present results showing that human participants acquire categorization rules for new visual hierarchies rapidly, and that, as they do, corresponding hierarchical representations of the categorized stimuli emerge in patterns of neural activation in the dorsal striatum and in posterior frontal and parietal cortex. Participants learned to categorize novel visual objects into a hierarchy with superordinate and subordinate levels based on the objects' shape features, without having been told the categorization rules for doing so. On each trial, participants were asked to report the category and subcategory of the object, after which they received feedback about the correctness of their categorization responses. Participants trained over the course of a one-hour-long session while their brain activation was measured using functional magnetic resonance imaging. Over the course of training, significant hierarchy learning took place as participants discovered the nested categorization rules, as evidenced by the occurrence of a learning trial, after which performance suddenly increased. This learning was associated with increased representational strength of the newly acquired hierarchical rules in a corticostriatal network including the posterior frontal and parietal cortex and the dorsal striatum. We also found evidence suggesting that reinforcement learning in the dorsal striatum contributed to hierarchical rule learning.

Visual Attention Modulates Glutamate-Glutamine Levels in Vestibular Cortex: Evidence from Magnetic Resonance Spectroscopy.

Attending to a stimulus enhances the neuronal responses to it, while responses to nonattended stimuli are not enhanced and may even be suppressed. Although the neural mechanisms of response enhancement for attended stimuli have been intensely studied, the neural mechanisms underlying attentional suppression remain largely unknown. It is uncertain whether attention acts to suppress the processing in sensory cortical areas that would otherwise process the nonattended stimulus or the subcortical input to these cortical areas. Moreover, the neurochemical mechanisms inducing a reduction or suppression of neuronal responses to nonattended stimuli are as yet unknown. Here, we investigated how attention directed toward visual processing cross-modally acts to suppress vestibular responses in the human brain. By using functional magnetic resonance spectroscopy in a group of female and male subjects, we find that attention to visual motion downregulates in a load-dependent manner the concentration of excitatory neurotransmitter (glutamate and its precursor glutamine, referred to together as Glx) within the parietoinsular vestibular cortex (PIVC), a core cortical area of the vestibular system, while leaving the concentration of inhibitory neurotransmitter (GABA) in PIVC unchanged. This makes PIVC less responsive to excitatory thalamic vestibular input, as corroborated by functional magnetic resonance imaging. Together, our results suggest that attention acts to suppress the processing of nonattended sensory cues cortically by neurochemically rendering the core cortical area of the nonattended sensory modality less responsive to excitatory thalamic input.SIGNIFICANCE STATEMENT Here, we address a fundamental problem that has eluded attention research for decades, namely, how the brain ignores irrelevant stimuli. To date, three classes of solutions to this problem have been proposed: (1) enhancement of GABAergic interneuron activity in cortex, (2) downregulation of glutamatergic cell activity in cortex; and (3) downregulation of neural activity in thalamic projection areas, which would then provide the cortex with less input. Here, we use magnetic resonance spectroscopy in humans and find support for the second hypothesis, implying that attention to one sensory modality involves the suppression of irrelevant stimuli of another sensory modality by downregulating glutamate in the cortex.

Endogenous attention biases transformational apparent motion based on high-level shape representations.

When two pre-existing, separated squares are connected by the sudden onset of a bar between them, viewers do not perceive the bar to appear all at once. Instead, they see an illusory morphing of the original squares over time. The direction of this transformational apparent motion (TAM) can be influenced by endogenous attention deployed before the appearance of the connecting bar. Here, we investigated whether the influence of endogenous attention on TAM results from operations over high-level feature-independent shape representations, or instead over lower level shape representations defined by specific visual features. To do so, we tested the influence of endogenous attention on TAM in first- and second-order displays, which shared common shapes but had different shape-defining attributes (luminance and texture contrast, respectively). In terms of both the magnitude of directional bias and timing, we found that endogenous attention exerted a similar influence on both first- and second-order objects. These results imply that endogenous attention biases the perceived direction of TAM by operating on high-level shape representations that are invariant to the low-level visual features that define them. Our results support a four-stage model of TAM, where a feature encoding stage passes a features-specific layout to a parsing stage that forms discrete, high-level meta-featural shapes, which are then matched and visually interpolated over time.

The parahippocampal place area and hippocampus encode the spatial significance of landmark objects.

