Electrophysiological correlates of associative visual agnosia lesioned in the ventral pathway

Visual agnosia has been well studied by anatomical, neuropsychological and neuroimaging studies. However, functional changes in the brain have been rarely assessed by electrophysiological methods. We carried out electrophysiological examinations on a 23-year-old man with associative visual agnosia, prosopagnosia and cerebral achromatopsia to evaluate the higher brain dysfunctions of visual recognition. Electrophysiological methods consisted of achromatic, chromatic and category-specific visual evoked potentials (CS-VEPs), and event-related potentials (ERPs) with color and motion discrimination tasks. Brain magnetic resonance imaging revealed large white matter lesions in the bilateral temporo-occipital lobes involving the lingual and fusiform gyri (V4) and inferior longitudinal fasciculi due to multiple sclerosis. Examinations including CS-VEPs demonstrated dysfunctions of face and object perception while sparing semantic word perception after primary visual cortex (V1) in the ventral pathway. ERPs showed abnormal color perception in the ventral pathway with normal motion perception in the dorsal pathway. These electrophysiological findings were consistent with lesions in the ventral pathway that were detected by clinical and neuroimaging findings. Therefore, CS-VEPs and ERPs with color and motion discrimination tasks are useful methods for assessing the functional changes of visual recognition such as visual agnosia.     

Developmental deficits in social perception in autism: the role of the amygdala and fusiform face area

Autism is a severe developmental disorder marked by a triad of deficits, including impairments in reciprocal social interaction, delays in early language and communication, and the presence of restrictive, repetitive and stereotyped behaviors. In this review, it is argued that the search for the neurobiological bases of the autism spectrum disorders should focus on the social deficits, as they alone are specific to autism and they are likely to be most informative with respect to modeling the pathophysiology of the disorder. Many recent studies have documented the difficulties persons with an autism spectrum disorder have accurately perceiving facial identity and facial expressions. This behavioral literature on face perception abnormalities in autism is reviewed and integrated with the functional magnetic resonance imaging (fMRI) literature in this area, and a heuristic model of the pathophysiology of autism is presented. This model posits an early developmental failure in autism involving the amygdala, with a cascading influence on the development of cortical areas that mediate social perception in the visual domain, specifically the fusiform "face area" of the ventral temporal lobe. Moreover, there are now some provocative data to suggest that visual perceptual areas of the ventral temporal pathway are also involved in important ways in representations of the semantic attributes of people, social knowledge and social cognition. Social perception and social cognition are postulated as normally linked during development such that growth in social perceptual skills during childhood provides important scaffolding for social skill development. It is argued that the development of face perception and social cognitive skills are supported by the amygdala-fusiform system, and that deficits in this network are instrumental in causing autism.     

The neural bases of prosopagnosia and pure alexia: recent insights from functional neuroimaging

PURPOSE OF REVIEW: To discuss whether recent functional neuroimaging results can account for clinical phenomenology in visual associative agnosias. RECENT FINDINGS: Functional neuroimaging studies in healthy human subjects have identified only two regions of ventral occipitotemporal cortex that invariantly respond to individual faces and visual words, respectively. The signature of face identity coding in the fusiform neural response was shown to be missing in a patient with prosopagnosia. Another case study established that a surgical lesion close to the region sensitive to visual words can result in pure alexia. SUMMARY: Evidence is increasing that functional specialization for processing face identity and visual word forms is restricted to two specialized sensory modules in the occipitotemporal cortex. A structural or functional lesion to face-sensitive and word-sensitive regions in the ventral occipitotemporal cortex can provide the most parsimonious account for the clinical syndromes of prosopagnosia and agnosic alexia. This review suggests that functional specialization should be considered in terms of whether exclusively one brain region (instead of many) underpins a defined function and not as whether this brain region underpins exclusively one cognitive function. Such functional specialization seems to exist for at least two higher-order visual perceptual functions, face and word identification.     

Disorders of face perception and recognition

Face recognition is one of the most complex visual tasks performed by the human brain. Data from monkeys suggest that area IT may play a key role in identifying faces, and functional imaging research suggests that the human homologue of IT may be located in the medial occipitotemporal cortex, where a FFA has been located. Damage to medial occipitotemporal structures on the right or bilaterally leads to prosopagnosia, the failure to recognize facial identity. Prosopagnosia is not a single functional disorder but a family of dysfunctions, with different patients having different degrees of impairments to various perceptual and memory stages involved in face processing. Understanding the perceptual basis of this disorder and epiphenomena, such as covert recognition, is a goal of current research. Deficits in face perception also may contribute to Capgras syndrome and may be related to the impaired social development of patients with Asperger syndrome. More recently, identified deficits in face processing include the false recognition of unfamiliar faces and the impaired extraction of social information from faces, independent of the recognition of identity. Many of these prosopagnosia and other face processing deficits can be placed in the context of cognitive models of face processing stages, which are being refined continually by data from neurologic patients and functional imaging in normal subjects.     

