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‘What’ and ‘where’ in the human brain

Leslie G Ungerleider and James V Haxby

National Institute of Mental Health, Bethesda, USA

Multiple visual areas in the cortex of nonhuman primates are organized

into two hierarchically organized and functionally specialized processing
pathways, a ‘ventral stream’ for object vision and a ‘dorsal stream’ for spatial
vision. Recent findings from positron emission tomography activation studies
have localized these pathways within the human brain, yielding insights into
cortical hierarchies, specialization of function, and attentional mechanisms.

Current Opinion in Neurobiology 1994, 4:157-l 65

Introduction: visual processing streams in in [3]). In contrast, posterior parietal lesions do not
nonhuman primates affect visual discrimination performance; but instead
cause severe deficits in visuospatial performance (for
Vision is by far the most richly represented sen- review, see 131). Physiological evidence also supports
sory modality in the cortex of nonhuman primates. this distinction, as neurons in areas (or modules of ar-
Anatomical and physiological studies of Old World eas) along the occipitotemporal cortical pathway (areas
monkeys have revealed at least thirty separate visual Vl, V2, V4, and inferior temporal areas TEO and TE)
cortical areas, occupying about one-half of the total respond selectively to visual features relevant to ob-
cortex [1,2]. As shown in Fig. 1, these areas appear ject identification (i.e. ‘what’), such as color and shape,
to be organized into two functionally specialized pro- whereas neurons in areas (or modules of areas) along
cessing pathways, each having the striate cortex as the occipitoparietal cortical pathway (areas Vl, V2, V3,
the source of in&al input [3,41. The occipitotemporal middle temporal area (MT), medial superior temporal
pathway, or ‘ventral stream’, is crucial for the visual area (MST), and further stations in inferior parietal and
identification of objects, whereas the occipitoparietal superior temporal sulcal cortex) respond selectively to
pathway, or ‘dorsal stream’, is crucial for appreciating spatial aspects of stimuli (i.e. ‘where’), such as direc-
the spatial relationships among objects, as well as for tion of motion and velocity, as well as to tracking eye
the visual guidance of movements toward objects in movements (for reviews, see [1,81). Recent connection-
space. ist models have suggested that there may be computa-
tional advantages to segregate these ‘what’ and ‘where’
Recently, Young [5*1 has analyzed the connectional functions into separate anatomical pathways [9,101.
topology for extrastriate cortical areas of Old World
monkeys using multidimensional scaling, and has con- Although it had been proposed that the occipitotem-
firmed the segregation of these areas into dorsal and poral and occipitoparietal pathways are the cortical ex-
ventral processing streams - with limited cross-talk tensions of separate subcortical ‘parve and ‘magno-’
between them. Multiple visual areas in the cortex of processing systems [ill, there is now considerable ev-
New World monkeys appear co be similarly organized idence that this is not the case. Although it is true
into separate dorsal and ventral streams 161, suggest- that the input to the occipitoparietal pathway derives
ing a common primate plan that probably extends to mainly from cells in the magnocellular layers of the lat-
the organization of the human visual cortex as well. In eral geniculate nucleus, the input to the occipitotempo-
this review, we will examine the results of recent work ral pathway derives from cells in both the magnocellu-
aimed at addressing this idea. lar and parvocellular layers (for review, see [12**1).
The original evidence for separate processing streams
for object vision and spatial vision was the contrast-
ing effects of inferior temporal and posterior parietal
lesions in monkeys. Lesions of inferior temporal car- Hieiarchical organization of visual cortical areas
tex cause severe deficits in performance on a wide va-
riety of visual discrimination tasks (e.g. pattern, object, Areas along both the occipitotemporal and occipi-
color) 171,but not on visuospatial tasks (e.g. visually toparietal pathways are organized hierarchically, such
guided reaching and judging which of two identical that low-level inputs are transformed into more use-
objects is located closer to a visual landmark; reviewed ful representations through successive stages of pro-

MRI-magnetic resonance imaging; MST-medial superior temporal area; MT-middle temporal area;
PET-positron emission tomography; rCBF-regional cerebral blood flow.

0 Current Biology Ltd ISSN 0959-4388 157

158 Cognitive neuroscience


Rostra1 STS

t I

Fig. 1. Summary diagram of the visual cortical hierarchy. Solid lines indicate connections originating from both central and peripheral field
representations, whereas dotted lines indicate connections restricted to peripheral field representations. Solid arrowheads indicate feedforward
connections, open arrowheads indicate feedbackconnections, and reciprocal solid arrowheads indicate intermediate-type connections. The
diagram demonstrates the divergence in the flow of visual information into ventral and dorsal streams directed toward the inferior temporal
(TE) and inferior parietal (PC) cortex, respectively, and possible sites for interaction between the two within the rostra1 superior temporal
sulcus (STS) [SSI. Reproduced with permission from 186.1.

cessing. As one proceeds from one area to the next, tive field size increase steadily, and neuronal response
both neuronal response latencies and average recep- properties become increasingly complex. Along the oc-
What’ and ‘where’ in the human brain Ungerleider and Haxby. 159