Landmark objects are points of reference that can anchor one's internal cognitive map to the external world while navigating. They are especially useful in indoor environments where other cues such as spatial geometries are often similar across locations. We used functional magnetic resonance imaging (fMRI) and multivariate pattern analysis (MVPA) to understand how the spatial significance of landmark objects is represented in the human brain. Participants learned the spatial layout of a virtual building with arbitrary objects as unique landmarks in each room during a navigation task. They were scanned while viewing the objects before and after learning. MVPA revealed that the neural representation of landmark objects in the right parahippocampal place area (rPPA) and the hippocampus transformed systematically according to their locations. Specifically, objects in different rooms became more distinguishable than objects in the same room. These results demonstrate that rPPA and the hippocampus encode the spatial significance of landmark objects in indoor spaces.

A position anchor sinks the double-drift illusion.

When the internal texture of a Gabor patch moves orthogonally to its envelope's motion, the perceived path, viewed in the periphery, shifts dramatically in position, and direction relative to the true path (the double-drift illusion). Here, we examine positional uncertainty as a critical factor underlying this illusory shift. We presented participants with an anchoring line at different distances from the drifting Gabor's physical path. Our results indicate that placing an anchor (a fixed line) close to the Gabor's path halved the magnitude of the illusion. This suppression was symmetrical for anchors placed on either side of the Gabor. In a second experiment, we used crowding to degrade the anchoring line's position information by embedding it in a set of parallel lines. In this case, despite the presence of the same lines that reduced the illusion when presented in isolation, the illusory shift was now largely restored. We suggest that the adjacent lines crowded each other, reducing their positional certainty, and thus their ability to anchor the location of the moving Gabor. These findings indicate that the positional uncertainty of the equiluminant Gabor patch is critical for the illusory position offset.

Effects of internal and external velocity on the perceived direction of the double-drift illusion.

In the double-drift illusion, the combination of the internal and external motion vectors produces large misperceptions of both position and direction of motion. Here, we investigate the role that speed plays in determining how these two sources of motion are combined to produce the double-drift illusion. To address this question, we measure the size of the illusion at seven internal speeds combined with six external speeds. We find that the illusion increases with increasing internal speed and decreases with increasing external speed. We model this by combining the external and internal vectors to produce the resulting, illusory direction (Tse & Hsieh, 2006). The relative effect of the two vectors is specified by a constant K in this model and the data reveal that K decreases linearly as external speed increases. This critical role of external speed in modulating the vector combination uncovers new details about how the visual system combines different sources of motion information to produce a global motion percept.

Smooth pursuit operates over perceived not physical positions of the double-drift stimulus.

The double-drift illusion produces a large deviation in perceived direction that strongly dissociates physical position from perceived position. Surprisingly, saccades do not seem to be affected by the illusion (Lisi & Cavanagh, 2015). When targeting a double-drift stimulus, the saccade system is driven by retinal rather than perceived position. Here, using paired double-drift targets, we test whether the smooth pursuit system is driven by perceived or physical position. Participants (n = 7) smoothly pursued the inferred midpoint (Steinbach, 1976) between two horizontally aligned Gabor patches that were separated by 20° and moving on parallel, oblique paths. On the first half of each trial, the Gabors' internal textures were static while both drifted obliquely downward. On the second half of each trial, while the envelope moved obliquely upward, the internal texture drifted orthogonally to the envelope's motion, producing a large perceived deviation from the downward path even though the upward and downward trajectories always followed the same physical path but in opposite directions. We find that smooth pursuit eye movements accurately followed the nonillusory downward path of the midpoint between the two Gabors, but then followed the illusory rather than the physical trajectory on the upward return. Thus, virtual targets for smooth pursuit are derived from perceived rather than retinal coordinates.

Long Time No See: Enduring Behavioral and Neuronal Changes in Perceptual Learning of Motion Trajectories 3 Years After Training.

Here, we report on the long-term stability of changes in behavior and brain activity following perceptual learning of conjunctions of simple motion features. Participants were trained for 3 weeks on a visual search task involving the detection of a dot moving in a "v"-shaped target trajectory among inverted "v"-shaped distractor trajectories. The first and last training sessions were carried out during functional magnetic resonance imaging (fMRI). Learning stability was again examined behaviorally and using fMRI 3 years after the end of training. Results show that acquired behavioral improvements were remarkably stable over time and that these changes were specific to trained target and distractor trajectories. A similar pattern was observed on the neuronal level, when the representation of target and distractor stimuli was examined in early retinotopic visual cortex (V1-V3): training enhanced activity for the target relative to the surrounding distractors in the search array and this enhancement persisted after 3 years. However, exchanging target and distractor trajectories abolished both neuronal and behavioral effects, suggesting that training-induced changes in stimulus representation are specific to trained stimulus identities.