Face identity recognition in autism spectrum disorders: a review of behavioral studies

Face recognition – the ability to recognize a person from their facial appearance – is essential for normal social interaction. Face recognition deficits have been implicated in the most common disorder of social interaction: autism. Here we ask: is face identity recognition in fact impaired in people with autism? Reviewing behavioral studies we find no strong evidence for a qualitative difference in how facial identity is processed between those with and without autism: markers of typical face identity recognition, such as the face inversion effect, seem to be present in people with autism. However, quantitatively – i.e., how well facial identity is remembered or discriminated – people with autism perform worse than typical individuals. This impairment is particularly clear in face memory and in face perception tasks in which a delay intervenes between sample and test, and less so in tasks with no memory demand. Although some evidence suggests that this deficit may be specific to faces, further evidence on this question is necessary.     

Visuomotor performance based on peripheral vision is impaired in the visual form agnostic patient DF

The perception-action model states that visual information is processed in different cortical areas depending on the purpose for which the information is acquired. Specifically, it was suggested that the ventral stream mediates visual perception, whereas the dorsal stream primarily processes visual information for the guidance of actions (Goodale & Milner, 1992). Evidence for the model comes from patient studies showing that patients with ventral stream damage (visual form agnosia) and patients with dorsal stream damage (optic ataxia) show divergent performance in action and perception tasks. Whereas DF, a patient suffering from visual form agnosia, was found to perform well in visuomotor tasks despite her inability to use vision for perceptual tasks, patients with optic ataxia show usually the opposite pattern, i.e. good perception but impaired visuomotor control. The finding that both disorders seem to provoke a mirror-reversed pattern of spared and impaired visual functions, led to the belief that optic ataxia and visual form agnosia can be considered as complementary disorders. However, the visuomotor performance of patients with optic ataxia is typically only impaired when they are tested in visual periphery while being often preserved when tested in central vision. Here, we show that DF's visuomotor performance is also only preserved when the target is presented centrally. Her reaching and grasping movements to targets in peripheral vision are abnormal. Our findings indicate that DF's visuomotor performance is quite similar to the visuomotor performance of patients with optic ataxia which undermines previous suggestions that the two disorders form a double-dissociation.     

Task-specific recruitment of dorsal and ventral visual areas during tactile perception

Many studies have found that visual cortical areas are active during tactile perception. Here we used positron emission tomographic (PET) scanning in normally sighted humans to show that extrastriate cortical regions are recruited in a task-specific manner during perceptual processing of tactile stimuli varying in two dimensions. Mental rotation of tactile Forms activated a focus around the anterior part of the left intraparietal sulcus. Since prior studies have reported activity nearby during mental rotation of visual stimuli, this focus appears to be associated with the dorsal visual (visuospatial) pathway. Discrimination between tactile Forms activated the right lateral occipital complex, an object-selective region in the ventral visual (visual Form) pathway. Thus, tactile tasks appear to recruit cortical regions that are active during corresponding visual tasks. Activation of these areas in both visual and tactile tasks could reflect visual imagery during tactile perception, activity in multisensory representations, or both.     

Neural representations of facial identity and its associative meaning

Since the discovery of "face cells" in the early 1980s, single-cell recording experiments in non-human primates have made significant contributions toward the elucidation of neural mechanisms underlying face perception and recognition. In this paper, we review the recent progress in face cell studies, including the recent remarkable findings of the face patches that are scattered around the anterior temporal cortical areas of monkeys. In particular, we focus on the neural representations of facial identity within these areas. The identification of faces requires both discrimination of facial identities and generalization across facial views. It has been indicated by some laboratories that the population of face cells found in the anterior ventral inferior temporal cortex of monkeys represent facial identity in a manner which is facial view-invariant. These findings suggest a relatively distributed representation that operates for facial identification. It has also been shown that certain individual neurons in the medial temporal lobe of humans represent view-invariant facial identity. This finding suggests a relatively sparse representation that may be employed for memory formation. Finally, we summarize our recent study, showing that the population of face cells in the anterior ventral inferior temporal cortex of monkeys that represent view-invariant facial identity, can also represent learned paired associations between an abstract picture and a particular facial identity, extending our understanding of the function of the anterior ventral inferior temporal cortex in the recognition of associative meanings of faces.     

