Dorsal-ventral integration in the recognition of motion-defined unfamiliar faces.

The primate visual system is organized into two parallel anatomical pathways, both originating in early visual areas but terminating in posterior parietal or inferior temporal regions. Classically, these two pathways have been thought to subserve spatial vision and visual guided actions (dorsal pathway) and object identification (ventral pathway). However, evidence is accumulating that dorsal visual areas may also represent many aspects of object shape in absence of demands for attention or action. Dorsal visual areas exhibit selectivity for three-dimensional cues of depth and are considered necessary for the extraction of surfaces from depth cues and can carry out cognitive functions with such cues as well. These results suggest that dorsal visual areas may participate in object recognition, but it is unclear to what capacity. Here, we tested whether three-dimensional structure-from-motion (SFM) cues, thought to be computed exclusively by dorsal stream mechanisms, are sufficient to drive complex object recognition. We then tested whether recognition of such stimuli relies on dorsal stream mechanisms alone, or whether dorsal-ventral integration is invoked. Results suggest that such cues are sufficient to drive unfamiliar face recognition in normal participants and that ventral stream areas are necessary for both identification and learning of unfamiliar faces from SFM cues.

Can anchor models explain inverted-U effects in facial judgments?

Researchers in a variety of disciplines have found that participants take less time and generate less diversity of responses when judging stimuli towards the ends of a scale than when judging those near the center. Three types of models, connectionist, exemplar, and anchor models, can account for these inverted-U effects. Anchor models assume that stimuli near the ends of the scale are used as anchors to compare with the other stimuli, implying that anchor representations are activated for each judgment. Therefore, participants should learn the anchors better than the other stimuli. Participants were 40 students from the Department of Psychology at McGill University (5 men; M age = 20.5 yr.; SD = 1.7). The experiment involved two tasks: first participants judged facial gender and then performed a recognition task. The results showed no correlation between the position on the gender scale and recognition accuracy. Several hypotheses were offered to explain these results.

Patchy organization and asymmetric distribution of the neural correlates of face processing in monkey inferotemporal cortex.

BACKGROUND: It is believed that a face-specific system exists within the primate ventral visual pathway that is separate from a domain-general nonface object coding system. In addition, it is believed that hemispheric asymmetry, which was long held to be a distinct feature of the human brain, can be found in the brains of other primates as well. We show here for the first time by way of a functional imaging technique that face- and object-selective neurons form spatially distinct clusters at the cellular level in monkey inferotemporal cortex. We have used a novel functional mapping technique that simultaneously generates two separate activity profiles by exploiting the differential time course of zif268 mRNA and protein expression. RESULTS: We show that neurons activated by face stimulation can be visualized at cellular resolution and distinguished from those activated by nonface complex objects. Our dual-activity maps of face and object selectivity show that face-selective patches of various sizes (mean, 22.30 mm2; std, 32.76 mm2) exist throughout the IT cortex in the context of a large expanse of cortical territory that is responsive to visual objects. CONCLUSIONS: These results add to recent findings that face-selective patches of various sizes exist throughout area IT and provide the first direct anatomical evidence at cellular resolution for a hemispheric asymmetry in favor of the right hemisphere. Together, our results support the notion that human and monkey brains share a similarity in both anatomical organization and distribution of function with respect to high-level visual processing.

Neuroanatomical, molecular genetic, and behavioral correlates of fragile X syndrome.

Fragile X syndrome (FXS) is a leading cause of inherited mental retardation. In the vast majority of cases, this X-linked disorder is due to a CGG expansion in the 5' untranslated region of the fmr-1 gene and the resulting decreased expression of its associated protein, FMRP. FXS is characterized by a number of cognitive, behavioral, anatomical, and biological abnormalities. FXS provides a unique opportunity to study the consequence of mutation in a single gene on the development and proper functioning of the CNS. The current focus on the role of FMRP in neuronal maturation makes it timely to assemble the extant information on how reduced expression of the fmr-1 gene leads to neuronal dysmorphology. The purpose of this review is to summarize recent genetic, neuroanatomical, and behavioral studies of fragile X syndrome and to offer potential mechanisms to account for the pleiotropic phenotype of this disorder.