The vector combination underlying the double-drift illusion is based on motion in world coordinates: Evidence from smooth pursuit.

If a Gabor pattern drifts in one direction while its internal texture drifts in the orthogonal direction, its perceived direction deviates strongly from its true direction and is instead some combination of its real external motion and its internal motion (Tse & Hsieh, 2006). In the first experiment, we confirm that, for the stimuli used in our experiment, the direction shifts on a gray background were explained by a vector combination of the internal and external motions whereas for the Gabor on a black background, we find no illusory shifts. These results suggest that the internal motion contributes to the perceived direction but only when the Gabor's positional uncertainty is high. Next, we test whether the vector combination is based on motions on the retina or motions in the world. When participants track a fixation point that moves in tandem with the Gabor, keeping it roughly stable on the retina, the illusion is undiminished. This finding indicates that the vector combination of internal and external motion that produces the double-drift illusion must happen after the eye movement signals have been factored into the stimulus motions to recover motions in the world, in particular, in areas V3A, V6, MSTd, and VIP.

Meridian interference reveals neural locus of motion-induced position shifts.

When a Gabor patch moves along a path in one direction while its internal texture drifts orthogonally to this path, it can appear to deviate from its physical path by 45° or more. This double-drift illusion is different from other motion-induced position shift effects in several ways: it has an integration period of over a second; the illusory displacement that accumulates over a second or more is orthogonal to rather than along the motion path; the perceptual deviations are much larger; and they have little or no effect on eye movements to the target. In this study we investigated the underlying neural mechanisms of the motion integration and position processing for this double-drift stimulus by testing possible anatomical constraints on its magnitude. We found that the illusion was reduced at the vertical and horizontal meridians when the perceptual path would cross or be driven toward the meridian, but not at other locations or other motion directions. The disruption of the accumulation of the position error at both the horizontal and vertical meridians suggests a central role of quadrantic areas in the generation of this type of motion-induced position shift. NEW & NOTEWORTHY The remarkably strong double-drift illusion is disrupted at both the vertical and horizontal meridians. We propose that this finding is the behavioral consequence of the anatomical gaps at both meridians, suggesting that neural areas with quadrantic representations (e.g., V2, V3) are the initial locus of this motion-induced position shift. This result rules out V1 as the source of the illusion because it has an anatomical break only at the vertical meridian.

Cross-Modal Attention Effects in the Vestibular Cortex during Attentive Tracking of Moving Objects.

The midposterior fundus of the Sylvian fissure in the human brain is central to the cortical processing of vestibular cues. At least two vestibular areas are located at this site: the parietoinsular vestibular cortex (PIVC) and the posterior insular cortex (PIC). It is now well established that activity in sensory systems is subject to cross-modal attention effects. Attending to a stimulus in one sensory modality enhances activity in the corresponding cortical sensory system, but simultaneously suppresses activity in other sensory systems. Here, we wanted to probe whether such cross-modal attention effects also target the vestibular system. To this end, we used a visual multiple-object tracking task. By parametrically varying the number of tracked targets, we could measure the effect of attentional load on the PIVC and the PIC while holding the perceptual load constant. Participants performed the tracking task during functional magnetic resonance imaging. Results show that, compared with passive viewing of object motion, activity during object tracking was suppressed in the PIVC and enhanced in the PIC. Greater attentional load, induced by increasing the number of tracked targets, was associated with a corresponding increase in the suppression of activity in the PIVC. Activity in the anterior part of the PIC decreased with increasing load, whereas load effects were absent in the posterior PIC. Results of a control experiment show that attention-induced suppression in the PIVC is stronger than any suppression evoked by the visual stimulus per se. Overall, our results suggest that attention has a cross-modal modulatory effect on the vestibular cortex during visual object tracking. SIGNIFICANCE STATEMENT: In this study we investigate cross-modal attention effects in the human vestibular cortex. We applied the visual multiple-object tracking task because it is known to evoke attentional load effects on neural activity in visual motion-processing and attention-processing areas. Here we demonstrate a load-dependent effect of attention on the activation in the vestibular cortex, despite constant visual motion stimulation. We find that activity in the parietoinsular vestibular cortex is more strongly suppressed the greater the attentional load on the visual tracking task. These findings suggest cross-modal attentional modulation in the vestibular cortex.

Pretraining Cortical Thickness Predicts Subsequent Perceptual Learning Rate in a Visual Search Task.