Visual object and face processing in mild-to-moderate Alzheimer's disease: from segmentation to imagination

Little is known about the fate of higher level visual perception and visual mental imagery in the early stages of Alzheimer's disease (AD). In this study, we assessed these abilities in a group of mild-to-moderate AD patients using tasks selected to satisfy two main criteria. First, they have been shown to be sensitive to impairments of perception and imagery caused by other neurological conditions. Second, they test specific stages of visual perception and cognition in a reasonably selective manner. These stages were (in their normal order of occurrence during perception): the segmentation of different local points of the visual field into regions belonging to distinct objects; the representation of the shapes of these segmented regions in the image; the construction of more abstract shape representations that possess constancy over changes in size, location, orientation or illumination (assessed separately for faces and objects); the use of these perceived shape representations to access stored shape representations; and the access of lexical semantic representations from these high-level visual representations. Additional tasks tested the top-down activation of earlier visual representations from the semantic level in visual mental imagery. Our findings indicate small, but in most cases reliable, impairments in visual perception, which are independent of degree of cognitive decline. Deficits in basic shape processing influenced performance on some higher level visual tasks, but did not contribute to poor performance on face processing, or to the profound deficit on object naming. The latter of these is related to semantic-lexical impairment.     

A Data-Driven Functional Mapping of the Anterior Temporal Lobes

Although the anterior temporal lobe (ATL) comprises several anatomic and functional subdivisions, it is often reduced to a homogeneous theoretical entity, such as a domain-general convergence zone, or “hub,” for semantic information. Methodological limitations are largely to blame for the imprecise mapping of function to structure in the ATL. There are two major obstacles to using fMRI to identify the precise functional organization of the ATL: the difficult choice of stimuli and tasks to activate, and dissociate, specific regions within the ATL; and poor signal quality because of magnetic field distortions near the sinuses. To circumvent these difficulties, we developed a data-driven parcellation routine using resting-state fMRI data (24 females, 64 males) acquired using a sequence that was optimized to enhance signal in the ATL. Focusing on patterns of functional connectivity between each ATL voxel and the rest of the brain, we found that the ATL comprises at least 34 distinct functional parcels that are arranged into bands along the lateral and ventral cortical surfaces, extending from the posterior temporal lobes into the temporal poles. In addition, the anterior region of the fusiform gyrus, most often cited as the location of the semantic hub, was found to be part of a domain-specific network associated with face and social processing, rather than a domain-general semantic hub. These findings offer a fine-grained functional map of the ATL and offer an initial step toward using more precise language to describe the locations of functional responses in this heterogeneous region of human cortex.SIGNIFICANCE STATEMENT The functional role of the anterior aspects of the temporal lobes (ATL) is a contentious issue. While it is likely that different regions within the ATL subserve unique cognitive functions, most studies revert to vaguely referring to particular functional regions as “the ATL,” and, thus, the mapping of function to anatomy remains unclear. We used resting-state fMRI connectivity patterns between the ATL and the rest of the brain to reveal that the ATL comprises at least 34 distinct functional parcels that are organized into a three-level functional hierarchy. These results provide a detailed functional map of the anterior temporal lobes that can guide future research on how distinct regions within the ATL support diverse cognitive functions.     

Neural correlates of conscious and unconscious vision in parietal extinction

Brain areas activated by stimuli in the left visual field of a right parietal patient suffering from left visual extinction were identified using event-related functional magnetic resonance imaging. Left visual field stimuli that were extinguished from awareness still activated the ventral visual cortex, including areas in the damaged right hemisphere. An extinguished face stimulus on the left produced robust category-specific activation of the right fusiform face area. On trials where the left visual stimulus was consciously seen rather than extinguished, greater activity was found in the ventral visual cortex of the damaged hemisphere, and also in frontal and parietal areas of the intact hemisphere. These findings extend recent observations on visual extinction, suggesting distinct neural correlates for conscious and unconscious perception.     

Neural Correlates of Conscious and Unconscious Vision in Parietal Extinction

Brain areas activated by stimuli in the left visual field of a right parietal patient suffering from left visual extinction were identified using event-related functional magnetic resonance imaging. Left visual field stimuli that were extinguished from awareness still activated the ventral visual cortex, including areas in the damaged right hemisphere. An extinguished face stimulus on the left produced robust category-specific activation of the right fusiform face area. On trials where the left visual stimulus was consciously seen rather than extinguished, greater activity was found in the ventral visual cortex of the damaged hemisphere, and also in frontal and parietal areas of the intact hemisphere. These findings extend recent observations on visual extinction, suggesting distinct neural correlates for conscious and unconscious perception.     

