The neural basis of visual skill learning: an fMRI study of mirror reading

The learning of perceptual skills is thought to rely upon multiple regions in the cerebral cortex, but imaging studies have not yet provided evidence about the changes in neural activity that accompany visual skill learning. Functional magnetic resonance imaging (fMRI) was used to examine changes in activation of posterior brain regions associated with the acquisition of mirror-reading skill for novel and practiced stimuli. Multiple regions in the occipital lobe, inferior temporal cortex, superior parietal cortex and cerebellum were involved in the reading of mirror-reversed compared to normally oriented text. For novel stimuli, skilled mirror-reading was associated with decreased activation in the right superior parietal cortex and posterior occipital regions and increased activation in the left inferior temporal lobe. These results suggest that learning to read mirror- reversed text involves a progression from visuospatial transformation to direct recognition of transformed letters. Reading practiced, relative to unpracticed, stimuli was associated with decreased activation in occipital visual cortices, inferior temporal cortex and superior parietal cortex and increased activation in occipito-parietal and lateral temporal regions. By examining skill learning and item- specific repetition priming in the same task, this study demonstrates that both of these forms of learning exhibit shifts in the set of neural structures that contribute to performance.      

Regional specificity of format-specific priming effects in mirror word reading using functional magnetic resonance imaging

The speed and accuracy with which subjects can read words is enhanced or "primed" by a prior presentation of the same words. Moreover, priming effects are generally larger when the physical form of the words is maintained from the first to the second presentation. We investigated the neural basis of format-specific priming in a mirror word-reading task using event-related functional magnetic resonance imaging (fMRI). Participants read words that were presented either in mirror-image (M) orientation or in normal (N) orientation and were repeated either in the same or the alternate orientation, creating 4 study-test conditions, N-N, M-N, N-M, and M-M. Priming of N words resulted in reductions in fMRI signal in multiple brain regions, even though reading times (RTs) were unchanged. Priming of M words showed a pattern of RTs consistent with format-specific priming, with greater reductions when the prime matched the form of the test word. Priming-related reductions in fMRI activity were evident in all regions involved in mirror-image reading, regardless of the orientation of the prime. Importantly, reductions in several posterior regions, including fusiform, superior parietal, and superior temporal regions were also format specific. That is, signal reductions in these regions were greatest when the visual form of the prime and target matched (M-M compared with N-M). The results indicate that, although there are global neural priming effects due to stimulus repetition, it is also possible to identify regional brain changes that are sensitive to the specific perceptual overlap of primes and targets.     

Repetition suppression and reactivation in auditory-verbal short-term recognition memory

The neural response to stimulus repetition is not uniform across brain regions, stimulus modalities, or task contexts. For instance, it has been observed in many functional magnetic resonance imaging (fMRI) studies that sometimes stimulus repetition leads to a relative reduction in neural activity (repetition suppression), whereas in other cases repetition results in a relative increase in activity (repetition enhancement). In the present study, we hypothesized that in the context of a verbal short-term recognition memory task, repetition-related "increases" should be observed in the same posterior temporal regions that have been previously associated with "persistent activity" in working memory rehearsal paradigms. We used fMRI and a continuous recognition memory paradigm with short lags to examine repetition effects in the posterior and anterior regions of the superior temporal cortex. Results showed that, consistent with our hypothesis, the 2 posterior temporal regions consistently associated with working memory maintenance, also show repetition increases during short-term recognition memory. In contrast, a region in the anterior superior temporal lobe showed repetition suppression effects, consistent with previous research work on perceptual adaptation in the auditory-verbal domain. We interpret these results in light of recent theories of the functional specialization along the anterior and posterior axes of the superior temporal lobe.     

