While a network of cortical regions contribute to face processing, the lesions in acquired prosopagnosia are highly variable, and likely result in different combinations of spared and affected regions of this network. To assess the residual functional sensitivities of spared regions in prosopagnosia, we designed a rapid event-related functional magnetic resonance imaging (fMRI) experiment that included pairs of faces with same or different identities and same or different expressions. By measuring the release from adaptation to these facial changes we determined the residual sensitivity of face-selective regions-of-interest. We tested three patients with acquired prosopagnosia, and all three of these patients demonstrated residual sensitivity for facial identity changes in surviving fusiform and occipital face areas of either the right or left hemisphere, but not in the right posterior superior temporal sulcus. The patients also showed some residual capabilities for facial discrimination with normal performance on the Benton Facial Recognition Test, but impaired performance on more complex tasks of facial discrimination. We conclude that fMRI can demonstrate residual processing of facial identity in acquired prosopagnosia, that this adaptation can occur in the same structures that show similar processing in healthy subjects, and further, that this adaptation may be related to behavioral indices of face perception.
face perception; identity; expression; fMRI; adaptation; sensitivity; prosopagnosia
The ability to dynamically and rapidly adjust task performance based on its outcome is fundamental to adaptive, flexible behavior. Over trials of a task, responses speed up until an error is committed and after the error responses slow down. These dynamic adjustments serve to optimize performance and are well-described by the speed-accuracy trade-off (SATO) function. We hypothesized that SATOs based on outcomes reflect reciprocal changes in the allocation of attention between the internal milieu and the task-at-hand, as indexed by reciprocal changes in activity between the default and dorsal attention brain networks. We tested this hypothesis using functional MRI to examine the pattern of network activation over a series of trials surrounding and including an error. We further hypothesized that these reciprocal changes in network activity are coordinated by the posterior cingulate cortex (PCC) and would rely on the structural integrity of its white matter connections. Using diffusion tensor imaging, we examined whether fractional anisotropy of the posterior cingulum bundle correlated with the magnitude of reciprocal changes in network activation around errors. As expected, reaction time (RT) in trials surrounding errors was consistent with predictions from the SATO function. Activation in the default network was: (i) inversely correlated with RT, (ii) greater on trials before than after an error and (iii) maximal at the error. In contrast, activation in the right intraparietal sulcus of the dorsal attention network was (i) positively correlated with RT and showed the opposite pattern: (ii) less activation before than after an error and (iii) the least activation on the error. Greater integrity of the posterior cingulum bundle was associated with greater reciprocity in network activation around errors. These findings suggest that dynamic changes in attention to the internal versus external milieu in response to errors underlie SATOs in RT and are mediated by the PCC.
Hemianopia patients have lost vision from the contralateral hemifield, but make behavioural adjustments to compensate for this field loss. As a result, their visual performance and behaviour contrast with those of hemineglect patients who fail to attend to objects contralateral to their lesion. These conditions differ in their ocular fixations and perceptual judgments. During visual search, hemianopic patients make more fixations in contralesional space while hemineglect patients make fewer. During line bisection, hemianopic patients fixate the contralesional line segment more and make a small contralesional bisection error, while hemineglect patients make few contralesional fixations and a larger ipsilesional bisection error. Hence, there is an attentional failure for contralesional space in hemineglect but a compensatory adaptation to attend more to the blind side in hemianopia. A challenge for models of visual attentional processes is to show how compensation is achieved in hemianopia, and why such processes are hindered or inaccessible in hemineglect. We used a neurophysiology-derived computational model to examine possible cortical compensatory processes in simulated hemianopia from a V1 lesion and compared results with those obtained with the same processes under conditions of simulated hemineglect from a parietal lesion. A spatial compensatory bias to increase attention contralesionally replicated hemianopic scanning patterns during visual search but not during line bisection. To reproduce the latter required a second process, an extrastriate lateral connectivity facilitating form completion into the blind field: this allowed accurate placement of fixations on contralesional stimuli and reproduced fixation patterns and the contralesional bisection error of hemianopia. Neither of these two cortical compensatory processes was effective in ameliorating the ipsilesional bias in the hemineglect model. Our results replicate normal and pathological patterns of visual scanning, line bisection, and differences between hemianopia and hemineglect, and may explain why compensatory processes that counter the effects of hemianopia are ineffective in hemineglect.
