Leslie G. Ungerleider

Object vision and spatial vision: two cortical pathways

Abstract Evidence is reviewed indicating that striate cortex in the monkey is the source of two multisynaptic corticocortical pathways. One courses ventrally, interconnecting the striate, prestriate, and inferior temporal areas, and enables the visual identification of objects. The other runs dorsally, interconnecting the striate, prestriate, and inferior parietal areas, and allows instead the visual location of objects. How the information carried in these two separate pathways is reintegrated has become an important question for future research.

Increased Activity in Human Visual Cortex during Directed Attention in the Absence of Visual Stimulation

When subjects direct attention to a particular location in a visual scene, responses in the visual cortex to stimuli presented at that location are enhanced, and the suppressive influences of nearby distractors are reduced. What is the top-down signal that modulates the response to an attended versus an unattended stimulus? Here, we demonstrate increased activity related to attention in the absence of visual stimulation in extrastriate cortex when subjects covertly directed attention to a peripheral location expecting the onset of visual stimuli. Frontal and parietal areas showed a stronger signal increase during this expectation than did visual areas. The increased activity in visual cortex in the absence of visual stimulation may reflect a top-down bias of neural signals in favor of the attended location, which derives from a fronto-parietal network.

The functional organization of human extrastriate cortex: a PET-rCBF study of selective attention to faces and locations

The functional dissociation of human extrastriate cortical processing streams for the perception of face identity and location was investigated in healthy men by measuring visual task-related changes in regional cerebral blood flow (rCBF) with positron emission tomography (PET) and H2(15)O. Separate scans were obtained while subjects performed face matching, location matching, or sensorimotor control tasks. The matching tasks used identical stimuli for some scans and stimuli of equivalent visual complexity for others. Face matching was associated with selective rCBF increases in the fusiform gyrus in occipital and occipitotemporal cortex bilaterally and in a right prefrontal area in the inferior frontal gyrus. Location matching was associated with selective rCBF increases in dorsal occipital, superior parietal, and intraparietal sulcus cortex bilaterally and in dorsal right premotor cortex. Decreases in rCBF, relative to the sensorimotor control task, were observed for both matching tasks in auditory, auditory association, somatosensory, and midcingulate cortex. These results suggest that, within a sensory modality, selective attention is associated with increased activity in those cortical areas that process the attended information but is not associated with decreased activity in areas that process unattended visual information. Selective attention to one sensory modality, on the other hand, is associated with decreased activity in cortical areas dedicated to processing input from other sensory modalities. Direct comparison of our results with those from other PET-rCBF studies of extrastriate cortex demonstrates agreement in the localization of cortical areas mediating face and location perception and dissociations between these areas and those mediating the perception of color and motion.

Neural processing of emotional faces requires attention

Attention gates the processing of stimuli relatively early in visual cortex. Yet, existing data suggest that emotional stimuli activate brain regions automatically, largely immune from attentional control. To resolve this puzzle, we used functional magnetic resonance imaging to first measure activation in regions that responded differentially to faces with emotional expressions (fearful and happy) compared with neutral faces. We then measured the modulation of these responses by attention, using a competing task with a high attentional load. Contrary to the prevailing view, all brain regions responding differentially to emotional faces, including the amygdala, did so only when sufficient attentional resources were available to process the faces. Thus, the processing of facial expression appears to be under top-down control.

Discrete Cortical Regions Associated with Knowledge of Color and Knowledge of Action

The areas of the brain that mediate knowledge about objects were investigated by measuring changes in regional cerebral blood flow (rCBF) using positron emission tomography (PET). Subjects generated words denoting colors and actions associated with static, achromatic line drawings of objects in one experiment, and with the written names of objects in a second experiment. In both studies, generation of color words selectively activated a region in the ventral temporal lobe just anterior to the area involved in the perception of color, whereas generation of action words activated a region in the middle temporal gyrus just anterior to the area involved in the perception of motion. These data suggest that object knowledge is organized as a distributed system in which the attributes of an object are stored close to the regions of the cortex that mediate perception of those attributes.

Distinct contribution of the cortico-striatal and cortico-cerebellar systems to motor skill learning

This review paper focuses on studies in healthy human subjects that examined the functional neuroanatomy and cerebral plasticity associated with the learning, consolidation and retention phases of motor skilled behaviors using modern brain imaging techniques. Evidence in support of a recent model proposed by Doyon and Ungerleider [Functional Anatomy of Motor Skill Learning. In: Squire LR, Schacter DL, editors. Neuropsychology of Memory. New York: Guilford Press, 2002.] is also discussed. The latter suggests that experience-dependent changes in the brain depend not only on the stage of learning, but also on whether subjects are required to learn a new sequence of movements (motor sequence learning) or learn to adapt to environmental perturbations (motor adaptation). This model proposes that the cortico-striatal and cortico-cerebellar systems contribute differentially to motor sequence learning and motor adaptation, respectively, and that this is most apparent during the slow learning phase (i.e. automatization) when subjects achieve asymptotic performance, as well as during reactivation of the new skilled behavior in the retention phase.