Neural basis for priming of pop-out during visual search revealed with fMRI

Maljkovic and Nakayama first showed that visual search efficiency can be influenced by priming effects. Even "pop-out" targets (defined by unique color) are judged quicker if they appear at the same location and/or in the same color as on the preceding trial, in an unpredictable sequence. Here, we studied the potential neural correlates of such priming in human visual search using functional magnetic resonance imaging (fMRI). We found that repeating either the location or the color of a singleton target led to repetition suppression of blood oxygen level-dependent (BOLD) activity in brain regions traditionally linked with attentional control, including bilateral intraparietal sulci. This indicates that the attention system of the human brain can be "primed," in apparent analogy to repetition-suppression effects on activity in other neural systems. For repetition of target color but not location, we also found repetition suppression in inferior temporal areas that may be associated with color processing, whereas repetition of target location led to greater reduction of activation in contralateral inferior parietal and frontal areas, relative to color repetition. The frontal eye fields were also implicated, notably when both target properties (color and location) were repeated together, which also led to further BOLD decreases in anterior fusiform cortex not seen when either property was repeated alone. These findings reveal the neural correlates for priming of pop-out search, including commonalities, differences, and interactions between location and color repetition. fMRI repetition-suppression effects may arise in components of the attention network because these settle into a stable "attractor state" more readily when the same target property is repeated than when a different attentional state is required.     

White-matter connectivity between face-responsive regions in the human brain

Face recognition is of major social importance and involves highly selective brain regions thought to be organized in a distributed functional network. However, the exact architecture of interconnections between these regions remains unknown. We used functional magnetic resonance imaging to identify face-responsive regions in 22 participants and then employed diffusion tensor imaging with probabilistic tractography to establish the white-matter pathways between these functionally defined regions. We identified strong white-matter connections between the occipital face area (OFA) and fusiform face area (FFA), with a significant right-hemisphere predominance. We found no evidence for direct anatomical connections between FFA and superior temporal sulcus (STS) or between OFA and STS, contrary to predictions based on current cognitive models. Instead, our findings point to segregated processing along a ventral extrastriate visual pathway to OFA-FFA and another more dorsal system connected to STS and frontoparietal areas. In addition, early occipital areas were found to have direct connections to the amygdala, which might underlie a rapid recruitment of limbic brain areas by visual inputs bypassing more elaborate extrastriate cortical processing. These results unveil the structural neural architecture of the human face recognition system and provide new insights on how distributed face-responsive areas may work together.     

Electrophysiological and haemodynamic correlates of face perception,recognition and priming

Face perception, recognition and priming were examined with event-related functional magnetic resonance imaging (fMRI) and scalp event-related potentials (ERPs). Face perception was associated with haemodynamic increases in regions including bilateral fusiform and right superior temporal cortices, and a right posterior negativity (N170), most likely generated in the superior temporal region. Face recognition was associated with haemodynamic increases in fusiform, medial frontal and orbitofrontal cortices, and with a frontocentral positivity from 550 ms poststimulus. Face repetition was associated with a positivity from 400 to 600 ms and behavioural priming. Repetition of familiar faces was also associated with earlier onset of the ERP familiarity effect, and haemodynamic decreases in fusiform cortex. These data support a multi-component model of face-processing, with priming arising from more than one stage.     

The sightless view: neural correlates of occluded objects

The relationship between neural activity and object perception has received considerable attention using stimulus manipulations such as masking or dichoptic presentation. Here we investigate the same problem by occluding objects with an opaque screen that acts to dissociate the direct perception of the object from the awareness of its presence. We used functional magnetic resonance imaging to measure brain activity when subjects viewed objects (faces and houses) that underwent occlusion and found that the response of the majority of the fusiform face area (FFA) and lateral occipital cortex is the same whether the object is visible or occluded. This suggests that when objects are directly viewed, activity within object-selective regions may reflect the awareness of presence, not the direct perception, of the object. Additionally, we identify a region of premotor cortex that is selectively activated by occlusion of either object type, suggesting its generic involvement with processing occluded objects.     

Cerebral bases of subliminal and supraliminal priming during reading

Several studies have investigated the neural correlates of conscious perception by contrasting functional magnetic resonance imaging (fMRI) activation to conscious and nonconscious visual stimuli. The results often reveal an amplification of posterior occipito-temporal activation and its extension into a parieto-frontal network. However, some of these effects might be due to a greater deployment of attentional or strategical processes in the conscious condition. Here, we examined the brain activity evoked by visible and invisible stimuli, both of which were irrelevant to the task. We collected fMRI data in a masking paradigm in which subliminal versus supraliminal letter strings were presented as primes while subjects focused attention on another subsequent, highly visible target word. Under those conditions, prime visibility was associated with greater activity confined to bilateral posterior occipito-temporal cortices, without extension into frontal and parietal cortices. However, supraliminal primes, compared with subliminal primes, evoked more extensive repetition suppression in a widely distributed set of parieto-frontal areas. Furthermore, only supraliminal primes caused phonological repetition enhancement in left inferior frontal and anterior insular cortex. Those results suggest a 2-stage view of conscious access: Relative to masked stimuli, unmasked stimuli elicit increased occipito-temporal activity, thus allowing them to compete for global conscious access and to induce priming in multiple distant areas. In the absence of attention, however, their access to a second stage of distributed parieto-frontal processing may remain blocked.     