Assessment of face specificity in prosopagnosia is hampered by difficulty in gauging pre-morbid expertise for non-face object categories, for which humans vary widely in interest and experience. In this study, we examined the correlation between visual and verbal semantic knowledge for cars to determine if visual recognition accuracy could be predicted from verbal semantic scores. We had 33 healthy subjects and six prosopagnosic patients first rated their own knowledge of cars. They were then given a test of verbal semantic knowledge that presented them with the names of car models, to which they were to match the manufacturer. Lastly, they were given a test of visual recognition, presenting them with images of cars to which they were to provide information at three levels of specificity: model, manufacturer and decade of make. In controls, while self-ratings were only moderately correlated with either visual recognition or verbal semantic knowledge, verbal semantic knowledge was highly correlated with visual recognition, particularly for more specific levels of information. Item concordance showed that less-expert subjects were more likely to provide the most specific information (model name) for the image when they could also match the manufacturer to its name. Prosopagnosic subjects showed reduced visual recognition of cars after adjusting for verbal semantic scores. We conclude that visual recognition is highly correlated with verbal semantic knowledge, that formal measures of verbal semantic knowledge are a more accurate gauge of expertise than self-ratings, and that verbal semantic knowledge can be used to adjust tests of visual recognition for pre-morbid expertise in prosopagnosia.
semantic memory; vision; object recognition; face processing
Simultanagnosia is a disorder of visual attention that leaves a patient's world unglued: scenes and objects are perceived in a piecemeal manner. It is generally agreed that simultanagnosia is related to an impairment of attention, but it is unclear whether this impairment is object- or space-based in nature. We first consider the findings that support a concept of simultanagnosia as deficit of object-based attention. We then examine the evidence suggesting that simultanagnosia results from damage to a space-based attentional system, and in particular a model of simultanagnosia as a narrowed spatial window of attention. We ask whether seemingly object-based deficits can be explained by space-based mechanisms, and consider the evidence that object processing influences spatial deficits in this condition. Finally, we discuss limitations of a space-based attentional explanation.
Bálint syndrome; simultanagnosia; object-based attention; space-based attention; vision
Impaired antisaccade performance is a consistent cognitive finding in schizophrenia. Antisaccades require both response inhibition and volitional motor programming, functions that are essential to flexible responding. We investigated whether abnormal timing of hemodynamic responses (HDRs) to antisaccades might contribute to perseveration of ocular motor responses in schizophrenia. We focused on the frontal eye field (FEF), which has been implicated in the persistent effects of antisaccades on subsequent responses in healthy individuals.
Eighteen chronic, medicated schizophrenia outpatients and 15 healthy controls performed antisaccades and prosaccades during functional MRI. Finite impulse response models provided unbiased estimates of event-related HDRs. We compared groups on the peak amplitude, time-to-peak, and full-width half-max of the HDRs.
In patients, HDRs in bilateral FEF were delayed and prolonged but ultimately of similar amplitude to that of controls. These abnormalities were present for antisaccades, but not prosaccades, and were not seen in a control region. More prolonged HDRs predicted slower responses in trials that followed an antisaccade. This suggests that persistent FEF activity following an antisaccade contributes to inter-trial effects on latency.
Delayed and prolonged HDRs for antisaccades in schizophrenia suggest that the functions necessary for successful antisaccade performance take longer to implement and are more persistent. If abnormally persistent neural responses on cognitively demanding tasks are a more general feature of schizophrenia, they may contribute to response perseveration, a classic behavioral abnormality. These findings also underscore the importance of evaluating the temporal dynamics of neural activity to understand cognitive dysfunction in schizophrenia.
schizophrenia; antisaccade; frontal eye field; functional MRI; perseveration; inhibition
Whether face adaptation confers any advantages to perceptual processing remains an open question. We investigated whether face adaptation can enhance the ability to make fine discriminations in the vicinity of the adapted face. We compared face discrimination thresholds in three adapting conditions: (i) same-face: where adapting and test faces were the same, (ii) different-face: where adapting and test faces differed, and (iii) baseline: where the adapting stimulus was a blank. Discrimination thresholds for morphed identity changes involving the adapted face (same-face) improved compared with those from both the baseline (no-adaptation) and different-face conditions. Since adapting to a face did not alter discrimination performance for other faces, this effect is selective for the facial identity that is adapted. These results indicate a form of gain control to heighten perceptual sensitivity in the vicinity of a currently viewed face, analogous to forms of adaptive gain control at lower levels of the visual system.
face perception; fine discrimination; face aftereffects; adaptation
There are few clinical tools that assess decision-making under risk. Tests that characterize sensitivity and bias in decisions between prospects varying in magnitude and probability of gain may provide insights in conditions with anomalous reward-related behaviour.