Visual and auditory socio‐cognitive perception in unilateral temporal lobe epilepsy in children and adolescents: a prospective controlled study

Aim. A high rate of abnormal social behavioural traits or perceptual deficits is observed in children with unilateral temporal lobe epilepsy. In the present study, perception of auditory and visual social signals, carried by faces and voices, was evaluated in children or adolescents with temporal lobe epilepsy. Methods. We prospectively investigated a sample of 62 children with focal non‐idiopathic epilepsy early in the course of the disorder. The present analysis included 39 children with a confirmed diagnosis of temporal lobe epilepsy. Control participants (72), distributed across 10 age groups, served as a control group. Our socio‐perceptual evaluation protocol comprised three socio‐visual tasks (face identity, facial emotion and gaze direction recognition), two socio‐auditory tasks (voice identity and emotional prosody recognition), and three control tasks (lip reading, geometrical pattern and linguistic intonation recognition). All 39 patients also benefited from a neuropsychological examination. Results. As a group, children with temporal lobe epilepsy performed at a significantly lower level compared to the control group with regards to recognition of facial identity, direction of eye gaze, and emotional facial expressions. We found no relationship between the type of visual deficit and age at first seizure, duration of epilepsy, or the epilepsy‐affected cerebral hemisphere. Deficits in socio‐perceptual tasks could be found independently of the presence of deficits in visual or auditory episodic memory, visual non‐facial pattern processing (control tasks), or speech perception. A normal FSIQ did not exempt some of the patients from an underlying deficit in some of the socio‐perceptual tasks. Conclusion. Temporal lobe epilepsy not only impairs development of emotion recognition, but can also impair development of perception of other socio‐perceptual signals in children with or without intellectual deficiency. Prospective studies need to be designed to evaluate the results of appropriate re‐education programs in children presenting with deficits in social cue processing.     

A double dissociation between sensitivity to changes in object identity and object orientation in the ventral and dorsal visual streams: a human fMRI study

We used an event-related fMR-adaptation paradigm to investigate changes in BOLD activity in the dorsal and ventral visual streams as a function of object identity and object orientation. Participants viewed successive paired images of real-world, graspable objects, separated by a visual mask. The second image of each pair was either: (i) the same as the first image, (ii) different only in identity, (iii) different only in orientation, or (iv) different in both identity and orientation. A region in the parieto-occipital cortex (dorsal stream) showed a selective increase in BOLD activity with changes in object orientation, but was insensitive to changes in object identity. In contrast, a region in the temporo-occipital cortex (ventral stream) showed a selective increase in activity with changes in identity, but was insensitive to changes in orientation. The differential sensitivity to orientation and identity is consistent with the idea that the dorsal stream plays a critical role in the visual control of object-directed actions while the ventral stream plays a critical role in object perception.     

Hemispheric differences in neural systems for face working memory: A PET-rCBF study

Neural systems that participate in working memory for faces were investigated in an experiment designed to distinguish face perception areas from working memory areas. Regional cerebral blood flow (rCBF) was measured using positron emission tomography (PET) while subjects performed a sensorimotor control task, a face perception control task, and five working memory tasks with parametrically varied retention intervals, ranging from 1 to 21 sec. Striate and ventral occipitotemporal extrastriate areas demonstrated a simple negative correlation between rCBF and retention delay, indicating that these areas participate principally in perceptual operations performed during visual stimulation. By contrast, right and left frontal areas demonstrated rCBF increases that were significantly more sustained across delays than were increases in ventral extrastriate areas, but the relation between rCBF and retention interval differed significantly by hemisphere. Whereas right frontal rCBF showed a nonsignificant tendency to diminish at longer delays, left inferior frontal, middle frontal, and anterior cingulate cortex, as well as left parietal and inferior temporal cortex, demonstrated their largest rCBF increases at the longest delays. These results indicate that right frontal and left frontal, parietal, and temporal areas all participate in face working memory, but that left hemisphere areas are associated with a more durable working memory representation or strategy that subjects rely on increasingly with longer retention intervals. One possible explanation for this hemispheric difference is that left hemisphere activity is associated with a face representation that embodies the result of more analysis and elaboration, whereas right frontal activity is associated with a simpler, icon-like image of a face that is harder to maintain in working memory. © 1995 Wiley-Liss, Inc.     

Object-based and action-based visual perception in children with spina bifida and hydrocephalus.