Gene profiling of pooled single neuronal cell bodies from laser capture microdissected vervet monkey lateral geniculate nucleus hybridized to the Rhesus Macaque Genome Array.

This report is based on an ongoing study to examine gene expression differences in monkey lateral geniculate nucleus (LGN). Here, samples from an Old World species, the vervet monkey (Cercopithecus aethiops), were cross-hybridized to the Rhesus Macaque Genome Array (Affymetrix). Microarray analysis was performed using laser capture microdissected populations of individual neuronal cell bodies isolated from the LGN compared to heterogeneous samples from whole lamina. Our results indicated that cross-species hybridization of microdissected brain tissue samples from vervet monkeys to the Rhesus array produced reliable and biologically relevant data sets. We present the first list of genes enriched in the large neuronal cell bodies of the LGN. We found that these cell bodies are concentrated with genes involved in metabolic processes and protein synthesis, whereas signaling molecules including chemokines and integrins were expressed at higher levels within heterogeneous samples. Our data set also provides support for a contribution of Wnt signaling in adult monkey LGN.

Activity of common marmosets (Callithrix jacchus) in limited spaces: hand movement characteristics.

The increasing popularity of marmoset monkeys (Callithrix jacchus) in anatomical, behavioral, and electrophysiological studies has called for a detailed analysis of their natural behavior within limited spaces. In the present study, the authors analyzed hand movements during horizontal and vertical progressions in a cylinder. The trajectory of each hand covered the entire cylinder floor during horizontal progressions and the entire cylinder wall during vertical progressions. Different marmosets have different patterns of hand movement. The average maximum angle of hand movements for all marmosets during horizontal and vertical progressions oscillates, although the average over time is constant and similar for both hands, whereas head movements during horizontal progressions become smaller with successive progressions. Another observed difference between rats and monkeys was in the size of head and hand movements at the beginning of each experimental session. During the 1st horizontal progression, all marmosets moved their heads to a greater extent than their hands. This sequential head and hand movement is referred as bistable behavior. The bistable pattern of motor behavior, which was also observed in successive progressions, may be derived from an inherent fear of predators or exploratory interest of a novel environment.

Quantification of three-dimensional exploration in the cylinder test by the common marmoset (Callithrix jacchus).

The increasing trend in use of marmoset monkeys in behavioral studies has necessitated a greater understanding of their natural behavior, especially within confined spatial environments. One way to approach this issue is to examine locomotor and exploratory strategies using the cylinder test, as done recently for the rat by Gharbawie et al. [Gharbawie OA, Whishaw PA, Whishaw IQ. The topography of three-dimensional exploration: a new quantification of vertical and horizontal exploration, postural support, and exploratory bouts in the cylinder test. Behav Brain Res 2004;151:125-35]. We have used this paradigm in conjunction with Eshkol-Wachmann movement analysis in marmoset monkeys. We provide evidence that marmosets display systematic changes in both horizontal and vertical progressions during exploration. Quantitative analysis and comparison with the extant data in rats showed both similarities and differences. For example, both species display horizontal and vertical scanning movements, although the variability is considerably greater for the marmoset. The horizontal progressions consist of head scans, turning, and stepping. The amplitude of these progressions oscillates and decreases with trial duration. Vertical progressions, which consist of rears, head scans, and descent, also strongly oscillate but with constant mean amplitude during a trial. The difference between the two species is most evident in locomotor behavior. Rats use their forepaws primarily for postural support and follow forequarter movements while body weight shifts are generated by the hind limbs. Marmosets, however, can hold a vertical position without hand support and display more complex movement characteristics during exploration. The data from this study should be of use in designing experiments in which marmosets are engaged in free-roaming behavior within a confined space.