We designed a simple test of how subjects integrate information about the magnitude and the probability of reward, which can determine discriminative thresholds and choice bias in decisions under risk.
Twenty subjects were required to choose between two explicitly described prospects, one with higher probability but lower magnitude of reward than the other, with the difference in expected value between the two prospects varying from 3 to 23%.
Subjects showed a mean threshold sensitivity of 43% difference in expected value. Regarding choice bias, there was a ‘risk premium’ of 38%, indicating a tendency to choose higher probability over higher reward. An analysis using prospect theory showed that this risk premium is the predicted outcome of hypothesized non-linearities in the subjective perception of reward value and probability.
This simple test provides a robust measure of discriminative value thresholds and biases in decisions under risk. Prospect theory can also make predictions about decisions when subjective perception of reward or probability is anomalous, as may occur in populations with dopaminergic or striatal dysfunction, such as Parkinson's disease and schizophrenia.
Optimizing outcomes involves rapidly and continuously adjusting behavior based on context. While most behavioral studies focus on immediate task conditions, responses to events are also influenced by recent history. We used magnetoencephalography and a saccadic paradigm to investigate the neural bases of 2 trial history effects that are well characterized in the behavioral eye movement literature: task-switching and the prior-antisaccade effect. We found that switched trials were associated with increased errors and transient increases in activity in the frontal eye field (FEF) and anterior cingulate cortex early in the preparatory period. These activity changes are consistent with active reconfiguration of the task set, a time-limited process that is triggered by the instructional cue. Following an antisaccade versus prosaccade, there was increased activity in the FEF and prefrontal cortex that persisted into the preparatory period of the subsequent trial, and saccadic latencies were prolonged. We attribute these effects to persistent inhibition of the ocular motor response system from the prior antisaccade. These findings refine our understanding of how trial history interacts with current task demands to adjust responses. Such dynamic modulations of neural activity and behavior by recent experience are at the heart of adaptive flexible behavior.
antisaccade; frontal eye field; magnetoencephalography; saccade; task-switching
Response inhibition, or the suppression of prepotent, but contextually inappropriate behaviors, is essential to adaptive, flexible responding. In autism spectrum disorders (ASD), difficulty inhibiting prepotent behaviors may contribute to restricted, repetitive behavior (RRB). Individuals with ASD consistently show deficient response inhibition while performing antisaccades, which require one to inhibit the prepotent response of looking towards a suddenly appearing stimulus (i.e., a prosaccade), and to substitute a gaze in the opposite direction. Here, we used fMRI to identify the neural correlates of this deficit. We focused on two regions that are critical for saccadic inhibition: the frontal eye field (FEF), the key cortical region for generating volitional saccades, and the dorsal anterior cingulate cortex (dACC), which is thought to exert top-down control on FEF. We also compared ASD and control groups on the functional connectivity of the dACC and FEF during saccadic performance. In the context of an increased antisaccade error rate, ASD participants showed decreased functional connectivity of the FEF and dACC and decreased inhibition-related activation (based on the contrast of antisaccades and prosaccades) in both regions. Decreased dACC activation correlated with a higher error rate in both groups, consistent with a role in top-down control. Within the ASD group, increased FEF activation and dACC/FEF functional connectivity were associated with more severe RRB. These findings demonstrate functional abnormalities in a circuit critical for volitional ocular motor control in ASD that may contribute to deficient response inhibition and to RRB. More generally, our findings suggest reduced cognitive control over behavior by the dACC in ASD.