Familiarity and conceptual priming engage distinct cortical networks

Familiarity refers to an explicit recognition experience without any necessary retrieval of specific detail related to the episode during which initial learning transpired. Prior experience can also implicitly influence subsequent processing through a memory phenomenon termed conceptual priming, which occurs without explicit awareness of recognition. Resolving current theoretical controversy on relationships between familiarity and conceptual priming requires a clarification of their neural substrates. Accordingly, we obtained functional magnetic resonance images in a novel paradigm for separately assessing neural correlates of familiarity and conceptual priming using famous and nonfamous faces. Conceptual priming, as shown by more accurate behavioral responses to strongly conceptually primed than to weakly conceptually primed faces, was associated with activity reductions in left prefrontal cortex, whereas familiarity was associated with activity enhancements in right parietal cortex for more-familiar compared with less-familiar faces. This neuroimaging evidence implicates separate neurocognitive processes operative in explicit stimulus recognition versus implicit conceptual priming.     

Similar frontal and distinct posterior cortical regions mediate visual and auditory perceptual awareness

Activity in ventral visual cortex is a consistent neural correlate of visual consciousness. However, activity in this area seems insufficient to produce awareness without additional involvement of frontoparietal regions. To test the generality of the frontoparietal response, neural correlates of auditory awareness were investigated in a paradigm that previously has revealed frontoparietal activity during conscious visual perception. A within-experiment comparison showed that frontal regions were related to both visual and auditory awareness, whereas parietal activity was correlated with visual awareness and superior temporal activity with auditory awareness. These results indicate that frontal regions interact with specific posterior regions to produce awareness in different sensory modalities.     

Decoding near-threshold perception of fear from distributed single-trial brain activation

Instead of contrasting functional magnetic resonance imaging (fMRI) signals associated with 2 conditions, as customarily done in neuroimaging, we reversed the direction of analysis and probed whether brain signals could be used to "predict" perceptual states. We probed the neural correlates of perceptual decisions by "decoding" brain states during near-threshold fear detection. Decoding was attempted by using support vector machines and other related techniques. Although previous decoding studies have employed relatively "blocked" data, our objective was to probe how the "moment-to-moment" fluctuation in fMRI signals across a population of voxels reflected the participant's perceptual decision. Accuracy increased from when 1 region was considered (approximately 64%) to when 10 regions were used (approximately 78%). When the best classifications per subject were averaged, accuracy levels ranged between 74% and 86% correct. An information theoretic analysis revealed that the information carried by pairs of regions reliably exceeded the sum of the information carried by individual regions, suggesting that information was combined "synergistically" across regions. Our results indicate that the representation of behavioral choice is "distributed" across several brain regions. Such distributed encoding may help prepare the organism to appropriately handle emotional stimuli and regulate the associated emotional response upon the conscious decision that a fearful face is present. In addition, the results show that challenging brain states can be decoded with high accuracy even when "single-trial" data are employed and suggest that multivariate analysis strategies have considerable potential in helping to elucidate the neural correlates of visual awareness and the encoding of perceptual decisions.     

Convergence of neural systems processing stimulus associations and coordinating motor responses

A sensory-sensory learning paradigm was used to measure neural changes in humans during acquisition of an association between an auditory and visual stimulus. Three multivariate partial least-squares (PLS) analyses of positron emission tomography data identified distributed neural systems related to (i) processing the significance of the auditory stimulus, (ii) mediating the acquisition of the behavioral response, and (iii) the spatial overlap between these two systems. The system that processed the significance of the tone engaged primarily right hemisphere regions and included dorsolateral prefrontal cortex, putamen, and inferior parietal and temporal cortices. Activity changes in left occipital cortex were also identified, most likely reflecting the learned expectancy of the upcoming visual event. The system related to behavior was similar to that which coded the significance of the tone, including dorsal occipital cortex. The PLS analysis of the concordance between these two systems showed substantial regional overlap, and included occipital, dorsolateral prefrontal, and limbic cortices. However, activity in dorsomedial prefrontal cortex was strictly related to processing the auditory stimulus and not to behavior. Taken together, the PLS analyses identified a system that contained a sensory-motor component (comprised of occipital, temporal association and sensorimotor cortices) and a medial prefrontallimbic component, that as a group simultaneously embodied the learning-related response to the stimuli and the subsequent change in behavior.      

