Timothy J. Andrews

Distinct representations for facial identity and changeable aspects of faces in the human temporal lobe

The neural system underlying face perception must represent the unchanging features of a face that specify identity, as well as the changeable aspects of a face that facilitate social communication. However, the way information about faces is represented in the brain remains controversial. In this study, we used fMR adaptation (the reduction in fMRI activity that follows the repeated presentation of identical images) to ask how different face- and object-selective regions of visual cortex contribute to specific aspects of face perception. We report that activity in the face-selective region of the fusiform gyrus (FG) was reduced following repeated presentations of the same face. Adaptation in this area was not sensitive to changes in image size, but was sensitive to changes in viewpoint. In contrast, face-selective regions in the superior temporal lobe failed to adapt to identical presentations of the same face, but showed an increased response when the same face was shown from different viewpoints and with different expressions. These results reveal a largely size-invariant neural representation in the inferior temporal lobe that could be involved in the recognition of facial identity, and a separate face-selective region in the superior temporal lobe that could be used to detect changeable aspects of faces. The absence of fMR-adaptation in object-selective regions of visual cortex challenges the idea that a more distributed network of areas is used to represent information about faces.

Correlated Size Variations in Human Visual Cortex, Lateral Geniculate Nucleus, and Optic Tract

We have examined several components of the human visual system to determine how the dimensions of the optic tract, lateral geniculate nucleus (LGN), and primary visual cortex (V1) vary within the same brain. Measurements were made of the cross-sectional area of the optic tract, the volumes of the magnocellular and parvocellular layers of the LGN, and the surface area and volume of V1 in one or both cerebral hemispheres of 15 neurologically normal human brains obtained at autopsy. Consistent with previous observations, there was a two- to threefold variation in the size of each of these visual components among the individuals studied. Importantly, this variation was coordinated within the visual system of any one individual. That is, a relatively large V1 was associated with a commensurately large LGN and optic tract, whereas a relatively small V1 was associated with a commensurately smaller LGN and optic tract. This relationship among the components of the human visual system indicates that the development of its different parts is interdependent. Such coordinated variation should generate substantial differences in visual ability among humans.

Idiosyncratic characteristics of saccadic eye movements when viewing different visual environments.

Eye position was recorded in different viewing conditions to assess whether the temporal and spatial characteristics of saccadic eye movements in different individuals are idiosyncratic. Our aim was to determine the degree to which oculomotor control is based on endogenous factors. A total of 15 naive subjects viewed five visual environments: (1) The absence of visual stimulation (i.e. a dark room); (2) a repetitive visual environment (i.e. simple textured patterns); (3) a complex natural scene; (4) a visual search task; and (5) reading text. Although differences in visual environment had significant effects on eye movements, idiosyncrasies were also apparent. For example, the mean fixation duration and size of an individuals saccadic eye movements when passively viewing a complex natural scene covaried significantly with those same parameters in the absence of visual stimulation and in a repetitive visual environment. In contrast, an individuals spatio-temporal characteristics of eye movements during active tasks such as reading text or visual search covaried together, but did not correlate with the pattern of eye movements detected when viewing a natural scene, simple patterns or in the dark. These idiosyncratic patterns of eye movements in normal viewing reveal an endogenous influence on oculomotor control. The independent covariance of eye movements during different visual tasks shows that saccadic eye movements during active tasks like reading or visual search differ from those engaged during the passive inspection of visual scenes.

Internal and External Features of the Face Are Represented Holistically in Face-Selective Regions of Visual Cortex

The perception and recognition of familiar faces depends critically on an analysis of the internal features of the face (eyes, nose, mouth). We therefore contrasted how information about the internal and external (hair, chin, face outline) features of familiar and unfamiliar faces is represented in face-selective regions. There was a significant response to both the internal and external features of the face when presented in isolation. However, the response to the internal features was greater than the response to the external features. There was significant adaptation to repeated images of either the internal or external features of the face in the fusiform face area (FFA). However, the magnitude of this adaptation was greater for the internal features of familiar faces. Next, we asked whether the internal features of the face are represented independently from the external features. There was a release from adaptation in the FFA to composite images in which the internal features were varied but the external features were unchanged, or when the internal features were unchanged but the external features varied, demonstrating a holistic response. Finally, we asked whether the holistic response to faces could be influenced by the context in which the face was presented. We found that adaptation was still evident to composite images in which the face was unchanged but body features were varied. Together, these findings show that although internal features are important in the neural representation of familiar faces, the faces internal and external features are represented holistically in face-selective regions of the human brain.