Face aftereffects are proving to be an effective means of examining the properties of face-specific processes in the human visual system. We examined the role of gender in the neural representation of faces using a contrast-based adaptation method. If faces of different genders share the same representational face space, then adaptation to a face of one gender should affect both same- and different-gender faces. Further, if these aftereffects differ in magnitude, this may indicate distinct gender-related factors in the organization of this face space. To control for a potential confound between physical similarity and gender, we used a Bayesian ideal observer and human discrimination data to construct a stimulus set in which pairs of different-gender faces were equally dissimilar as same-gender pairs. We found that the recognition of both same-gender and different-gender faces was suppressed following a brief exposure of 100ms. Moreover, recognition was more suppressed for test faces of a different-gender than those of the same-gender as the adaptor, despite the equivalence in physical and psychophysical similarity. Our results suggest that male and female faces likely occupy the same face space, allowing transfer of aftereffects between the genders, but that there are special properties that emerge along gender-defining dimensions of this space.
The amygdala detects aversive events and coordinates with rostral anterior cingulate cortex to adapt behavior. We assessed error-related activation in these regions and its relation to task performance using functional MRI and a saccadic paradigm. Both amygdalae showed increased activation during error versus correct antisaccade trials that was correlated with error-related activation in the corresponding rostral anterior cingulate cortex. Together, activation in right amygdala and right rostral anterior cingulate cortex predicted greater accuracy. In contrast, left amygdala activation predicted a higher error rate. These findings support a role for amygdala in response monitoring. Consistent with proposed specializations of right and left amygdala in aversive conditioning, we hypothesize that right amygdala-rostral anterior cingulate cortex interactions mediate learning to avoid errors, while left error-related amygdala activation underpins detrimental negative affect.
response monitoring; reinforcement learning; emotion; amygdala; anterior cingulate cortex; antisaccade; errors; limbic system
The recognition of facial identity and expression are distinct tasks, with current models hypothesizing anatomic segregation of processing within a face-processing network. Using fMRI adaptation and a region-of-interest approach, we assessed how the perception of identity and expression changes in morphed stimuli affected the signal within this network, by contrasting (a) changes that crossed categorical boundaries of identity or expression with those that did not, and (b) changes that subjects perceived as causing identity or expression to change, versus changes that they perceived as not affecting the category of identity or expression. The occipital face area (OFA) was sensitive to any structural change in a face, whether it was identity or expression, but its signal did not correlate with whether subjects perceived a change or not. Both the fusiform face area (FFA) and the posterior superior temporal sulcus (pSTS) showed release from adaptation when subjects perceived a change in either identity or expression, although in the pSTS this effect only occurred when subjects were explicitly attending to expression. The middle superior temporal sulcus (mSTS) showed release from adaptation for expression only, and the precuneus for identity only. The data support models where the OFA is involved in the early perception of facial structure. However, evidence for a functional overlap in the FFA and pSTS, with both identity and expression signals in both areas, argues against a complete independence of identity and expression processing in these regions of the core face-processing network.
face perception; OFA; FFA; STS; adaptation; identity; expression; fMRI
The neurophysiological basis of variability in the latency of evoked neural responses has been of interest for decades. We describe a method to identify white matter pathways that may contribute to inter-individual variability in the timing of neural activity. We investigated the relation of the latency of peak visual responses in occipital cortex as measured by magnetoencephalography (MEG) to fractional anisotropy (FA) in the entire brain as measured with diffusion tensor imaging (DTI) in eight healthy young adults. This method makes no assumptions about the anatomy of white matter connections. Visual responses were evoked during a saccadic paradigm and were time-locked to arrival at a saccadic goal. The latency of the peak visual response was inversely related to FA in bilateral parietal and right lateral frontal white matter adjacent to cortical regions that modulate early visual responses. These relations suggest that biophysical properties of white matter affect the timing of early visual responses. This preliminary report demonstrates a non-invasive, unbiased method to relate the timing information from evoked-response experiments to the biophysical properties of white matter measured with DTI.
