Attention modulates gamma-band oscillations differently in the human lateral occipital cortex and fusiform gyrus

We studied the existence, localization and attentional modulation of gamma-band oscillatory activity (30-130 Hz) in the human intracranial region. Two areas known to play a key role in visual object processing: the lateral occipital (LO) cortex and the fusiform gyrus. These areas consistently displayed large gamma oscillations during visual stimulus encoding, while other extrastriate areas remained systematically silent, across 14 patients and 291 recording sites scattered throughout extrastriate visual cortex. The lateral extent of the responsive regions was small, in the range of 5 mm. Induced gamma oscillations and evoked potentials were not systematically co-localized. LO and the fusiform gyrus displayed markedly different patterns of attentional modulation. In the fusiform gyrus, attention enhanced stimulus-driven gamma oscillations. In LO, attention increased the baseline level of gamma oscillations during the expectation period preceding the stimulus. Subsequent gamma oscillations produced by attended stimuli were smaller than those produced by unattended, irrelevant stimuli. Attentional modulations of gamma oscillations in LO and the fusiform gyrus were thus very different, both in their time-course (preparatory period and/or stimulus processing) and direction of modulation (increase or decrease). Our results thus suggest that the functional role of gamma oscillations depends on the area in which they occur.     

Linking hemodynamic and electrophysiological measures of brain activity: evidence from functional MRI and intracranial field potentials

We investigated the relation between electrophysiological and hemodynamic measures of brain activity through comparison of intracranially recorded event-related local field potentials (ERPs) and blood-oxygenation level dependent functional magnetic resonance imaging (BOLD fMRI). We manipulated the duration of visual checkerboard stimuli across trials and measured stimulus-duration-related changes in ERP and BOLD activity in three brain regions: peri-calcarine cortex, the fusiform gyrus and lateral temporal-occipital (LTO) cortex. ERPs were recorded from patients who had indwelling subdural electrodes as part of presurgical testing, while BOLD responses were measured in similar brain regions in a second set of subjects. Similar BOLD responses were measured in peri-calcarine and fusiform regions, with both showing monotonic but non-linear increases in hemodynamic amplitude with stimulus duration. In sharp contrast, very different ERP responses were observed in these same regions, such that calcarine electrodes exhibited onset potentials, sustained activity over the course of stimulus duration and prominent offset potentials, while fusiform electrodes only exhibited onset potentials that did not vary with stimulus duration. No duration-related ERP or BOLD changes were observed in LTO. Additional analyses revealed no consistent changes in the EEG spectrum across different brain sites that correlated with duration-related changes in the BOLD response. We conclude that the relation between ERPs and fMRI differs across brain regions.     

An fMRI version of the Farnsworth-Munsell 100-Hue test reveals multiple color-selective areas in human ventral occipitotemporal cortex.

Studies of patients with cerebral achromatopsia have suggested that ventral occipitotemporal cortex is important for color perception. We created a functional magnetic resonance imaging (fMRI) version of a clinical test commonly used to assess achromatopsia, the Farnsworth-Munsell 100-Hue test. The test required normal subjects to use color information in the visual stimulus to perform a color sequencing task. A modification of the test requiring ordering by luminance was used as a control task. Subjects were also imaged as they passively viewed colored stimuli. A limited number of areas responded more to chromatic than achromatic stimulation, including primary visual cortex. Most color-selective activity was concentrated in ventral occipitotemporal cortex. Several areas in ventral cortex were identified. The most posterior, located in posterior fusiform gyrus, corresponded to the area activated by passive viewing of colored stimuli. More anterior and medial color-selective areas were located in the collateral sulcus and fusiform gyrus. These more anterior areas were not identified in previous imaging studies which used passive viewing of colored stimuli, and were most active in our study when visual color information was behaviorally relevant, suggesting that attention influences activity in color-selective areas. The fMRI version of the Farnsworth-Munsell test may be useful in the study of achromatopsia.     