Representations of familiar and unfamiliar faces as revealed by viewpoint-aftereffects.

A viewpoint-dependent aftereffect occurs after prolonged viewing of a stimulus of a particular orientation, with the result that the test image is perceived to be facing away from the adapting orientation. Prior psychophysical work has led to the suggestion that the visual brain encodes a limited range of viewpoint information with regard to complex images. In this study, we investigated whether familiar faces were susceptible to a viewpoint aftereffect. Familiar faces are believed to be represented in a view-invariant manner, whereas unfamiliar faces are represented in a viewpoint-dependent manner. Adaptation to both familiar and unfamiliar faces influenced the perception of viewpoint of subsequent face images. However, category-specific transfer of a repulsive viewpoint-dependent aftereffect was observed with unfamiliar faces. Our results suggest that neural networks that mediate viewpoint information are also involved in view-invariant representation of familiar faces.

Monocular enucleation induces nuclear localization of calcium/calmodulin-dependent protein kinase IV in cortical interneurons of adult monkey area V1.

Elevation of intracellular Ca2+ levels activates calcium/calmodulin-dependent protein kinase (CaMK) IV, which in turn plays an important role in neuroprotection and neuroplasticity. The possibility that CaMKIV is similarly involved in neocortical tissue has not been examined previously, especially with regard to the plastic nature of ocular dominance features in the primary visual cortex (area V1). We addressed this question by way of monocular enucleation (ME) to disrupt sensory input and examine CaMKIV expression changes in monkey area V1. Immunohistochemical staining of area V1 in normal infants showed a nuclear presence of CaMKIV, which did not changed after ME. However, a striking set of layer- and time-dependent changes in nuclear CaMKIV expression was observed in adult area V1 after ME. A strong increase in nuclear CaMKIV levels was evident in cortical layers II/III and VI after 1 d of ME and in layer IVC after 5 d of ME. These specific laminar changes persisted after 30 d of ME and, most notably, showed a columnar profile in which CaMKIV expression was linked to open-eye columns. Real-time quantitative reverse transcription-PCR and Western blot analysis showed that total amounts of CaMKIV mRNA and protein remained unchanged after ME, suggesting that a nuclear translocation may occur from the cytoplasm. Finally, double-label immunohistochemical staining with a pyramidal cell marker (SMI-32) showed that CaMKIV was absent in this subtype, whereas coincidental expression with GABA, parvalbumin, and calretinin, but not calbindin, showed its clear presence in a subset of interneurons. We propose that CaMKIV activity within diverse groups of cortical interneurons may play an important role in adaptive plastic reorganization of adult neocortical tissue.

Cellular-resolution activity mapping of the brain using immediate-early gene expression.

Immediate-Early Genes are a class of genes that are rapidly up-regulated following neural stimulation. Due to their quality as potential activity markers in the CNS, they have been used extensively in functional mapping studies. At least three genes have been popularly used, including zif268 (Egr1, NGFI, Krox-24, or ZENK), c-fos and recently, Arc. A number of techniques have been developed in applying IEG labelling for the development of functional maps, thus overcoming some of the earlier limitations of this approach. Current developments highlight the future prospects of cellular-resolution functional activity mapping of the brain.

Reassessing the 3/4 view effect in face recognition.

It is generally accepted that unfamiliar faces are better recognized if presented in 3/4 view. A common interpretation of this result is that the 3/4 view represents a canonical view for faces. This article presents a critical review of this claim. Two kinds of advantage, in which a 3/4 view either generalizes better to a different view or produces better recognition in the same view, are discussed. Our analysis of the literature shows that the first effect almost invariably depended on different amounts of angular rotation that was present between learning and test views. The advantage usually vanished when angular rotation was equalized between conditions. Reports in favor of the second effect are scant and can be countered by studies reporting negative findings. To clarify this ambiguity, we conducted a recognition experiment. Subjects were trained and tested on the same three views (full-face, 3/4 and profile). The results showed no difference between the three view conditions. Our analysis of the literature, along with the new results, shows that the evidence for a 3/4 view advantage in both categories is weak at best. We suggest that a better predictor of performance for recognition in different views is the angular difference between learning and test views. For recognition in the same view, there may be a wide range of views whose effectiveness is comparable to the 3/4 view.

