Two distinct neural mechanisms for category-selective responses

The cognitive and neural mechanisms mediating category-selective responses in the human brain remain controversial. Using functional magnetic resonance imaging and effective connectivity analyses (Dynamic Causal Modelling), we investigated animal- and tool-selective responses by manipulating stimulus modality (pictures versus words) and task (implicit versus explicit semantic). We dissociated two distinct mechanisms that engender category selectivity: in the ventral occipito-temporal cortex, tool-selective responses were observed irrespective of task, greater for pictures and mediated by bottom-up effects. In a left temporo-parietal action system, tool-selective responses were observed irrespective of modality, greater for explicit semantic tasks and mediated by top-down modulation from the left prefrontal cortex. These distinct activation and connectivity patterns suggest that the two systems support different cognitive operations, with the ventral occipito-temporal regions engaged in structural processing and the dorsal visuo-motor system in strategic semantic processing. Consistent with current semantic theories, explicit semantic processing of tools might thus rely on reactivating their associated action representations via top-down modulation. In terms of neuronal mechanisms, the category selectivity may be mediated by distinct top-down (task-dependent) and bottom-up (stimulus-dependent) mechanisms.     

Mechanisms of top-down facilitation in perception of visual objects studied by FMRI

Prior knowledge regarding the possible identity of an object facilitates its recognition from a degraded visual input, though the underlying mechanisms are unclear. Previous work implicated ventral visual cortex but did not disambiguate whether activity-changes in these regions are causal to or merely reflect an effect of facilitated recognition. We used functional magnetic resonance imaging to study top-down influences on processing of gradually revealed objects, by preceding each object with a name that was congruent or incongruent with the object. Congruently primed objects were recognized earlier than incongruently primed, and this was paralleled by shifts in activation profiles for ventral visual, parietal, and prefrontal cortices. Prior to recognition, defined on a trial-by-trial basis, activity in ventral visual cortex rose gradually but equivalently for congruently and incongruently primed objects. In contrast, prerecognition activity was greater with congruent priming in lateral parietal, retrosplenial, and lateral prefrontal cortices, whereas functional coupling between parietal and ventral visual (and also left lateral prefrontal and parietal) cortices was enhanced in the same context. Thus, when controlling for recognition point and stimulus information, activity in ventral visual cortex mirrors recognition success, independent of condition. Facilitation by top-down cues involves lateral parietal cortex interacting with ventral visual areas, potentially explaining why parietal lesions can lead to deficits in recognizing degraded objects even in the context of top-down knowledge.     

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.     

Matching two imagined clocks: the functional anatomy of spatial analysis in the absence of visual stimulation

Do spatial operations on mental images and those on visually presented material share the same neural substrate? We used the high spatial resolution of functional magnetic resonance imaging to determine whether areas in the parietal lobe that have been implicated in the spatial transformation of visual percepts are also activated during the generation and spatial analysis of imagined objects. Using a behaviourally controlled mental imagery paradigm, which did not involve any visual stimulation, we found robust activation in posterior parietal cortex in both hemispheres. We could thus identify the subset of spatial analysis-related activity that is involved in spatial operations on mental images in the absence of external visual input. This result clarifies the nature of top-down processes in the dorsal stream of the human cerebral cortex and provides evidence for a specific convergence of the pathways of imagery and visual perception within the parietal lobes.     

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.     

Imagery and perception share cortical representations of content and location

Visual imagery allows us to vividly imagine scenes in the absence of visual stimulation. The likeness of visual imagery to visual perception suggests that they might share neural mechanisms in the brain. Here, we directly investigated whether perception and visual imagery share cortical representations. Specifically, we used a combination of functional magnetic resonance imaging (fMRI) and multivariate pattern classification to assess whether imagery and perception encode the "category" of objects and their "location" in a similar fashion. Our results indicate that the fMRI response patterns for different categories of imagined objects can be used to predict the fMRI response patters for seen objects. Similarly, we found a shared representation of location in low-level and high-level ventral visual cortex. Thus, our results support the view that imagery and perception are based on similar neural representations.     

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.     