The effects of feature attention on prestimulus cortical activity in the human visual system

Covert attention affects prestimulus activity in the visual cortex. Although most studies investigating neural mechanisms of attention have focused on the effects of spatial attention, attention can also be directed to particular features. To investigate the spatiotemporal nature of feature attention, we measured subjects' brain activity using magnetoencephalography (MEG) and functional magnetic resonance imaging (fMRI) while subjects attended to color or motion of a stimulus based on a visual cue, which was presented 1 s before the stimulus onset. We used the hierarchical Bayesian method that allows us to estimate cortical currents with MEG and fMRI data in the order of millimeters and milliseconds. When subjects attended to color, activity within the color-sensitive area (fusiform gyrus) was selectively enhanced within the prestimulus period. By contrast, when subjects attended to motion, activity within the motion-sensitive area (middle temporal gyrus) was selectively enhanced during this period. This effect was not seen in frontal, parietal, and lower visual areas. Additionally, this effect was transient rather than sustained, suggesting that it differs from temporal aspects of spatial attention. These results suggest that, although both spatial and feature attention modulate prestimulus activity within specific visual areas, neural mechanisms underlying these effects might be different.     

Stimulus-dependent modulations of correlated high-frequency oscillations in cat visual cortex

The hypothesis that correlated neural activity is involved in the cortical representation of visual stimuli was examined by recording multi-unit activity and local field potentials from neurons with non- overlapping receptive fields in areas 17 and 18. Using coherence functions, correlations of oscillatory patterns (35-100 Hz) of neural signals were investigated under three stimulus conditions: (i) a whole field grating or a long bar moving across both receptive fields; (ii) masking the region between both receptive fields while stimulating the remaining visual field; and (iii) two separate stimuli simultaneously moving in opposite directions. Coherences of oscillations were found to be significantly higher in the first stimulus condition than in the other two conditions. Since different visual stimuli were reflected in the coherence of neural activity, we concluded that correlated neural activity is a potential candidate for coding of sensory information.      

Revisiting the role of the fusiform face area in visual expertise

It has previously been reported (Gauthier et al., 2000, Nat. Neurosci., 3:191-197) in a functional magnetic resonance imaging (fMRI) study that objects of visual expertise (cars and birds) activate the right fusiform face area (FFA) more strongly than non-expertise stimuli, and it was argued that the right FFA is involved in expertise specific rather than face specific visual processing. This expertise effect, however, may be due to experts taking advantage of the 'faceness' of the stimuli: birds have faces and three-quarter frontal views of cars resemble faces. This expertise effect may also be caused by a biased attentional modulation: with a blocked fMRI design, experts may attend more to a block of expertise than a block of non-expertise stimuli. In this study, using both side-view car images that do not resemble faces and bird images in an event-related fMRI design that minimizes attentional modulation, an expertise effect in the right FFA is observed in both car and bird experts (although a baseline bias makes the bird expertise effect less reliable). These results are consistent with those of Gauthier et al., and suggest the involvement of the right FFA in processing non-face expertise visual stimuli.     

Motor planning, imagery, and execution in the distributed motor network: a time-course study with functional MRI

Activation of motor-related areas has consistently been found during various motor imagery tasks and is regarded as the central mechanism generating motor imagery. However, the extent to which motor execution and imagery share neural substrates remains controversial. We examined brain activity during preparation for and execution of physical or mental finger tapping. During a functional magnetic resonance imaging at 3 T, 13 healthy volunteers performed an instructed delay finger-tapping task either in a physical mode or mental mode. Number stimuli instructed subjects about a finger-tapping sequence. After an instructed delay period, cue stimuli prompted them either to execute the tapping movement or to imagine it. Two types of planning/preparatory activity common for movement and imagery were found: instruction stimulus-related activity represented widely in multiple motor-related areas and delay period activity in the medial frontal areas. Although brain activity during movement execution and imagery was largely shared in the distributed motor network, imagery-related activity was in general more closely related to instruction-related activity than to the motor execution-related activity. Specifically, activity in the medial superior frontal gyrus, anterior cingulate cortex, precentral sulcus, supramarginal gyrus, fusiform gyrus, and posterolateral cerebellum likely reflects willed generation of virtual motor commands and analysis of virtual sensory signals.     

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.     