magnetoencephalography; diffusion tensor imaging; visual evoked potentials; saccades; white matter; frontal eye field
Current cognitive models suggest that the processing of dynamic facial attributes, including social signals such as gaze direction and facial expression, involves the superior temporal sulcus, whereas the processing of invariant facial structure such as the individuals’ identity involves the fusiform face area. Where facial attractiveness, a social signal that may emerge from invariant facial structure, is processed within this dual–route model of face perception is uncertain. Here, we present two studies. First, we investigated the explicit judgments of facial attractiveness and attractiveness-motivated behaviour in patients with acquired prosopagnosia, a deficit in familiar face recognition usually associated with damage to medial occipitotemporal cortex. We found that both abilities were impaired in these patients, with some weak residual ability for attractiveness judgments found only in those patients with unilateral right occipitotemporal or bilateral anterior temporal lesions. Importantly, deficits in attractiveness perception correlated with the severity of the face recognition deficit. Second, we performed a functional magnetic resonance imaging study in healthy subjects that included an implicit and explicit processing of facial attractiveness. We found increased neural activity when explicitly judging facial attractiveness within a number of cortical regions including the fusiform face area, but not the superior temporal sulcus, indicating a potential contribution of the fusiform face area to this judgment. Thus, converging neuropsychological and neuroimaging evidence points to a critical role of the inferior occipitotemporal cortex in the processing of facial attractiveness.
Aesthetic; Attraction; Face perception; Fusiform; Prosopagnosia; Temporal
To perform a saccadic response to a visual stimulus, a ‘sensorimotor transformation’ is required (i.e., transforming stimulus location into a motor command). Where in the brain is this accomplished? While previous monkey neurophysiology and human fMRI studies examined either parietal cortex or frontal eye field, we studied both of these regions simultaneously using magnetoencephalography (MEG). Nineteen healthy participants performed a pseudorandom series of prosaccades and antisaccades during MEG. Antisaccades require a saccade in the direction opposite a suddenly appearing stimulus. We exploited this dissociation between stimulus and saccadic direction to identify cortical regions that show early activity for a contralateral stimulus and late activity for a contralateral saccade. We found that in the left hemisphere both the intraparietal sulcus and the frontal eye field showed a pattern of activity consistent with sensorimotor transformation - a transition from activity reflecting the direction of the stimulus to that representing the saccadic goal. These findings suggest that sensorimotor transformation is the product of coordinated activity across the intraparietal sulcus and frontal eye field, key components of a cortical network for saccadic generation.
intraparietal sulcus; frontal eye field; antisaccade; saccade; magnetoencephalography; sensorimotor transformation
Autism spectrum disorders (ASD) are characterized by inflexible and repetitive behaviour. Response monitoring involves evaluating the consequences of behaviour and making adjustments to optimize outcomes. Deficiencies in this function, and abnormalities in the anterior cingulate cortex (ACC) on which it relies, have been reported as contributing factors to autistic disorders. We investigated whether ACC structure and function during response monitoring were associated with repetitive behaviour in ASD. We compared ACC activation to correct and erroneous antisaccades using rapid presentation event-related functional MRI in 14 control and ten ASD participants. Because response monitoring is the product of coordinated activity in ACC networks, we also examined the microstructural integrity of the white matter (WM) underlying this brain region using diffusion tensor imaging (DTI) measures of fractional anisotropy (FA) in 12 control and 12 adult ASD participants. ACC activation and FA were examined in relation to Autism Diagnostic Interview-Revised ratings of restricted and repetitive behaviour. Relative to controls, ASD participants: (i) made more antisaccade errors and responded more quickly on correct trials; (ii) showed reduced discrimination between error and correct responses in rostral ACC (rACC), which was primarily due to (iii) abnormally increased activation on correct trials and (iv) showed reduced FA in WM underlying ACC. Finally, in ASD (v) increased activation on correct trials and reduced FA in rACC WM were related to higher ratings of repetitive behaviour. These findings demonstrate functional and structural abnormalities of the ACC in ASD that may contribute to repetitive behaviour. rACC activity following errors is thought to reflect affective appraisal of the error. Thus, the hyperactive rACC response to correct trials can be interpreted as a misleading affective signal that something is awry, which may trigger repetitive attempts at correction. Another possible consequence of reduced affective discrimination between error and correct responses is that it might interfere with the reinforcement of responses that optimize outcomes. Furthermore, dysconnection of the ACC, as suggested by reduced FA, to regions involved in behavioural control might impair on-line modulations of response speed to optimize performance (i.e. speed-accuracy trade-off) and increase error likelihood. These findings suggest that in ASD, structural and functional abnormalities of the ACC compromise response monitoring and thereby contribute to behaviour that is rigid and repetitive rather than flexible and responsive to contingencies. Illuminating the mechanisms and clinical significance of abnormal response monitoring in ASD represents a fruitful avenue for further research.
autism; anterior cingulate cortex; response monitoring; functional MRI; diffusion tensor imaging