Visual Brain Areas Research Articles

Acetylcholine Mediates Behavioral and Neural Post-Error Control

Humans often commit errors when they are distracted by irrelevant information and no longer focus on what is relevant to the task at hand. Adjustments following errors are essential for optimizing goal achievement. The posterior medial frontal cortex (pMFC), a key area for monitoring errors, has been shown to trigger such post-error adjustments by modulating activity in visual cortical areas. However, the mechanisms by which pMFC controls sensory cortices are unknown. Weprovide evidence for a mechanism based on pMFC-induced recruitment of cholinergic projections to task-relevant sensory areas. Using fMRI in healthy volunteers, we found that error-related pMFC activity predicted subsequent adjustments in task-relevant visual brain areas. In particular, following an error, activity increased in those visual cortical areas involved in processing task-relevant stimulus features, whereas activity decreased in areas representing irrelevant, distracting features. Following treatment with the muscarinic acetylcholine receptor antagonist biperiden, activity in visual areas was no longer under control of error-related pMFC activity. This was paralleled by abolished post-error behavioral adjustments under biperiden. Our results reveal a prominent role of acetylcholinein cognitive control that has not been recognized thus far. Regaining optimal performance after errors critically depends on top-down control of perception driven by the pMFC and mediated by acetylcholine. This may explain the lack of adaptivity in conditions with reduced availability of cortical acetylcholine, such as Alzheimer's disease.

Dissociating visual and motor directional selectivity using visuomotor adaptation.

Directional selectivity during visually guided hand movements is a fundamental characteristic of neural populations in multiple motor areas of the primate brain. In the current study, we assessed how directional selectivity changes when reaching movements are dissociated from their visual feedback by rotating the visual field. We recorded simultaneous movement kinematics and fMRI activity while human subjects performed out-and-back movements to four peripheral targets before and after adaptation to a 45° visuomotor rotation. A classification algorithm was trained to identify movement direction according to voxel-by-voxel fMRI patterns in each of several brain areas. The direction of movements was successfully decoded with above-chance accuracy in multiple motor and visual areas when training and testing the classifier on trials within each condition, thereby demonstrating the existence of directionally selective fMRI patterns within each stage of the experiment. Most importantly, when training the classifier on baseline trials and decoding rotated trials, motor brain areas exhibited above-chance decoding according to the original movement direction and visual brain areas exhibited above-chance decoding according to the rotated visual target location, while posterior parietal cortex (PPC) exhibited chance-level decoding according to both. These results reveal that directionally selective fMRI patterns in motor system areas faithfully represent movement direction regardless of visual feedback, while fMRI patterns in visual system areas faithfully represent target location regardless of movement direction. Directionally selective fMRI patterns in PPC, however, were altered following adaptation learning, thereby suggesting that the novel visuomotor mapping, which was learned during visuomotor adaptation, is stored in PPC.

Redundancy reduction explains the expansion of visual direction space around the cardinal axes

Motion direction discrimination in humans is worse for oblique directions than for the cardinal directions (the oblique effect). For some unknown reason, the human visual system makes systematic errors in the estimation of particular motion directions; a direction displacement near a cardinal axis appears larger than it really is whereas the same displacement near an oblique axis appears to be smaller. Although the perceptual effects are robust and are clearly measurable in smooth pursuit eye movements, all attempts to identify the neural underpinnings for the oblique effect have failed. Here we show that a model of image velocity estimation based on the known properties of neurons in primary visual cortex (V1) and the middle temporal (MT) visual area of the primate brain produces the oblique effect. We also provide an explanation for the unusual asymmetric patterns of inhibition that have been found surrounding MT neurons. These patterns are consistent with a mechanism within the visual system that prevents redundant velocity signals from being passed onto the next motion-integration stage, (dorsal Medial superior temporal, MSTd). We show that model redundancy-reduction mechanisms within the MT-MSTd pathway produce the oblique effect.