Children with spina bifida and hydrocephalus (SBH) have long been known to have difficulties with visual perception. We studied how children with SBH perform 12 visual perception tasks requiring object identification, multistable representations of visual space, or visually guided overt actions. Four tasks required object-based processing (visual constancy illusions, face recognition, recognition of fragmented objects, line orientation). Four tasks required the representation of visual space in egocentric coordinates (stereopsis, visual figure-ground identification, perception of multistable figures, egocentric mental rotation). Four tasks required the coupling of visual space to overt movement (visual pursuit, figure drawing, visually guided route finding, visually guided route planning). Effect sizes, measuring the magnitude of the difference between SBH children and controls, were consistently larger for action-based than object-based visual perception tasks. Within action-based tasks, effect sizes were large and roughly comparable for tasks requiring the representation of visual space and for tasks requiring visually guided action. The results are discussed in terms of the physical and brain problems of children with SBH that limit their ability to build effective situation models of space.     

Dorsal‐movement and ventral‐form regions are functionally connected during visual‐speech recognition

Faces convey social information such as emotion and speech. Facial emotion processing is supported via interactions between dorsal‐movement and ventral‐form visual cortex regions. Here, we explored, for the first time, whether similar dorsal–ventral interactions (assessed via functional connectivity), might also exist for visual‐speech processing. We then examined whether altered dorsal–ventral connectivity is observed in adults with high‐functioning autism spectrum disorder (ASD), a disorder associated with impaired visual‐speech recognition. We acquired functional magnetic resonance imaging (fMRI) data with concurrent eye tracking in pairwise matched control and ASD participants. In both groups, dorsal‐movement regions in the visual motion area 5 (V5/MT) and the temporal visual speech area (TVSA) were functionally connected to ventral‐form regions (i.e., the occipital face area [OFA] and the fusiform face area [FFA]) during the recognition of visual speech, in contrast to the recognition of face identity. Notably, parts of this functional connectivity were decreased in the ASD group compared to the controls (i.e., right V5/MT—right OFA, left TVSA—left FFA). The results confirmed our hypothesis that functional connectivity between dorsal‐movement and ventral‐form regions exists during visual‐speech processing. Its partial dysfunction in ASD might contribute to difficulties in the recognition of dynamic face information relevant for successful face‐to‐face communication.     

Symptoms and lesion localization in visual agnosia]

There are two cortical visual processing streams, the ventral and dorsal stream. The ventral visual stream plays the major role in constructing our perceptual representation of the visual world and the objects within it. Disturbance of visual processing at any stage of the ventral stream could result in impairment of visual recognition. Thus we need systematic investigations to diagnose visual agnosia and its type. Two types of category-selective visual agnosia, prosopagnosia and landmark agnosia, are different from others in that patients could recognize a face as a face and buildings as buildings, but could not identify an individual person or building. Neuronal bases of prosopagnosia and landmark agnosia are distinct. Importance of the right fusiform gyrus for face recognition was confirmed by both clinical and neuroimaging studies. Landmark agnosia is related to lesions in the right parahippocampal gyrus. Enlarged lesions including both the right fusiform and parahippocampal gyri can result in prosopagnosia and landmark agnosia at the same time. Category non-selective visual agnosia is related to bilateral occipito-temporal lesions, which is in agreement with the results of neuroimaging studies that revealed activation of the bilateral occipito-temporal during object recognition tasks.     

The relationship between repetition suppression and face perception

Repetition of identical face stimuli leads to fMRI response attenuation (fMRI adaptation, fMRIa) in the core face-selective occipito-temporal visual cortical network, involving the bilateral fusiform face area (FFA) and the occipital face area (OFA). However, the functional relevance of fMRIa observed in these regions is unclear as of today. Therefore, here we aimed at investigating the relationship between fMRIa and face perception ability by measuring in the same human participants both the repetition-induced reduction of fMRI responses and identity discrimination performance outside the scanner for upright and inverted face stimuli. In the correlation analysis, the behavioral and fMRI results for the inverted faces were used as covariates to control for the individual differences in overall object perception ability and basic visual feature adaptation processes, respectively. The results revealed a significant positive correlation between the participants’ identity discrimination performance and the strength of fMRIa in the core face processing network, but not in the extrastriate body area (EBA). Furthermore, we found a strong correlation of the fMRIa between OFA and FFA and also between OFA and EBA, but not between FFA and EBA. These findings suggest that there is a face-selective component of the repetition-induced reduction of fMRI responses within the core face processing network, which reflects functionally relevant adaptation processes involved in face identity perception.