Differential contributions of prefrontal, medial temporal, and sensory-perceptual regions to true and false memory formation

The neural correlates of true memory formation (TMF) and false memory formation (FMF) were investigated using functional magnetic resonance imaging (fMRI). Using a parametric subsequent memory paradigm, encoding activity was analyzed as a function of whether it predicted subsequent hits to targets (TMF activity) or subsequent false alarms to critical lures (FMF activity). The fMRI analyses yielded 3 main findings. First, the left prefrontal cortex (PFC) was involved in both TMF and FMF activities. This finding is consistent with the evidence that semantic elaboration, which has been associated with left PFC, tends to enhance both true and false remembering. Second, the left posterior medial temporal lobes (MTLs) contributed to TMF but not to FMF activity. This finding is consistent with the notion that MTL is involved in the storage of a consciously, but not unconsciously, processed event. Third, late visual regions were engaged in both TMF and FMF activities, whereas early visual areas were involved primarily in TMF activity. This dissociation indicates that elaborative perceptual processing, but not basic sensory processing, contributes to false remembering. Taken together, the results suggest that FMF is an unintended consequence, or by-product, of elaborative semantic and visual encoding processes.     

Evidence for separate perceptual reactivation and search processes during remembering

Remembering involves the coordinated recruitment of strategic search processes and processes involved in reconstructing the content of the past experience. In the present study we used a cueing paradigm based on event-related functional magnetic resonance imaging to separate activity in the initial preparation phases of retrieval from later phases during which retrieval search ensued, and detailed auditory and visual memories were reconstructed. Results suggest a dissociation among inferior temporal (IT) and parieto-occipital (PO) processing regions in how they were influenced by preparatory cues prior to remembering, and indicate a dissociation in how they were influenced by the subsequent validity of those cues during remembering. Regions in IT cortex appeared to show search-related activity during retrieval, as well as robust modality effects, but they were not influenced by preparatory cues. These findings suggest a specific role for IT regions in reconstruction of visual details during remembering. While dorsal regions in parietal and superior occipital cortex also appeared to show search-related activity as well as robust modality effects, they were also influenced by preparatory cues during the retrieval phase, and to a lesser degree during the cue phase. These findings indicate a role in integrating perceptual reactivation and search processes during remembering.     

The neural correlates of conscious vision

Conflicting accounts of the neurobiology of consciousness have emerged from previous imaging studies. Some studies suggest that visual consciousness relates to a distributed network of frontal and partietal regions while others point to localized activity within individual visual areas. While the two positions seem mutually exclusive, timing issues may help reconcile the two. Networks that appear unified in functional magnetic resonance imaging (fMRI) studies may reflect processes that are widely distributed in time. To help resolve this issue, we have investigated timing across a network correlating with consciousness in parallel fMRI and evoked potential (EP) studies of grating stimuli. At threshold, a stimulus is perceived on some occasions but not on others, dissociating sensory input and perception. We have found correlates of consciousness in the occipital lobe at 100 ms and in parietal, frontal, auditory and motor regions from 260 ms onwards. The broad temporal and spatial distribution of activity argues against a unified, distributed fronto-parietal correlate of consciousness. Instead, it suggests that correlates of consciousness are divided into primary and secondary network nodes, with early activity in the occipital lobe correlating with perception and later activity in downstream areas with secondary processes contingent on the outcome of earlier perceptual processing.     

Task-dependency of the neural correlates of episodic encoding as measured by fMRI.

Using event-related functional magnetic resonance imaging (fMRI), the neural correlates of memory encoding can be studied by contrasting item-related activity elicited in a study task according to whether the items are remembered or forgotten in a subsequent memory test. Previous studies using this approach have implicated the left prefrontal cortex in the successful encoding of verbal material into episodic memory when the study task is semantic in nature. In the current study, we asked whether the neural correlates of episodic encoding differ depending on type of study task. Seventeen volunteers participated in an event-related fMRI experiment in which at study, volunteers were cued to make either animacy or syllable judgements about words. A recognition memory test followed after a delay of approximately 15 min. For the animacy task, words that were subsequently remembered showed greater activation in left and medial prefrontal regions. For the syllable task, by contrast, successful memory for words was associated with activations in bilateral intraparietal sulcus, bilateral fusiform gyrus, right prefrontal cortex and left superior occipital gyrus. These findings suggest that the brain networks supporting episodic encoding differ according to study task.     