Visual and Motor Cortices Differentially Support the Translation of Foreign Language Words

At present, it is largely unclear how the human brain optimally learns foreign languages. We investigated teaching strategies that utilize complementary information ("enrichment"), such as pictures or gestures, to optimize vocabulary learning outcome. We found that learning while performing gestures was more efficient than the common practice of learning with pictures and that both enrichment strategies were better than learning without enrichment ("verbal learning"). We tested the prediction of an influential cognitive neuroscience theory that provides explanations for the beneficial behavioral effects of enrichment: the "multisensory learning theory" attributes the benefits of enrichment to recruitment of brain areas specialized in processing the enrichment. To test this prediction, we asked participants to translate auditorily presented foreign words during fMRI. Multivariate pattern classification allowed us to decode from the brain activity under which enrichment condition the vocabulary had been learned. The visual-object-sensitive lateral occipital complex (LOC) represented auditory words that had been learned with pictures. The biological motion superior temporal sulcus (bmSTS) and motor areas represented auditory words that had been learned with gestures. Importantly, brain activity in these specialized visual and motor brain areas correlated with behavioral performance. The cortical activation pattern found in the present study strongly supports the multisensory learning theory in contrast to alternative explanations. In addition, the results highlight the importance of learning foreign language vocabulary with enrichment, particularly with self-performed gestures.

Autobiographical recall triggers visual exploration

Autobiographical recall is thought to rely on the ability to generate a visual image of the remembered event. Neuropsychological studies suggest a relationship between deterioration in visual mental imagery and autobiographical distortions, while neuroimaging data similarly implicate visual brain areas in autobiographical recall. However, neither whether autobiographical retrieval is associated with visual exploration, or not. Our paper aimed to provide such evidence one way or the other. Using an eye tracking system, we recorded eye movements of 40 participants during autobiographical recall and during a control condition in which participants had to count aloud. In both conditions, the participants had to look at a blank screen while their gaze location was recorded by the eye-tracker. Autobiographical recall triggered a lower number of fixations and reduced their duration. In contrast, the number, duration, and amplitude of saccades increased compared to the control condition. Our data suggest that autobiographical recall is characterized by visual processing.

Functional reorganization of the visual dorsal stream as probed by 3-D visual coherence in Williams syndrome.

Object and depth perception from motion cues involves the recruitment of visual dorsal stream brain areas. In 3-D structure-from-motion (SFM) perception, motion and depth information are first extracted in this visual stream to allow object categorization, which is in turn mediated by the ventral visual stream. Such interplay justifies the use of SFM paradigms to understand dorsal-ventral integration of visual information. The nature of such processing is particularly interesting to be investigated in a neurological model of cognitive dissociation between dorsal (impaired) and ventral stream (relatively preserved) processing, Williams syndrome (WS). In the current fMRI study, we assessed dorsal versus ventral stream processing by using a performance-matched 3-D SFM object categorization task. We found evidence for substantial reorganization of the dorsal stream in WS as assessed by whole-brain ANOVA random effects analysis, with subtle differences in ventral activation. Dorsal reorganization was expressed by larger medial recruitment in WS (cuneus, precuneus, and retrosplenial cortex) in contrast with controls, which showed the expected dorsolateral pattern (caudal intraparietal sulcus and lateral occipital cortex). In summary, we found a substantial reorganization of dorsal stream regions in WS in response to simple visual categories and 3-D SFM perception, with less affected ventral stream. Our results corroborate the existence of a medial dorsal pathway that provides the substrate for information rerouting and reorganization in the presence of lateral dorsal stream vulnerability. This interpretation is consistent with recent findings suggesting parallel routing of information in medial and lateral parts of dorsal stream.

Altered Brain Structure and Function Correlate with Disease Severity and Pain Catastrophizing in Migraine Patients.

To investigate the neuroanatomical and functional brain changes in migraine patients relative to healthy controls, we used a combined analytical approach including voxel- and surface-based morphometry along with resting-state functional connectivity to determine whether areas showing structural alterations in patients also showed abnormal functional connectivity. Additionally, we wanted to assess whether these structural and functional changes were associated with group differences in pain catastrophizing and migraine-related disease variables in patients. We acquired T1-weighted anatomical and functional magnetic resonance imaging scans during rest in human subjects with a diagnosis of migraine and healthy controls. Structural analyses revealed greater left hippocampal gray matter volume and reduced cortical thickness in the left anterior midcingulate in patients compared with controls. We also observed negative associations between pain catastrophizing and migraine disease variables and gray matter in areas implicated in processing the sensory, affective, and cognitive aspects of pain in patients. Functional connectivity analyses showed that migraine patients displayed disrupted connectivity between default mode, salience, cognitive, visuospatial, and sensorimotor networks, which was associated with group differences in pain catastrophizing and migraine-related disease variables in patients. Together, our findings show widespread morphological and functional brain abnormalities in migraineurs in affective, cognitive, visual, and pain-related brain areas, which are associated with increased pain catastrophizing, disease chronicity, and severity of symptoms, suggesting that these structural and functional changes may be a consequence of repeated, long-term nociceptive signaling leading to increased pain sensitivity, mood disturbances, and maladaptive coping strategies to deal with unrelenting pain.