,-ipitotemporal pathway, for example, whereas many or spatial relations (e.g. geographic directions) are also
VI cells function as local spatiotemporal filters, V2 dissociable following temporal and parietal lesions 1441.
cells may respond to ‘virtual’ or illusory contours of
Recently, Goodale, Milner and colleagues [45-47,48*1
figures [I31, some V4 cells respond only if a stimu-
have proposed that the ventral and dorsal streams,
lus stands out from its background on the basis of a
rather than mediating ‘what it is’ versus ‘where it is’,
difference in color or form 114,151, and inferior tempo-
are best understood as subserving the perception of
ral cells respond selectively to global or overall object
objects versus the control of skilled actions directed
features, such as shape 116181, with a small proportion
toward those objects. It should be pointed out that,
being specialized for faces (117,19-211; for reviews, see
in its original formulation, the what and where model
[22,23]). Similarly, as one proceeds from Vl to MT, to
acknowledged the importance of the parietal cortex for
MST, and thence to areas in parietal cortex, new types
mediating visually guided reaching 131.However, what
of directional selectivity emerge. For example, whereas
was central to the model was that, in the perceptual
cells in Vl are sensitive to the direction of motion of
domain, parietal damage produces visuospatial rather
the Fourier components of a complex pattern, many
than object-recognition impairments.
MT cells are sensitive to the global motion of the pat-
tern, that is, the vector sum of the component motions Nonetheless, Goodale and Milner 145-47,48’1 have ar-
[24]. Within MST, many cells are selective for rotation or gued, largely on the basis of a single case, patient D.F.,
for the expansion/contraction of the image of any ob- that separate object vision and spatial vision pathways
ject moving in depth 125,261, and whereas such motion cannot explain the ability of this patient to-use the size
selectivity has also been reported for parietal neurons, and orientation of objects to appropriately control her
these neurons demonstrate even more complex spatial visually guided grasping movements, despite her pro-
properties 127,281. found inability to describe or recognize these same
Thus, much of the neural mechanism for both object vi- features of the object. What is the evidence, how-
sion and spatial vision can be viewed as a ‘bottom-up’ ever, that parietal cortex is mediating these visually
process subserved by feedforward projections between guided movements? According to Goodale and Mil-
successive pairs of areas within a pathway. Anatomical ner 145,46,48*1, patient D.F. suffered an anoxic epi-
studies have shown, however, that each of these feed- sode from carbon monoxide poisoning, resulting in
forward projections is reciprocated by a feedback pro- diffuse brain damage, which was most apparent in
jection [1,21. Projections from higher-order processing cortical areas 18 and 19. These areas are the source
stations back to lower-order ones could mediate some of visual input to parietal, as well as temporal, cor-
‘top-down’ aspects of visual processing, such as the in- tex. Thus, it is not at all clear which brain regions
fluence of selective attention. It has also been proposed are mediating patient D.E’s intact abilities. They may
that feedback, or re-entrant, projections could mediate even be subcortical. The crucial question is whether
perceptual completion effects or perceptual binding of patients with parietal damage demonstrate visuospatial
stimulus attributes [29,30,31*1. impairments that cannot be attributed to a primary vi-
suomotor defect. The answer is clearly yes. In a recent
review summarizing the results of testing 67 patients
with focal parietal lesions confirmed with magnetic res-
onance imaging (MRI), von Cramon and Kerkhoff 149’1
The effects of focal brain lesions in humans reported that the patients had impaired perception of
horizontal and vertical axes, poor length and distance
The differential visual impairments produced by focal estimation, a deficit in orientation discrimination, as
lesions in clinical cases suggest that human visual cor- well as a deficit in position matching. Furthermore,
tex, like that of the monkey, may be similarly organized there was some evidence that impaired perception of
into two anatomically distinct and functionally special- axes and angles was more closely associated with an-
ized pathways: the ventral and dorsal streams 132-371. terior parietal damage, whereas impaired perception
In the most recent of these studies, for example, a of position and distance was more closely assoicated
double dissociation of visual recognition (face percep- with posterior parietal damage. Thus, although visu-
tion camouflaged by shadows) and visuospatial perfor- ospatial deficits may be accompanied by visuomotor
mance (stylus maze learning) was demonstrated in two impairments, they are not explained by them.
men with lesions of occipitotemporal and occipitopari-
eta1 cortex, respectively - confirmed by postmortem
examination 1371. The specific clinical syndromes pro-
duced by occipitotemporal lesions include visual ob-
ject agnosia, prosopagnosia, and achromatopsia (for PET-rCBF studies of dorsal and ventral streams
reviews, see 138,391), whereas those produced by oc- in human cortex
cipitoparietal lesions include optic ataxia (misreach-
ing>, visuospatial neglect, constructional apraxia, gaze By measuring local hemodynamic changes associated
apraxia, akinotopsia, and disorders of spatial cogni- with specific visual processes, functional brain imag-
tion (see e.g. 140-421; reviewed in 1431). Interestingly, ing makes it possible to map the organization of hu-
imagery disorders involving descriptions of either ob- man extrastriate cortex with far greater precision than
jects (especially faces, animals, and colors of objects) is possible with human lesion studies, and without the
160 Coenitive neuroscience