Brain networks involved in viewing angry hands or faces

Most neuropsychological research on the perception of emotion concerns the perception of faces. Yet in everyday life, hand actions are also modulated by our affective state, revealing it, in turn, to the observer. We used functional magnetic resonance imaging (fMRI) to identify brain regions engaged during the observation of hand actions performed either in a neutral or an angry way. We also asked whether these are the same regions as those involved in perceiving expressive faces. During the passive observation of emotionally neutral hand movements, the fMRI signal increased significantly in dorsal and ventral premotor cortices, with the exact location of the 'peaks' distinct from those induced by face observation. Various areas in the extrastriate visual cortex were also engaged, overlapping with the face-related activity. When the observed hand action was performed with emotion, additional regions were recruited including the right dorsal premotor, the right medial prefrontal cortex, the left anterior insula and a region in the rostral part of the supramarginal gyrus bilaterally. These regions, except for the supramarginal gyrus, were also activated during the perception of angry faces. These results complement the wealth of studies on the perception of affect from faces and provide further insights into the processes involved in the perception of others underlying, perhaps, social constructs such as empathy.     

Cross-modal binding and activated attentional networks during audio-visual speech integration: a functional MRI study

We evaluated the neural substrates of cross-modal binding and divided attention during audio-visual speech integration using functional magnetic resonance imaging. The subjects (n = 17) were exposed to phonemically concordant or discordant auditory and visual speech stimuli. Three different matching tasks were performed: auditory-auditory (AA), visual-visual (VV) and auditory-visual (AV). Subjects were asked whether the prompted pair were congruent or not. We defined the neural substrates for the within-modal matching tasks by VV-AA and AA-VV. We defined the cross-modal area as the intersection of the loci defined by AV-AA and AV-VV. The auditory task activated the bilateral anterior superior temporal gyrus and superior temporal sulcus, the left planum temporale and left lingual gyrus. The visual task activated the bilateral middle and inferior frontal gyrus, right occipito-temporal junction, intraparietal sulcus and left cerebellum. The bilateral dorsal premotor cortex, posterior parietal cortex (including the bilateral superior parietal lobule and the left intraparietal sulcus) and right cerebellum showed more prominent activation during AV compared with AA and VV. Within these areas, the posterior parietal cortex showed more activation during concordant than discordant stimuli, and hence was related to cross-modal binding. Our results indicate a close relationship between cross-modal attentional control and cross-modal binding during speech reading.     

Distinct causal influences of parietal versus frontal areas on human visual cortex: evidence from concurrent TMS-fMRI

It has often been proposed that regions of the human parietal and/or frontal lobe may modulate activity in visual cortex, for example, during selective attention or saccade preparation. However, direct evidence for such causal claims is largely missing in human studies, and it remains unclear to what degree the putative roles of parietal and frontal regions in modulating visual cortex may differ. Here we used transcranial magnetic stimulation (TMS) and functional magnetic resonance imaging (fMRI) concurrently, to show that stimulating right human intraparietal sulcus (IPS, at a site previously implicated in attention) elicits a pattern of activity changes in visual cortex that strongly depends on current visual context. Increased intensity of IPS TMS affected the blood oxygen level-dependent (BOLD) signal in V5/MT+ only when moving stimuli were present to drive this visual region, whereas TMS-elicited BOLD signal changes were observed in areas V1-V4 only during the absence of visual input. These influences of IPS TMS upon remote visual cortex differed significantly from corresponding effects of frontal (eye field) TMS, in terms of how they related to current visual input and their spatial topography for retinotopic areas V1-V4. Our results show directly that parietal and frontal regions can indeed have distinct patterns of causal influence upon functional activity in human visual cortex.     

Cortical connections of the inferior parietal cortical convexity of the macaque monkey

We traced the cortical connections of the 4 cytoarchitectonic fields--Opt, PG, PFG, PF--forming the cortical convexity of the macaque inferior parietal lobule (IPL). Each of these fields displayed markedly distinct sets of connections. Although Opt and PG are both targets of dorsal visual stream and temporal visual areas, PG is also target of somatosensory and auditory areas. Primary parietal and frontal connections of Opt include area PGm and eye-related areas. In contrast, major parietal and frontal connections of PG include IPL, caudal superior parietal lobule (SPL), and agranular frontal arm-related areas. PFG is target of somatosensory areas and also of the medial superior temporal area (MST) and temporal visual areas and is connected with IPL, rostral SPL, and ventral premotor arm- and face-related areas. Finally, PF is primarily connected with somatosensory areas and with parietal and frontal face- and arm-related areas. The present data challenge the bipartite subdivision of the IPL convexity into a caudal and a rostral area (7a and 7b, respectively) and provide a new anatomical frame of reference of the macaque IPL convexity that advances our present knowledge on the functional organization of this cortical sector, giving new insight into its possible role in space perception and motor control.     