The influence of attention on holistic face encoding.

We examined the influence of attention on the formation of holistic face representations using the composite effect (Perception 16 (1987) 747). In Experiment 1, stimuli composed of a face superimposed on a house were shown during encoding. Subjects delineated either the face or the house, thus manipulating attention away or toward the face. In Experiment 2, an intact face image was presented with letters scrolling from top to bottom. Subjects were asked to either ignore the letters or read them and decipher the words that they formed. Aligned and misaligned composites were shown at testing. Recognition performance was consistently better for misaligned than aligned stimuli, regardless of the allocation of attention during encoding. In Experiment 3, we show that the composite effect can be eliminated by a disruption in holistic processing at the time of encoding. We conclude that holistic encoding is one aspect of face analysis that occurs equally well with or without attention.

Differential induction and decay curves of c-fos and zif268 revealed through dual activity maps.

The use of inducible transcription factors for mapping neural activity is now a common procedure. We have previously developed a double-labelling technique that allows visualization of activated neurons after two different stimulation sequences. The technique exploits the differential time course of mRNA versus protein expression of transcription factors. However, the precise details of the differential time course remained unknown. Here, we provide a complete up- and downregulation profile for both the c-fos and zif268 genes, as determined through combined in situ hybridization and immunocytochemical detection of the mRNA and protein products in primary visual cortex. The data presented here can be used in the design of future studies employing double-label mapping of neural activation following a compound stimulus.

Face recognition is affected by similarity in spatial frequency range to a greater degree than within-category object recognition.

Previous studies have suggested that face identification is more sensitive to variations in spatial frequency content than object recognition, but none have compared how sensitive the 2 processes are to variations in spatial frequency overlap (SFO). The authors tested face and object matching accuracy under varying SFO conditions. Their results showed that object recognition was more robust to SFO variations than face recognition and that the vulnerability of faces was not due to reliance on configural processing. They suggest that variations in sensitivity to SFO help explain the vulnerability of face recognition to changes in image format and the lack of a middle-frequency advantage in object recognition.

Task-dependent transfer of perceptual to memory representations during delayed spatial frequency discrimination.

Discrimination thresholds were obtained using a delayed spatial frequency discrimination task. In Experiment 1, we found that presentation of a mask 3 s before onset of a reference Gabor patch caused a selective, spatial frequency dependent interference in a subsequent discrimination task. However, a 10 s interval abolished this masking effect. In Experiment 2, the mask was associated with a second spatial frequency discrimination task so that a representation of the mask had to be coded into short-term perceptual memory. This experiment was performed to assess whether absence of masking in the 10 s condition of Experiment 1 might be due to decay of the mask information in the perceptual or the memory representational domain. The presence of this second discrimination task now caused similar interference effects on the primary discrimination task at both the 3 s and 10 s interstimulus intervals (ISI) conditions. Finally, to test the robustness of the masking effect, the nature of the secondary masking task was changed from a spatial frequency discrimination task to an orientation discrimination task in Experiment 3. The masking effect was now abolished in both the 3 and 10 s ISI conditions. Together, the results from these experiments are consistent with the idea of a two-level perceptual memory mechanism. The results also suggest that stimulus representations during a perceptual discrimination task are shared between the perceptual and memory representation domains in a task-dependent manner.

Face recognition with perspective transformation.