Spontaneous activity associated with primary visual cortex: a resting-state FMRI study

Brain functions during the resting state have attracted considerable attention in the past several years. However, little has been known about spontaneous activity in the sensory cortices in the task-free state. This study used functional magnetic resonance imaging (fMRI) to investigate the existence of spontaneous activity in the primary visual areas (PVA) of normal-sighted subjects and to explore the physiological implications of such activity. Our results revealed that we were able to detect spontaneous activity, which was nonrandom in that it was distinctly clustered both temporally and spatially in the PVA of each subject. In addition, the neural network associated with the PVA-related spontaneous activity included the visual association areas, the precuneus, the precentral/postcentral gyrus, the middle frontal gyrus, the fusiform gyrus, the inferior/middle temporal gyrus, and the parahippocampal gyrus. After considering the functions of these regions, we speculated that the PVA-related spontaneous activity may be associated with memory-related mental imagery and/or visual memory consolidation processes. These findings confirm the presence of spontaneous activity in the PVA and related brain areas. This confirmation supports the perspective that brain is a system intrinsically operating on its own, and sensory information interacts with rather than determines the operation of the system.     

Cognitive response profile of the human fusiform face area as determined by MEG

Activation in or near the fusiform gyrus was estimated to faces and control stimuli. Activation peaked at 165 ms and was strongest to digitized photographs of human faces, regardless of whether they were presented in color or grayscale, suggesting that face- and color-specific areas are functionally separate. Schematic sketche evoked approximately 30% less activation than did face photographs. Scrambling the locations of facial features reduced the response by approximately 25% in either hemisphere, suggesting that configurational versus analytic processing is not lateralized at this latency. Animal faces evoked approximately 50% less activity, and common objects, animal bodies or sensory controls evoked approximately 80% less activity than human faces. The (small) responses evoked by meaningless control images were stronger when they included surfaces and shading, suggesting that the fusiform gyrus may use these features in constructing its face-specific response. Putative fusiform activation was not significantly related to stimulus repetition, gender or emotional expression. A midline occipital source significantly distinguished between faces and control images as early as 110 ms, but was more sensitive to sensory qualities. This source significantly distinguished happy and sad faces from those with neutral expressions. We conclude that the fusiform gyrus may selectively encode faces at 165 ms, transforming sensory input for further processing.     

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.      

Dynamic adjustments in prefrontal, hippocampal, and inferior temporal interactions with increasing visual working memory load

The maintenance of visual stimuli across a delay interval in working memory tasks is thought to involve reverberant neural communication between the prefrontal cortex and posterior visual association areas. Recent studies suggest that the hippocampus might also contribute to this retention process, presumably via reciprocal interactions with visual regions. To characterize the nature of these interactions, we performed functional connectivity analysis on an event-related functional magnetic resonance imaging data set in which participants performed a delayed face recognition task. As the number of faces that participants were required to remember was parametrically increased, the right inferior frontal gyrus (IFG) showed a linearly decreasing degree of functional connectivity with the fusiform face area (FFA) during the delay period. In contrast, the hippocampus linearly increased its delay period connectivity with both the FFA and the IFG as the mnemonic load increased. Moreover, the degree to which participants' FFA showed a load-dependent increase in its connectivity with the hippocampus predicted the degree to which its connectivity with the IFG decreased with load. Thus, these neural circuits may dynamically trade off to accommodate the particular mnemonic demands of the task, with IFG-FFA interactions mediating maintenance at lower loads and hippocampal interactions supporting retention at higher loads.     

The potato chip really does look like Elvis! Neural hallmarks of conceptual processing associated with finding novel shapes subjectively meaningful

Clouds and inkblots often compellingly resemble something else--faces, animals, or other identifiable objects. Here, we investigated illusions of meaning produced by novel visual shapes. Individuals found some shapes meaningful and others meaningless, with considerable variability among individuals in these subjective categorizations. Repetition for shapes endorsed as meaningful produced conceptual priming in a priming test along with concurrent activity reductions in cortical regions associated with conceptual processing of real objects. Subjectively meaningless shapes elicited robust activity in the same brain areas, but activity was not influenced by repetition. Thus, all shapes were conceptually evaluated, but stable conceptual representations supported neural priming for meaningful shapes only. During a recognition memory test, performance was associated with increased frontoparietal activity, regardless of meaningfulness. In contrast, neural conceptual priming effects for meaningful shapes occurred during both priming and recognition testing. These different patterns of brain activation as a function of stimulus repetition, type of memory test, and subjective meaningfulness underscore the distinctive neural bases of conceptual fluency versus episodic memory retrieval. Finding meaning in ambiguous stimuli appears to depend on conceptual evaluation and cortical processing events similar to those typically observed for known objects. To the brain, the vaguely Elvis-like potato chip truly can provide a substitute for the King himself.     