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.     

Cortical connections of the macaque anterior intraparietal (AIP) area

We traced the cortical connections of the anterior intraparietal (AIP) area, which is known to play a crucial role in visuomotor transformations for grasping. AIP displayed major connections with 1) areas of the inferior parietal lobule convexity, the rostral part of the lateral intraparietal area and the SII region; 2) ventral visual stream areas of the lower bank of the superior temporal sulcus and the middle temporal gyrus; and 3) the premotor area F5 and prefrontal areas 46 and 12. Additional connections were observed with the caudal intraparietal area and the ventral part of the frontal eye field. This study suggests that visuomotor transformations for object-oriented actions, processed in AIP, rely not only on dorsal visual stream information related to the object's physical properties but also on ventral visual stream information related to object identity. The identification of direct anatomical connections with the inferotemporal cortex suggests that AIP also has a unique role in linking the parietofrontal network of areas involved in sensorimotor transformations for grasping with areas involved in object recognition. Thus, AIP could represent a crucial node in a cortical circuit in which hand-related sensory and motor signals gain access to representations of object identity for tactile object recognition.     

Mistaking a house for a face: neural correlates of misperception in healthy humans

Individuals with normal vision can sometimes momentarily mistake one object for another. In this functional magnetic resonance imaging study, we investigated how extrastriate visual regions respond during these erroneous perceptual judgements. Subjects were asked to discriminate images of houses and faces that were degraded such that they were close to an individually defined threshold for perception. On correct trials, voxels localized on the inferior occipital (OFA), fusiform (FFA) and parahippocampal (PPA) gyri exhibited selectivity for face and house images as expected. On incorrect trials, no face- or place-selectivity was observed for OFA or PPA. However, consistent with 'predictive coding' accounts of perception, we observed that the FFA also responded robustly on trials where a house was misperceived as a face, and concurrent activation was observed in medio-frontal and right parietal regions previously implicated in decision making under uncertainty. We suggest that FFA responses during misperception may be driven by a predictive top-down signal from these regions.     

Competition in working memory reduces frontal guidance of visual selection

Working memory (WM) representations can bias visual selection to matching stimuli in the field. WM biases can, however, be modulated by the level of cognitive load, with WM guidance reduced as memory load increases. Here, we used functional magnetic resonance imaging to distinguish between competing hypotheses for the reduction of WM guidance under load: 1) poor neural representations of memory contents under high load, 2) strategic control at high loads to direct attention away from search distracters matching the WM content, and 3) reduction of frontal top-down biasing of visual areas with increasing memory loads. We show that matching between WM contents and the visual display appeared to be well represented in visual areas under high memory loads, despite a lack of WM guidance at the behavioral level. There was little engagement of "cognitive control" areas in the prefrontal cortex during search at high loads. More importantly, WM guidance at low loads engaged a set of frontal regions in the superior and inferior ventral frontal cortex. Functional connectivity analyses revealed frontal regions working in concert with occipital areas at low memory loads, but this coupling was disrupted by increased memory load. We discuss the implications for understanding the mechanisms supporting the interplay between WM and attention.     

Dorsal cortical regions subserving visually guided saccades in humans: an fMRI study

Neurophysiological studies in non-human primates have identified saccade-related neuronal activity in cortical regions including frontal (FEF), supplementary (SEF) and parietal eye fields. Lesion and neuroimaging studies suggest a generally homologous mapping of the oculomotor system in humans; however, a detailed mapping of the precise anatomical location of these functional regions has not yet been achieved. We investigated dorsal frontal and parietal cortex during a saccade task vs. central fixation in 10 adult subjects using functional magnetic resonance imaging (fMRI). The FEF were restricted to the precentral sulcus, and did not extend anteriorly into Brodmann area 8, which has traditionally been viewed as their location in humans. The SEF were located in cortex along the interhemispheric fissure and extended minimally onto the dorsal cortical surface. Parietal activation was seen in precuneus and along the intraparietal sulcus, extending into both superior and inferior parietal lobules. These findings localize areas in frontal and parietal cortex involved in saccade generation in humans, and indicate significant differences from the macaque monkey in both frontal and parietal cortex. These differences may have functional implications for the roles these areas play in visuomotor processes.      