Effective connectivity during visual processing is affected by emotional state.

The limitations of our cognitive resources necessitate the selection of relevant information from the incoming visual stream. This selection and prioritizing of stimuli allows the organism to adapt to the current conditions. However, the characteristics of this process vary with time and depend on numerous external and internal factors. The present study was aimed at determining how the emotional state affects effective connectivity between visual, attentional and control brain areas during the perception of affective visual stimuli. The Directed Transfer Function was applied on a 32-electrode EEG recording to quantify the direction and intensity of the information flow during two sessions: positive and negative. These data were correlated with a self-report of the emotional state. We demonstrated that the current mood, as measured by self-report, is a factor which affects the patterns of effective cortical connectivity. An increase in prefrontal top-down control over the visual and attentional areas was revealed in a state of tension. It was accompanied by increased outflow within and from the areas recognized as the ventral attentional network. By contrast, a positive emotional state was associated with heightened flow from the parietal to the occipital area. The functional significance of the revealed effects is discussed.

Prolonged fasting impairs neural reactivity to visual stimulation

Previous literature has shown that hypoglycemia influences the intensity of the BOLD signal. A similar but smaller effect may also be elicited by low normal blood glucose levels in healthy individuals. This may not only confound the BOLD signal measured in fMRI, but also more generally interact with cognitive processing, and thus indirectly influence fMRI results. Here we show in a placebo-controlled, crossover, double-blind study on 40 healthy subjects, that overnight fasting and low normal levels of glucose contrasted to an activated, elevated glucose condition have an impact on brain activation during basal visual stimulation. Additionally, functional connectivity of the visual cortex shows a strengthened association with higher-order attention-related brain areas in an elevated blood glucose condition compared to the fasting condition. In a fasting state visual brain areas show stronger coupling to the inferior temporal gyrus. Results demonstrate that prolonged overnight fasting leads to a diminished BOLD signal in higher-order occipital processing areas when compared to an elevated blood glucose condition. Additionally, functional connectivity patterns underscore the modulatory influence of fasting on visual brain networks. Patterns of brain activation and functional connectivity associated with a broad range of attentional processes are affected by maturation and aging and associated with psychiatric disease and intoxication. Thus, we conclude that prolonged fasting may decrease fMRI design sensitivity in any task involving attentional processes when fasting status or blood glucose is not controlled.

Silent music reading: Auditory imagery and visuotonal modality transfer in singers and non-singers

In daily life, responses are often facilitated by anticipatory imagery of expected targets which are announced by associated stimuli from different sensory modalities. Silent music reading represents an intriguing case of visuotonal modality transfer in working memory as it induces highly defined auditory imagery on the basis of presented visuospatial information (i.e. musical notes). Using functional MRI and a delayed sequence matching-to-sample paradigm, we compared brain activations during retention intervals (10s) of visual (VV) or tonal (TT) unimodal maintenance versus visuospatial-to-tonal modality transfer (VT) tasks. Visual or tonal sequences were comprised of six elements, white squares or tones, which were low, middle, or high regarding vertical screen position or pitch, respectively (presentation duration: 1.5s). For the cross-modal condition (VT, session 3), the visuospatial elements from condition VV (session 1) were re-defined as low, middle or high “notes” indicating low, middle or high tones from condition TT (session 2), respectively, and subjects had to match tonal sequences (probe) to previously presented note sequences. Tasks alternately had low or high cognitive load. To evaluate possible effects of music reading expertise, 15 singers and 15 non-musicians were included. Scanner task performance was excellent in both groups. Despite identity of applied visuospatial stimuli, visuotonal modality transfer versus visual maintenance (VT>VV) induced “inhibition” of visual brain areas and activation of primary and higher auditory brain areas which exceeded auditory activation elicited by tonal stimulation (VT>TT). This transfer-related visual-to-auditory activation shift occurred in both groups but was more pronounced in experts. Frontoparietal areas were activated by higher cognitive load but not by modality transfer. The auditory brain showed a potential to anticipate expected auditory target stimuli on the basis of non-auditory information and sensory brain activation rather mirrored expectation than stimulation. Silent music reading probably relies on these basic neurocognitive mechanisms.