Retinotopic organization in human visual cortex and the spatial precision of functional MRI

A method of using functional magnetic resonance imaging (fMRI) to measure retinotopic organization within human cortex is described. The method is based on a visual stimulus that creates a traveling wave of neural activity within retinotopically organized visual areas. We measured the fMRI signal caused by this stimulus in visual cortex and represented the results on images of the flattened cortical sheet. We used the method to locate visual areas and to evaluate the spatial precision of fMRI. Specifically, we: (i) identified the borders between several retinotopically organized visual areas in the posterior occipital lobe; (ii) measured the function relating cortical position to visual field eccentricity within area V1; (iii) localized activity to within 1.1 mm of visual cortex; and (iv) estimated the spatial resolution of the fMRI signal and found that signal amplitude falls to 60% at a spatial frequency of 1 cycle per 9 mm of visual cortex. This spatial resolution is consistent with a linespread whose full width at half maximum spreads across 3.5 mm of visual cortex.      

Enhanced motion sensitivity follows saccadic suppression in the superior temporal sulcus of the macaque cortex

The responses of neurons in the middle temporal and medial superior temporal areas of macaque cortex are suppressed during saccades compared with saccade-like stimulus movements. We utilized the short-latency ocular following paradigm to show that this saccadic suppression is followed by postsaccadic enhancement of motion responses. The level of enhancement decays with a time constant of 100 ms from saccade end. The speed of ocular following is also enhanced after saccades and decays over a similar time course, suggesting a link between the neural and behavioral effects. There is some evidence that maximum postsaccadic enhancement occurs when cells are stimulated at their optimum speeds. Latencies of motion responses are saccade dependent: 37 ms for saccade-generated motion, 45 ms for motion in the half-second after saccades, and 70 ms with no prior saccades. The finding that saccades alter response latencies may partially explain perceptual time compression during saccades and time dilation after saccades.     

On the functional relevance of frontal cortex for passive and voluntarily controlled bistable vision

In bistable vision, one constant ambiguous stimulus leads to 2 alternating conscious percepts. This perceptual switching occurs spontaneously but can also be influenced through voluntary control. Neuroimaging studies have reported that frontal regions are activated during spontaneous perceptual switches, leading some researchers to suggest that frontal regions causally induce perceptual switches. But the opposite also seems possible: frontal activations may themselves be caused by spontaneous switches. Classically implicated in attentional processes, these same regions are also candidates for the origins of voluntary control over bistable vision. Here too, it remains unknown whether frontal cortex is actually functionally relevant. It is even possible that spontaneous perceptual switches and voluntarily induced switches are mediated by the same top-down mechanisms. To directly address these issues, we here induced "virtual lesions," with transcranial magnetic stimulation, in frontal, parietal, and 2 lower level visual cortices using an established ambiguous structure-from-motion stimulus. We found that dorsolateral prefrontal cortex was causally relevant for voluntary control over perceptual switches. In contrast, we failed to find any evidence for an active role of frontal cortex in passive bistable vision. Thus, it seems the same pathway used for willed top-down modulation of bistable vision is not used during passive bistable viewing.     

Impaired face discrimination in acquired prosopagnosia is associated with abnormal response to individual faces in the right middle fusiform gyrus

The middle fusiform gyrus (MFG) and the inferior occipital gyrus (IOG) are activated by both detection and identification of faces. Paradoxically, patients with acquired prosopagnosia following lesions to either of these regions in the right hemisphere cannot identify faces, but can still detect faces. Here we acquired functional magnetic resonance imaging (fMRI) data during face processing in a patient presenting a specific deficit in individual face recognition, following lesions encompassing the right IOG. Using an adaptation paradigm we show that the fMRI signal in the rMFG of the patient, while being larger in response to faces as compared to objects, does not differ between conditions presenting identical and distinct faces, in contrast to the larger response to distinct faces observed in controls. These results suggest that individual discrimination of faces critically depends on the integrity of both the rMFG and the rIOG, which may interact through re-entrant cortical connections in the normal brain.