Fractionating attentional control using event-related fMRI

Despite numerous functional neuroimaging and lesion studies of human executive function, the precise neuroanatomical correlates of specific components of attentional control remain controversial. Using a novel approach that focused upon volunteer behavior rather than experimental manipulations, specific components of attentional shifting were fractionated, and their neural correlates differentiated using event-related fMRI. The results demonstrate that the ventrolateral prefrontal cortex is involved in switching attention "between" stimulus dimensions, whereas the posterior parietal cortex mediates changes in stimulus-response mapping. Furthermore, reversals based on negative feedback activated the lateral orbitofrontal cortex, whereas positive feedback modulated activity in the medial orbital frontal cortex. Finally, the dorsolateral prefrontal cortex was active throughout solution search. These findings support the hypothesis that lateral prefrontal, orbital, and parietal areas form a supervisory network that controls the focus of attention and suggests that these regions can be fractionated in terms of their specific contributions.     

Connections of Inferior Temporal Areas TEO and TE with Parietal and Frontal Cortex in Macaque Monkeys

Inferior temporal cortex is perhaps the highest visual processingarea and much anatomical work has focused on its connectionswith other visual areas in temporal and occipital cortex. Herewe report connections of inferior temporal cortex with regionsin the frontal and parietal lobes. Inferior temporal areas TEOand TE were injected with WGA-HRP and ³H-AA, respectively, orvice versa, in 1-week-old infant and 3–4–year-oldadult monkeys (Macaca mulatta). The results indicated that whereasTEO has more extensive connections with parietal areas, TE hasmore extensive connections with prefrontal areas. Thus, in theintraparietal sulcus, area TEO is connected with areas LIPd,LIPv, and V3A, and with the as yet undefined region betweenLIPv and V3A, whereas the connections of TE are predominantlywith LIPd, and to a lesser extent with LIPv. In the prefrontalcortex, area TE is connected with areas 8 and 45 in the inferiorlimb of the anterior bank of the arcuate sulcus, with area 12on the inferior prefrontal convexity, and with areas 11 and13 on the orbital surface. By contrast, the connections of areaTEO are limited to areas 8, 45, and 12. Furthermore, withinprefrontal cortex, the projections from areas TEO and TE terminatein different layers in areas 8 and 45, such that those fromTEO terminate in all layers, whereas those from TE terminatein layers I and V/VI only. In contrast to the connections ofareas TEO and TE with various medical temporal-lobe and subcorticalstructures, which are immature in infant monkeys (Webster etal., 1991, 1993b), the connections with parietal and prefrontalareas appear adult-like as early as 1 week of age.     

Modulation of connectivity in visual pathways by attention: cortical interactions evaluated with structural equation modelling and fMRI

Electrophysiological and neuroimaging studies have shown that attention to visual motion can increase the responsiveness of the motion- selective cortical area V5 and the posterior parietal cortex (PP). Increased or decreased activation in a cortical area is often attributed to attentional modulation of the cortical projections to that area. This leads to the notion that attention is associated with changes in connectivity. We have addressed attentional modulation of effective connectivity using functional magnetic resonance imaging (fMRI). Three subjects were scanned under identical stimulus conditions (visual motion) while varying only the attentional component of the task. Haemodynamic responses defined an occipito-parieto-frontal network, including the, primary visual cortex (V1), V5 and PR A structural equation model of the interactions among these dorsal visual pathway areas revealed increased connectivity between V5 and PP related to attention. On the basis of our analysis and the neuroanatomical pattern of projections from the prefrontal cortex to PP we attributed the source of modulatory influences, on the posterior visual pathway, to the prefrontal cortex (PFC). To test this hypothesis we included the PFC in our model as a 'modulator' of the pathway between V5 and PP, using interaction terms in the structural equation model. This analysis revealed a significant modulatory effect of prefrontal regions on V5 afferents to posterior parietal cortex.      

Working memory of auditory localization

To investigate brain mechanisms of sound location memory, we studied the distribution of brain activation with functional magnetic resonance imaging (fMRI) in subjects performing an audiospatial n-back task with three memory load levels. Working memory processing of audiospatial information activated areas in the superior, middle and inferior frontal gyri, and in the posterior parietal and middle temporal cortices. In a control experiment, fMRI during audio- and visuospatial 2-back task performances revealed only few differentially activated subregions between the two tasks. These results demonstrate that working memory processing of auditory locations involves a distributed network of brain areas and suggest that mnemonic processing of audio- and visuospatial information is directed along a common neural pathway in the posterior parietal and prefrontal cortices.