We report that preexisting individual differences in the cortical thickness of brain areas involved in a perceptual learning task predict the subsequent perceptual learning rate. Participants trained in a motion-discrimination task involving visual search for a "V"-shaped target motion trajectory among inverted "V"-shaped distractor trajectories. Motion-sensitive area MT+ (V5) was functionally identified as critical to the task: after 3 weeks of training, activity increased in MT+ during task performance, as measured by functional magnetic resonance imaging. We computed the cortical thickness of MT+ from anatomical magnetic resonance imaging volumes collected before training started, and found that it significantly predicted subsequent perceptual learning rates in the visual search task. Participants with thicker neocortex in MT+ before training learned faster than those with thinner neocortex in that area. A similar association between cortical thickness and training success was also found in posterior parietal cortex (PPC).

Information Processing in the Mental Workspace Is Fundamentally Distributed.

The brain is a complex, interconnected information processing network. In humans, this network supports a mental workspace that enables high-level abilities such as scientific and artistic creativity. Do the component processes underlying these abilities occur in discrete anatomical modules, or are they distributed widely throughout the brain? How does the flow of information within this network support specific cognitive functions? Current approaches have limited ability to answer such questions. Here, we report novel multivariate methods to analyze information flow within the mental workspace during visual imagery manipulation. We find that mental imagery entails distributed information flow and shared representations throughout the cortex. These findings challenge existing, anatomically modular models of the neural basis of higher-order mental functions, suggesting that such processes may occur at least in part at a fundamentally distributed level of organization. The novel methods we report may be useful in studying other similarly complex, high-level informational processes.

Fundamentally Distributed Information Processing Integrates the Motor Network into the Mental Workspace during Mental Rotation.

The manipulation of mental representations in the human brain appears to share similarities with the physical manipulation of real-world objects. In particular, some neuroimaging studies have found increased activity in motor regions during mental rotation, suggesting that mental and physical operations may involve overlapping neural populations. Does the motor network contribute information processing to mental rotation? If so, does it play a similar computational role in both mental and manual rotation, and how does it communicate with the wider network of areas involved in the mental workspace? Here we used multivariate methods and fMRI to study 24 participants as they mentally rotated 3-D objects or manually rotated their hands in one of four directions. We find that information processing related to mental rotations is distributed widely among many cortical and subcortical regions, that the motor network becomes tightly integrated into a wider mental workspace network during mental rotation, and that motor network activity during mental rotation only partially resembles that involved in manual rotation. Additionally, these findings provide evidence that the mental workspace is organized as a distributed core network that dynamically recruits specialized subnetworks for specific tasks as needed.

Neural correlates of context-dependent feature conjunction learning in visual search tasks.

Many perceptual learning experiments show that repeated exposure to a basic visual feature such as a specific orientation or spatial frequency can modify perception of that feature, and that those perceptual changes are associated with changes in neural tuning early in visual processing. Such perceptual learning effects thus exert a bottom-up influence on subsequent stimulus processing, independent of task-demands or endogenous influences (e.g., volitional attention). However, it is unclear whether such bottom-up changes in perception can occur as more complex stimuli such as conjunctions of visual features are learned. It is not known whether changes in the efficiency with which people learn to process feature conjunctions in a task (e.g., visual search) reflect true bottom-up perceptual learning versus top-down, task-related learning (e.g., learning better control of endogenous attention). Here we show that feature conjunction learning in visual search leads to bottom-up changes in stimulus processing. First, using fMRI, we demonstrate that conjunction learning in visual search has a distinct neural signature: an increase in target-evoked activity relative to distractor-evoked activity (i.e., a relative increase in target salience). Second, we demonstrate that after learning, this neural signature is still evident even when participants passively view learned stimuli while performing an unrelated, attention-demanding task. This suggests that conjunction learning results in altered bottom-up perceptual processing of the learned conjunction stimuli (i.e., a perceptual change independent of the task). We further show that the acquired change in target-evoked activity is contextually dependent on the presence of distractors, suggesting that search array Gestalts are learned. Hum Brain Mapp 37:2319-2330, 2016. © 2016 Wiley Periodicals, Inc.

Extrastriate Visual Areas Integrate Form Features over Space and Time to Construct Representations of Stationary and Rigidly Rotating Objects.