Frontal theta activity is pronounced during illusory perception

Object perception is driven by sensory information as well as expectations and prior experiences. The latter influence may increase when the sensory information is poor or inconclusive. Visual illusions, for example induced by ambiguous stimuli, provide a tool to investigate perceptual uncertainty, because ambiguous stimuli elicit switching between at least two perceptual alternatives. Theta oscillations may reflect the impact of visual illusion on perception since they are specifically important to coordinate information in large-scale brain networks, including visual sensory as well as higher-order brain areas. Theta responses elicited by an ambiguous and an unambiguous apparent motion-inducing stimulus were compared, thereby differentiating time periods of perceptual switching and perceptual stability (non-switching). The theta responses were larger at anterior than at posterior sites. This gradient was stronger during the ambiguous task than during the unambiguous task, even though sensory stimulation was comparable for both tasks. A transient increase of the theta response occurred during switching time periods for both the ambiguous and the unambiguous tasks, indicating that the theta response related to the perceptual switch might not be affected by the ambiguity of the stimulus. Irrespective of the percept switching or not, ambiguous stimuli elicited an enduring more prominent activation of higher-order rather than visual sensory brain areas. This indicates an increased reliance on expectations and prior information to ensure coherent object perception in particular when the visual information is degraded or elicits an ongoing conflict between perceptual interpretations.

Visual brain areas predict haptic (and visual) behavioral similarities between novel objects

Visual brain areas predict haptic (and visual) behavioral similarities between novel objects

Visual brain areas predict haptic (and visual) behavioral similarities between novel objects

Visual brain areas predict haptic (and visual) behavioral similarities between novel objects

Locally-Optimized Inter-Subject Alignment of Functional Cortical Regions

Inter-subject registration of cortical areas is necessary in functional imaging (fMRI) studies for making inferences about equivalent brain function across a population. However, many high-level visual brain areas are defined as peaks of functional contrasts and it is usually difficult to identify clear anatomical landmarks and boundaries for these areas, due to large variability in their cortical position. As a consequence, previous methods usually fail to accurately map such functional regions of interest (ROIs) across participants. To address this problem, we propose a locally optimized registration method that directly predicts the location of a seed ROI on a separate target cortical sheet by maximizing the functional correlation between regions and simultaneously constraining the global structure of the mapping, while allowing for non-local deformations in its topology. Our registration method outperformed two canonical baselines (anatomical landmark-based AFNI alignment and cortical curvature-based FreeSurfer alignment) in the percentage of overlap between predicted region and ground truth LOC. Furthermore, the maps obtained using our method are more consistent across subjects than both baseline measures. Consequently, our method has the ability to directly and immediately improve the quality of group maps for high-level visual areas in countless fMRI studies. This would dramatically increase the statistical power of such studies, as a more accurate mapping to a common space implies less smoothing and larger effect sizes.

Flexibility in embodied language processing: context effects in lexical access.

According to embodied theories of language (ETLs), word meaning relies on sensorimotor brain areas, generally dedicated to acting and perceiving in the real world. More specifically, words denoting actions are postulated to make use of neural motor areas, while words denoting visual properties draw on the resources of visual brain areas. Therefore, there is a direct correspondence between word meaning and the experience a listener has had with a word's referent on the brain level. Behavioral and neuroimaging studies have provided evidence in favor of ETLs; however, recent studies have also shown that sensorimotor information is recruited in a flexible manner during language comprehension (e.g., Raposo et al.; Van Dam et al.,), leaving open the question as to what level of language processing sensorimotor activations contribute. In this study, we investigated the time course of modality-specific contributions (i.e., the contribution of action information) as to word processing by manipulating both (a) the linguistic and (b) the action context in which target words were presented. Our results demonstrate that processes reflecting sensorimotor information play a role early in word processing (i.e., within 200 ms of word presentation), but that they are sensitive to the linguistic context in which a word is presented. In other words, when sensorimotor information is activated, it is activated quickly; however, specific words do not reliably activate a consistent sensorimotor pattern.

Brain-potential analysis of visual word recognition in dyslexics and typically reading children

The specialization of visual brain areas for fast processing of printed words plays an important role in the acquisition of reading skills. Dysregulation of these areas may be among the deficits underlying developmental dyslexia. The present study examines the specificity of word activation in dyslexic children in 3rd grade by comparing early components of brain potentials elicited by visually presented words vs. strings of meaningless letter-like symbols. Results showed a more pronounced N1 component for words compared to symbols for both groups. The dyslexic group revealed larger left-lateralized, word-specific N1 responses than the typically reading group. Furthermore, positive correlations between N1 amplitudes and reading fluency were found in the dyslexic group. Our results support the notion of N1 as a sensitive index of visual word processing involved in reading fluency.