Differential sensitivity for viewpoint between familiar and unfamiliar faces in human visual cortex

People are extremely proficient at recognizing faces that are familiar to them, but are poor at identifying unfamiliar faces. We used fMR-adaptation to ask whether this difference in recognition might be reflected in the relative viewpoint-dependence of face-selective regions in the brain. A reduced response (adaptation) to repeated images of unfamiliar or familiar faces was found in the fusiform face area (FFA), but not in the superior temporal sulcus (STS) face-selective region. To establish if the neural representation of faces was invariant to changes in viewpoint, we parametrically varied the viewing angle of successive images using 3-dimensional models of unfamiliar and familiar faces. We found adaptation to familiar faces across all changes in viewpoint in the FFA. In contrast, a release from adaptation was apparent in the FFA when unfamiliar faces were viewed at increasing viewing angles. These results provide a neural basis for differences in the recognition of familiar and unfamiliar faces.

Intra- and interhemispheric connectivity between face-selective regions in the human brain.

Neuroimaging studies have revealed a number of regions in the human brain that respond to faces. However, the way these regions interact is a matter of current debate. The aim of this study was to use functional MRI to define face-selective regions in the human brain and then determine how these regions interact in a large population of subjects (n = 72). We found consistent face selectivity in the core face regions of the occipital and temporal lobes: the fusiform face area (FFA), occipital face area (OFA), and superior temporal sulcus (STS). Face selectivity extended into the intraparietal sulcus (IPS), precuneus (PCu), superior colliculus (SC), amygdala (AMG), and inferior frontal gyrus (IFG). We found evidence for significant functional connectivity between the core face-selective regions, particularly between the OFA and FFA. However, we found that the covariation in activity between corresponding face regions in different hemispheres (e.g., right and left FFA) was higher than between different face regions in the same hemisphere (e.g., right OFA and right FFA). Although functional connectivity was evident between regions in the core and extended network, there were significant differences in the magnitude of the connectivity between regions. Activity in the OFA and FFA were most correlated with the IPS, PCu, and SC. In contrast, activity in the STS was most correlated with the AMG and IFG. Correlations between the extended regions suggest strong functional connectivity between the IPS, PCu, and SC. In contrast, the IFG was only correlated with the AMG. This study reveals that interhemispheric as well as intrahemispheric connections play an important role in face perception.

An image-dependent representation of familiar and unfamiliar faces in the human ventral stream

People are extremely proficient at recognizing faces that are familiar to them, but are much worse at matching unfamiliar faces. We used fMR-adaptation to ask whether this difference in recognition might be reflected by an image-invariant representation for familiar faces in face-selective regions of the human ventral visual processing stream. Consistent with models of face processing, we found adaptation to repeated images of the same face image in the fusiform face area (FFA), but not in the superior-temporal face region (STS). To establish if the neural representation in the FFA was invariant to changes in view, we presented different images of the same face. Contrary to our hypothesis, we found that the response in the FFA to different images of the same person was the same as the response to images of different people. A group analysis showed a distributed pattern of adaptation to the same image of a face, which extended beyond the face-selective areas, including other regions of the ventral visual stream. However, this analysis failed to reveal any regions showing significant image-invariant adaptation. These results suggest that information about faces is represented in a distributed network using an image-dependent neural code.

Morphing between expressions dissociates continuous from categorical representations of facial expression in the human brain

Whether the brain represents facial expressions as perceptual continua or as emotion categories remains controversial. Here, we measured the neural response to morphed images to directly address how facial expressions of emotion are represented in the brain. We found that face-selective regions in the posterior superior temporal sulcus and the amygdala responded selectively to changes in facial expression, independent of changes in identity. We then asked whether the responses in these regions reflected categorical or continuous neural representations of facial expression. Participants viewed images from continua generated by morphing between faces posing different expressions such that the expression could be the same, could involve a physical change but convey the same emotion, or could differ by the same physical amount but be perceived as two different emotions. We found that the posterior superior temporal sulcus was equally sensitive to all changes in facial expression, consistent with a continuous representation. In contrast, the amygdala was only sensitive to changes in expression that altered the perceived emotion, demonstrating a more categorical representation. These results offer a resolution to the controversy about how facial expression is processed in the brain by showing that both continuous and categorical representations underlie our ability to extract this important social cue.

Binocular rivalry and visual awareness

Physiological studies of binocular rivalry have provided important clues to the relationship between neural activity in the brain and visual awareness. However, uncertainty about these insights has been raised by a recent study showing that the events underlying binocular rivalry occur earlier in the visual pathway than was previously thought.

Target-specific differences in the dendritic morphology and neuropeptide content of neurons in the rat SCG during development and aging

Our purpose in this work was to investigate the role of target tissues in the regulation of dendritic morphology from sympathetic neurons during development and aging. Neurons were retrogradely labeled from three targets, the iris, the submandibular gland (SMG), and the middle cerebral artery (MCA). They were then fixed and intracellularly injected to demonstrate their dendritic arborizations. Dendritic geometry varied quantitatively in sympathetic neurons innervating different target tissues at all stages of development. Neurons innervating the iris had the largest cell bodies and most extensive dendritic arborizations, whereas the vasomotor neurons were the smallest. The number of primary dendrites, however, did not vary significantly between the different neuronal populations.