When an object moves behind a bush, for example, its visible fragments are revealed at different times and locations across the visual field. Nonetheless, a whole moving object is perceived. Unlike traditional modal and amodal completion mechanisms known to support spatial form integration when all parts of a stimulus are simultaneously visible, relatively little is known about the neural substrates of the spatiotemporal form integration (STFI) processes involved in generating coherent object representations from a succession visible fragments. We used fMRI to identify brain regions involved in two mechanisms supporting the representation of stationary and rigidly rotating objects whose form features are shown in succession: STFI and position updating. STFI allows past and present form cues to be integrated over space and time into a coherent object even when the object is not visible in any given frame. STFI can occur whether or not the object is moving. Position updating allows us to perceive a moving object, whether rigidly rotating or translating, even when its form features are revealed at different times and locations in space. Our results suggest that STFI is mediated by visual regions beyond V1 and V2. Moreover, although widespread cortical activation has been observed for other motion percepts derived solely from form-based analyses [Tse, P. U. Neural correlates of transformational apparent motion. Neuroimage, 31, 766-773, 2006; Krekelberg, B., Vatakis, A., & Kourtzi, Z. Implied motion from form in the human visual cortex. Journal of Neurophysiology, 94, 4373-4386, 2005], increased responses for the position updating that lead to rigidly rotating object representations were only observed in visual areas KO and possibly hMT+, indicating that this is a distinct and highly specialized type of processing.

Caudate nucleus reactivity predicts perceptual learning rate for visual feature conjunctions.

Useful information in the visual environment is often contained in specific conjunctions of visual features (e.g., color and shape). The ability to quickly and accurately process such conjunctions can be learned. However, the neural mechanisms responsible for such learning remain largely unknown. It has been suggested that some forms of visual learning might involve the dopaminergic neuromodulatory system (Roelfsema et al., 2010; Seitz and Watanabe, 2005), but this hypothesis has not yet been directly tested. Here we test the hypothesis that learning visual feature conjunctions involves the dopaminergic system, using functional neuroimaging, genetic assays, and behavioral testing techniques. We use a correlative approach to evaluate potential associations between individual differences in visual feature conjunction learning rate and individual differences in dopaminergic function as indexed by neuroimaging and genetic markers. We find a significant correlation between activity in the caudate nucleus (a component of the dopaminergic system connected to visual areas of the brain) and visual feature conjunction learning rate. Specifically, individuals who showed a larger difference in activity between positive and negative feedback on an unrelated cognitive task, indicative of a more reactive dopaminergic system, learned visual feature conjunctions more quickly than those who showed a smaller activity difference. This finding supports the hypothesis that the dopaminergic system is involved in visual learning, and suggests that visual feature conjunction learning could be closely related to associative learning. However, no significant, reliable correlations were found between feature conjunction learning and genotype or dopaminergic activity in any other regions of interest.

The artist emerges: visual art learning alters neural structure and function.

How does the brain mediate visual artistic creativity? Here we studied behavioral and neural changes in drawing and painting students compared to students who did not study art. We investigated three aspects of cognition vital to many visual artists: creative cognition, perception, and perception-to-action. We found that the art students became more creative via the reorganization of prefrontal white matter but did not find any significant changes in perceptual ability or related neural activity in the art students relative to the control group. Moreover, the art students improved in their ability to sketch human figures from observation, and multivariate patterns of cortical and cerebellar activity evoked by this drawing task became increasingly separable between art and non-art students. Our findings suggest that the emergence of visual artistic skills is supported by plasticity in neural pathways that enable creative cognition and mediate perceptuomotor integration.

Neural mechanisms of feature conjunction learning: enduring changes in occipital cortex after a week of training.

Most visual activities, whether reading, driving, or playing video games, require rapid detection and identification of learned patterns defined by arbitrary conjunctions of visual features. Initially, such detection is slow and inefficient, but it can become fast and efficient with training. To determine how the brain learns to process conjunctions of visual features efficiently, we trained participants over eight consecutive days to search for a target defined by an arbitrary conjunction of color and location among distractors with a different conjunction of the same features. During each training session, we measured brain activity with functional magnetic resonance imaging (fMRI). The speed of visual search for feature conjunctions improved dramatically within just a few days. These behavioral improvements were correlated with increased neural responses to the stimuli in visual cortex. This suggests that changes in neural processing in visual cortex contribute to the speeding up of visual feature conjunction search. We find evidence that this effect is driven by an increase in the signal-to-noise ratio (SNR) of the BOLD signal for search targets over distractors. In a control condition where target and distractor identities were exchanged after training, learned search efficiency was abolished, suggesting that the primary improvement was perceptual learning for the search stimuli, not task-learning. Moreover, when participants were retested on the original task after nine months without further training, the acquired changes in behavior and brain activity were still present, showing that this can be an enduring form of learning and neural reorganization.