The neural substrates of biological motion perception: an fMRI study

We used fMRI to identify the brain areas related to the perception of biological motion (4 T EPI; whole brain). In experiment 1, 10 subjects viewed biological motion (a human figure jumping up and down, composed of 21 dots), alternating with a control stimulus created by applying autoregressive models to the biological motion stimulus (such that the dots' speeds and amplitudes were preserved whereas their linking structure was not). The lengths of the stimulus bouts varied, and therefore the transitions between biological motion and control stimuli were unpredictable. Subjects had to indicate with a button press when each transition occurred. In a related biological motion task, subjects detected short (1 s) disturbances within these displays. We also examined the neural substrates of motion and shape perception, as well as motor imagery, to determine whether or not the cortical regions involved in these processes are also recruited during biological motion perception. Subjects viewed linear motion displays alternating with static dots and a series of common objects alternating with band-limited white noise patterns. Subjects also generated imagery of their own arm movements alternating with visual imagery of common objects. Biological motion specific BOLD signal was found within regions of the lingual gyrus at the cuneus border, showing little overlap with object recognition, linear motion or motion imagery areas. The lingual gyrus activation was replicated in a second experiment that also mapped retinotopic visual areas in three subjects. The results suggest that a region of the lingual gyrus within VP is involved in higher-order processing of motion information.     

Category-specific conceptual processing of color and form in left fronto-temporal cortex

To investigate the cortical basis of color and form concepts, we examined event-related functional magnetic resonance imaging (fMRI) responses to matched words related to abstract color and form information. Silent word reading elicited activity in left temporal and frontal cortex, where category-specific activity differences were also observed. Whereas color words preferentially activated anterior parahippocampal gyrus, form words evoked category-specific activity in fusiform and middle temporal gyrus as well as premotor and dorsolateral prefrontal areas in inferior and middle frontal gyri. These results demonstrate that word meanings and concepts are not processed by a unique cortical area, but by different sets of areas, each of which may contribute differentially to conceptual semantic processing. We hypothesize that the anterior parahippocampal activation to color words indexes computation of the visual feature conjunctions and disjunctions necessary for classifying visual stimuli under a color concept. The predominant premotor and prefrontal activation to form words suggests action-related information processing and may reflect the involvement of neuronal elements responding in an either-or fashion to mirror neurons related to adumbrating shapes.     

Enhanced temporal non-linearities in human object-related occipito-temporal cortex

To what extent does neural activation in human visual cortex follow the temporal dynamics of the optical retinal stimulus? Specifically, to what extent does stimulus evoked neural activation persist after stimulus termination? In the present study, we used functional magnetic resonance imaging (fMRI) to explore the resulting temporal non-linearities across the entire constellation of human visual areas. Gray-scale images of animals, houses and faces were presented at two different presentation rates - 1 and 4 Hz - and the fMRI signal was analyzed in retinotopic and in high order occipito-temporal visual areas. In early visual areas and the motion sensitive area MT/V5, a fourfold increase in stimulus presentation rate evoked a twofold increase in signal amplitude. However, in high order visual areas, signal amplitude increased only by 25%. A control experiment ruled out the possibility that this difference was due to signal saturation ('ceiling') effects. A likely explanation for the stronger non-linearities in occipito-temporal cortex is a persistent neuronal activation that continues well after stimulus termination in the 1 Hz condition. These persistent activations might serve as a short term (iconic) memory mechanism for preserving a trace of the stimulus even in its absence and for future integration with temporally correlated stimuli. Two alternative models of persistence (inhibitory and excitatory) are proposed to explain the data.     

Time representations can be made from nontemporal information in the brain: an MEG study

Perceiving the passage of time is an essential ability for humans and animals. Here we used magnetoencephalography and investigated how our internal clock system in the brain converts sensory experiences into their time representations. We focused on neural activities in the high-level visual areas of human subjects when they saw visual patterns and estimated the duration of their presentation. The activities in the visual areas could give us neural indices about when subjects perceived the appearance and disappearance of visual patterns, thus enabling us to measure the stimulus duration "in the brain." Comparing these neural indices of time with subjective durations of stimuli measured psychophysically, we showed that, under some circumstances, these 2 durations can be dissociated in the opposite directions: although the neural index signals a "longer" interval of a stimulus over another one, it is perceived as "shorter" in subjective time scale. Instead, we found that these subjective intervals are closely linked to the strength, not timings, of neural activity evoked by visual patterns. Our results indicate that "nontemporal information" of perceptual neural activity, such as the strength (not latency) of neural responses, can influence the shaping of time representations in our brain.     