Organization of visual inputs to the inferior temporal and posterior parietal cortex in macaques

It has been proposed that visual information in the extrastriate cortex is conveyed along 2 major processing pathways, a “dorsal” pathway directed to the posterior parietal cortex, underlying spatial vision, and a “ventral” pathway directed to the inferior temporal cortex, underlying object vision. To determine the relative distributions of cells projecting to the 2 pathways, we injected the posterior parietal and inferior temporal cortex with different fluorescent tracers in 5 rhesus monkeys. The parietal injections included the ventral intraparietal (VIP) and lateral intraparietal (LIP) areas, and the temporal injections included the lateral portions of cytoarchitectonic areas TE and TEO. There was a remarkable segregation of cells projecting to the 2 systems. Inputs to the parietal cortex tended to arise either from areas that have been implicated in spatial or motion analysis or from peripheral field representations in the prestriate cortex. By contrast, inputs to the temporal cortex tended to arise from areas that have been implicated in form and color analysis or from central field representations. Cells projecting to the parietal cortex were found in visual area 2 (V2), but only in the far peripheral representations of both the upper and lower visual field. Likewise, labeled cells found in visual areas 3 (V3) and 4 (V4) were densest in their peripheral representations. Heavy accumulations of labeled cells were found in the dorsal parieto-occipital cortex, including the parieto-occipital (PO) area, part A of V3 (V3A), and the dorsal prelunate area (DP). In the superior temporal sulcus, cells were found within several motion-sensitive areas, including the middle temporal area (MT), the medial superior temporal area (MST), the fundus of the superior temporal area (FST), and the superior temporal polysensory area (STP), as well as within anterior portions of the sulcus whose organization is as yet poorly defined. Cells projecting to areas TE and TEO in the temporal cortex were located within cytoarchitectonic area TG at the temporal pole and cytoarchitectonic areas TF and TH on the parahippocampal gyrus, as well as in noninjected portions of area TE buried within the superior temporal sulcus. In the prestriate cortex, labeled cells were found in V2, V3, and V4, but, in contrast to the loci labeled after parietal injections, those labeled after temporal injections were concentrated in the foveal or central field representations. Although few double-labeled cells were seen, 2 regions containing intermingled parietal- and temporal-projection cells were area V4 and the cortex at the bottom of the anterior superior temporal sulcus.(ABSTRACT TRUNCATED AT 400 WORDS)

The neural systems that mediate human perceptual decision making

Perceptual decision making is the act of choosing one option or course of action from a set of alternatives on the basis of available sensory evidence. Thus, when we make such decisions, sensory information must be interpreted and translated into behaviour. Neurophysiological work in monkeys performing sensory discriminations, combined with computational modelling, has paved the way for neuroimaging studies that are aimed at understanding decision-related processes in the human brain. Here we review findings from human neuroimaging studies in conjunction with data analysis methods that can directly link decisions and signals in the human brain on a trial-by-trial basis. This leads to a new view about the neural basis of human perceptual decision-making processes.

The Effect of Face Inversion on Activity in Human Neural Systems for Face and Object Perception

The differential effect of stimulus inversion on face and object recognition suggests that inverted faces are processed by mechanisms for the perception of other objects rather than by face perception mechanisms. We investigated the face inversion using functional magnetic resonance imaging (fMRI). The principal effect of face inversion on was an increased response in ventral extrastriate regions that respond preferentially to another class of objects (houses). In contrast, house inversion did not produce a similar change in face-selective regions. Moreover, stimulus inversion had equivalent, minimal effects for faces in in face-selective regions and for houses in house-selective regions. The results suggest that the failure of face perception systems with inverted faces leads to the recruitment of processing resources in object perception systems, but this failure is not reflected by altered activity in face perception systems.

Contour, color and shape analysis beyond the striate cortex

The corticocortical pathway from striate cortex into the temporal lobe plays a crucial role in the visual recognition of objects. Anatomical studies indicate that this pathway is mainly organized as a serial hierarchy of multiple visual areas, including V1, V2, V3, V4, and inferior temporal cortex (IT). As expected from the anatomy, we have found that neurons in V4 and IT, like those in V1 and V2, are sensitive to many kinds of information relevant to object recognition. In the spatial domain, many V4 cells exhibit length, width, orientation, direction of motion and spatial frequency selectivity. In the spectral domain, many V4 cells are also tuned to wavelength. Thus, V4 is not specialized to analyze one particular attribute of a visual stimulus; rather, V4 appears to process both spatial and spectral information in parallel. A special contribution of V4 neurons to visual processing may lie in specific spatial and spectral interactions between their small excitatory receptive fields and large silent suppressive surrounds. Thus, although the excitatory receptive fields of V4 neurons are small, the responses of V4 neurons are influenced by stimuli throughout a much larger portion of the visual field. In IT, neurons also appear to process both spatial and spectral information throughout a large portion of the visual field. However, unlike V4 neurons, the excitatory receptive fields of IT neurons are very large. Many IT neurons, for example, are selective for the overall shape, color, or texture of a stimulus, anywhere within the central visual field. Together, these results suggest that within the areas of the occipito-temporal pathway, many different stimulus qualities are processed in parallel, but the type of analysis may become more global at each stage of processing.