Cortical processing of object affordances for self and others' action.

The perception of objects does not rely only on visual brain areas, but also involves cortical motor regions. In particular, different parietal and premotor areas host neurons discharging during both object observation and grasping. Most of these cells often show similar visual and motor selectivity for a specific object (or set of objects), suggesting that they might play a crucial role in representing the “potential motor act” afforded by the object. The existence of such a mechanism for the visuomotor transformation of object physical properties in the most appropriate motor plan for interacting with them has been convincingly demonstrated in humans as well. Interestingly, human studies have shown that visually presented objects can automatically trigger the representation of an action provided that they are located within the observer's reaching space (peripersonal space). The “affordance effect” also occurs when the presented object is outside the observer's peripersonal space, but inside the peripersonal space of an observed agent. These findings recently received direct support by single neuron studies in monkey, indicating that space-constrained processing of objects in the ventral premotor cortex might be relevant to represent objects as potential targets for one's own or others' action.

Predictive codes of interoception, emotion, and the self

Interoception is the ability to perceive and integrate physiological signals from within the body. It is closely related to the autonomic system and is a key component in the generation of affective states and abstract representations of the self (Critchley et al., 2004; Ainley and Tsakiris, 2013). Seth proposes a predictive coding (PC) model of interoception that involves a free-energy based explanation of emotion awareness and selfhood. In this model, emotions, and in turn the sense of self, rely on predictions of the causes of interoceptive signals. Within this framework, the interoceptive system minimizes free-energy, or the discrepancy between predictions and interoceptive signals. Free-energy can be minimized either by updating predictions about the causes of the sensory signals (perceptual updating), or by acting to change autonomic states such that bodily states are more predictable (active inference).

Distinct spatio-temporal profiles of beta-oscillations within visual and sensorimotor areas during action recognition as revealed by MEG

The neural correlates of action recognition have been widely studied in visual and sensorimotor areas of the human brain. However, the role of neuronal oscillations involved during the process of action recognition remains unclear. Here, we were interested in how the plausibility of an action modulates neuronal oscillations in visual and sensorimotor areas. Subjects viewed point-light displays (PLDs) of biomechanically plausible and implausible versions of the same actions. Using magnetoencephalography (MEG), we examined dynamic changes of oscillatory activity during these action recognition processes. While both actions elicited oscillatory activity in visual and sensorimotor areas in several frequency bands, a significant difference was confined to the beta-band (∼20 Hz). An increase of power for plausible actions was observed in left temporal, parieto-occipital and sensorimotor areas of the brain, in the beta-band in successive order between 1650 and 2650 msec. These distinct spatio-temporal beta-band profiles suggest that the action recognition process is modulated by the degree of biomechanical plausibility of the action, and that spectral power in the beta-band may provide a functional interaction between visual and sensorimotor areas in humans.

EEG correlates of perceptual reversals in Boring's ambiguous old/young woman stimulus.

Ambiguous figures attract observers because perception alternates between different interpretations while the sensory information stays unchanged. Understanding the underlying processes is difficult because the precise time instant of this endogenous reversal event needs to be known but is difficult to measure. Presenting ambiguous figures discontinuously and using stimulus onset as estimation of the reversal event increased temporal resolution and provided a series of well-confirmed EEG signatures. In the current EEG study we used this 'onset paradigm' for the first time with Boring's old/young woman stimulus. We found an early occipital event-related potential (ERP) correlate of reversals between the perception of the old woman and the perception of the young woman that fits well with previous ERP findings. This component was not followed by the often-reported occipito-parietal Reversal Negativity at 260 ms, but instead by an occipito-temporal N170, that is typically reported with face stimuli. We interpret our results as follows: ambiguity conflicts take place during processing of stimulus elements in early visual areas roughly 130 ms after stimulus onset. The disambiguation of these elements and their assembly to object 'gestalts' result from an interplay between early visual and object-specific brain areas in a temporal window between 130 and 260 ms after stimulus onset. In the particular case of Boring's old/young woman the processes of element disambiguation and gestalt construction are already finished at 170 ms and, thus, 90 ms earlier than in the case of ambiguous geometric figures (eg Necker cube or Schroeder staircase) or of binocular rivalrous gratings.