A genetic model for understanding higher order visual processing: functional interactions of the ventral visual stream in Williams syndrome

Williams syndrome (WS) is a rare neurodevelopmental disorder caused by a 1.6 Mb microdeletion on chromosome 7q11.23 and characterized by hypersocial personality and prominent visuospatial construction impairments. Previous WS studies have identified functional and structural abnormalities in the hippocampal formation, prefrontal regions crucial for amygdala regulation and social cognition, and the dorsal visual stream, notably the intraparietal sulcus (IPS). Although aberrant ventral stream activation has not been found in WS, object-related visual information that is processed in the ventral stream is a critical source of input into these abnormal regions. The present study, therefore, examined neural interactions of ventral stream areas in WS. Using a passive face- and house-viewing paradigm, activation and functional connectivity of stimulus-selective regions in fusiform and parahippocampal gyri, respectively, were investigated. During house viewing, significant activation differences were observed between participants with WS and a matched control group in IPS. Abnormal functional connectivity was found between parahippocampal gyrus and parietal cortex and between fusiform gyrus and a network of brain regions including amygdala and portions of prefrontal cortex. These results indicate that abnormal upstream visual object processing may contribute to the complex cognitive/behavioral phenotype in WS and provide a systems-level characterization of genetically mediated abnormalities of neural interactions.     

Attentional load and sensory competition in human vision: modulation of fMRI responses by load at fixation during task-irrelevant stimulation in the peripheral visual field

Perceptual suppression of distractors may depend on both endogenous and exogenous factors, such as attentional load of the current task and sensory competition among simultaneous stimuli, respectively. We used functional magnetic resonance imaging (fMRI) to compare these two types of attentional effects and examine how they may interact in the human brain. We varied the attentional load of a visual monitoring task performed on a rapid stream at central fixation without altering the central stimuli themselves, while measuring the impact on fMRI responses to task-irrelevant peripheral checkerboards presented either unilaterally or bilaterally. Activations in visual cortex for irrelevant peripheral stimulation decreased with increasing attentional load at fixation. This relative decrease was present even in V1, but became larger for successive visual areas through to V4. Decreases in activation for contralateral peripheral checkerboards due to higher central load were more pronounced within retinotopic cortex corresponding to 'inner' peripheral locations relatively near the central targets than for more eccentric 'outer' locations, demonstrating a predominant suppression of nearby surround rather than strict 'tunnel vision' during higher task load at central fixation. Contralateral activations for peripheral stimulation in one hemifield were reduced by competition with concurrent stimulation in the other hemifield only in inferior parietal cortex, not in retinotopic areas of occipital visual cortex. In addition, central attentional load interacted with competition due to bilateral versus unilateral peripheral stimuli specifically in posterior parietal and fusiform regions. These results reveal that task-dependent attentional load, and interhemifield stimulus-competition, can produce distinct influences on the neural responses to peripheral visual stimuli within the human visual system. These distinct mechanisms in selective visual processing may be integrated within posterior parietal areas, rather than earlier occipital cortex.     

The effect of prior visual information on recognition of speech and sounds

To identify and categorize complex stimuli such as familiar objects or speech, the human brain integrates information that is abstracted at multiple levels from its sensory inputs. Using cross-modal priming for spoken words and sounds, this functional magnetic resonance imaging study identified 3 distinct classes of visuoauditory incongruency effects: visuoauditory incongruency effects were selective for 1) spoken words in the left superior temporal sulcus (STS), 2) environmental sounds in the left angular gyrus (AG), and 3) both words and sounds in the lateral and medial prefrontal cortices (IFS/mPFC). From a cognitive perspective, these incongruency effects suggest that prior visual information influences the neural processes underlying speech and sound recognition at multiple levels, with the STS being involved in phonological, AG in semantic, and mPFC/IFS in higher conceptual processing. In terms of neural mechanisms, effective connectivity analyses (dynamic causal modeling) suggest that these incongruency effects may emerge via greater bottom-up effects from early auditory regions to intermediate multisensory integration areas (i.e., STS and AG). This is consistent with a predictive coding perspective on hierarchical Bayesian inference in the cortex where the domain of the prediction error (phonological vs. semantic) determines its regional expression (middle temporal gyrus/STS vs. AG/intraparietal sulcus).