The effect of perspective transformation on transfer of face training was investigated in a yes/no recognition task using face stimuli with 42 degrees, 10 degrees, or no perspective convergence. A strong dependence of recognition performance on the magnitude of perspective transformation was found, with large perspective changes such as from 42 degrees at learning to orthogonal at test producing the strongest impairment and small perspective changes such as from 10 degrees at learning to orthogonal at test the least. In a second experiment, the internal and external features of a face from different perspective convergence were artificially combined to produce identical local features between this composite image and the original but producing an impossible perspective transformation from either. The results of transfer between the composite and untouched images showed face recognition to be strongly affected by local featural similarities and relatively insensitive to global coherence of perspective transformation.

Face recognition is robust with incongruent image resolution: relationship to security video images.

Identifying a criminal captured on conventional security video typically requires matching poor-quality video footage against a high-quality photograph. The authors examined the consequence of such a large discrepancy in image quality. Recognition and matching performance of this incongruent-quality condition was compared with that of a congruent one, in which a high-quality photograph was reduced to a low-quality video. Recognition memory was little affected by this manipulation, whereas matching performance of the incongruent condition enjoyed occasional advantage. The results show that person identification can tolerate a large discrepancy between image qualities of matching stimuli when one of the images is of poor quality.

Associating neural alterations and genotype in autism and fragile x syndrome: incorporating perceptual phenotypes in causal modeling.

We have previously described (see companion paper, this issue) the utility of using perceptual signatures for defining and dissociating condition-specific neural functioning underlying early visual processes in autism and FXS. These perceptually-driven hypotheses are based on differential performance evidenced only at the earliest stages of visual information processing, mediated by local neural network functioning. In this paper, we first review how most large-scale neural models are unable to address atypical low-level perceptual functioning in autism, and then suggest how condition-specific, local neural endophenotypes (described in our companion paper) can be incorporated into causal models to infer target candidate gene or gene clusters that are implicated in autism's pathogenesis. The usefulness of such a translational research approach is discussed.

Using perceptual signatures to define and dissociate condition-specific neural etiology: autism and fragile X syndrome as model conditions.

The functional link between genetic alteration and behavioral end-state is rarely straightforward and never linear. Cases where neurodevelopmental conditions defined by a distinct genetic etiology share behavioral phenotypes are exemplary, as is the case for autism and Fragile X Syndrome (FXS). In this paper and its companion paper, we propose a method for assessing the functional link between genotype and neural alteration across these target conditions by comparing their perceptual signatures. In the present paper, we discuss how such signatures can be used to (1) define and differentiate various aspects of neural functioning in autism and FXS, and subsequently, (2) to infer candidate causal (genetic) mechanisms based on such signatures (see companion paper, this issue).

Whole-brain expression analysis of FMRP in adult monkey and its relationship to cognitive deficits in fragile X syndrome.

Fragile X syndrome (FXS) is one of the most prevalent forms of heritable mental retardation and developmental delay in males. The syndrome is caused by the silencing of a single gene (fragile X mental retardation-1; FMR1) and the lack of expression of its protein product (fragile X mental retardation-1 protein; FMRP). Recent work has linked the high expression levels of FMRP in the magnocellular layers of lateral geniculate nucleus (M-LGN) of the visual system to a specific reduction of perceptual function known to be mediated by that neural structure. This finding has given rise to the intriguing notion that FMRP expression level may be used as an index of susceptibility of specific brain regions to the observed perceptual and cognitive deficits in FXS. We undertook a comprehensive expression profiling study of FMRP in the monkey to obtain further insight into the link between FMPR expression and the behavioural impact of its loss in FXS. We report here the first 3D whole-brain map of FMRP expression in the Old-World monkey and show that certain brain structures display high FMRP levels, such as the cerebellum, striatum, and temporal lobe structures. This finding provides support for the notion that FMRP expression loss is linked to behavioural and cognitive impairment associated with these structures. We argue that whole-brain FMRP expression mapping may be used to formulate and test new hypotheses about other forms of impairments in FXS that were not specifically examined in this study.