confounding influence of compensatory responses to to-sample task have been corroborated in two recent
brain injury. In experiments designed to investigate the studies of visuospatial processing, one of which em-
possible existence of separate object vision and spatial ployed a spatial attention task 152**1 and the other
vision pathways in humans, changes in regional cere- of which employed a spatial working memory task
bral blood flow GCBF) were measured using positron 153’1. Similarly, the locations of occipitotemporal foci
emission tomography (PET) while subjects performed activated during face perception have also been cor-
object identity and spatial location matching-to-sample roborated (154”l; see below).
tasks 150,51’1. In the object identity task, the subject
indicated which of the two (choice) faces matched
the sample face, whereas in the spatial location task,
the subject indicated which of two (choice) stimuli
contained a small square (or a dot) in the same lo- Hierarchical organization of face processing in
cation, relative to a double line, as the small square the ventral stream
(or dot) in the sample stimulus. For some conditions,
the small squares contained faces, such that identical Having identified dorsal and ventral processing streams
stimuli were used for face and location matching, with in human cortex, it is possible to use different experi-
only the task requirements changing. mental paradigms to explore the functional specializa-
The results identified specific occipitotemporal and oc- tion of areas within them. For example, whereas multi-
cipitoparietal regions associated with face and location ple regions within occipitotemporal and ventral tempo-
matching, respectively, and specific posterior occipital ral cortex are activated during ‘face’ tasks, the locations
regions associated with both visual functions (Fig. 2). of these activations are task dependent. As shown in
Within the occipitotemporal cortex, areas in the poste- Fig. 2, identification based on facial features, as in face
rior and mid-fusiform gyrus (Brodmann areas 19 and matching 150,5I*l or gender discrimination 154”1, acti-
37) were selectively activated by the face-matching vates the posterior fusiform gyrus, whereas identifica-
task 151.1. Within occipitoparietal cortex, areas in the tion of a unique individual’s face activates the mid-fusi-
dorsolateral occipital cortex (Brodmann area 191, su- form gyrus, and retrieving knowledge about an individ-
perior parietal cortex, and the cortex near the fun- ual, such as in naming the individual’s profession, acti-
dus of the intraparietal sulcus (both Brodmann area vates even more anterior regions in the parahippocam-
7) were selectively activated by the location-match- pal gyrus, midtemporal gyrus, and temporal pole 154”l.
ing task 151.1. In addition, regions in right inferior These results suggest a hierachical organization as one
prefrontal (Brodmann areas 45 and 47) and right dorsal proceeds from posterior to anterior extrastriate areas in
premotor (Brodmann area 6) cortex were activated se- the ventral stream. Posteriorly, facial features appear to
lectively by face- and location-matching, respectively be extracted in order to construct, in more anterior re-
(JV Haxby, unpublished data). These findings, thus, gions, a unique representation of a face. Yet more ante-
indicate the existence in humans, as in monkeys, of riorly, this representation can be associated and stored
two functionally specialized and anatomically segre- with knowledge about that individual. This hierarchi-
gated visual processing pathways and further suggest cal scheme, derived from PET studies, fits well with the
the extensions of each into the frontal lobe. As shown clinical literature on the kinds of face-recognition im-
in Fig. 2, the locations of the occipitoparietal and pre- pairments produced by selective temporal lobe lesions
motor foci activated by the spatial location matching- 1551.

Fig. 2. Cortical regions in human dorsal

and ventral streams selectively activated
by perception of location or faces, as
demonstrated by increased rCBF, meas-
ured with PET. The two top diagrams
depict the left and right lateral views of
each of the two cortical hemispheres, and
the two bottom diagrams represent the
left and right ventral views. Numbers in
symbols indicate the study reporting each
activated focus: 1 - face and location
matching-to-sample ([51*]; JV Haxby, un-
published data); 2a - gender discrimi-
nation [54**]; 2b -face identity [54**];
3 - shifting attention to spatial locations
[52**]; and 4 - spatial working memory
0 Face [53*]. In some instances, multiple nearby
Location foci are shown as a single focus, repre-
4 19’34 Current Opinion in Neurobiology
senting their center of gravity.
‘What’ and ‘where’ in the human brain Ungerleider and Haxby 161

Areas MT and V4 in the human brain? evidence for the hypothesis that this region is the hu-
man homologue of area MT. It should be pointed out,
In the monkey, a major route by which visual informa- however, that, in addition to MT, the monkey contains
tion is transmitted to inferior temporal cortex is via area numerous areas in parietal cortex and the superior tem-
V4, whereas a major route to inferior parietal cortex is poral sulcus that are selective for motion, and some of
via area MT, also known as area V5 (Fig. 1). PET studies these areas (e.g. area MST) are also heavily myelinated
have indicated the locations of possible homologues of [25,26,66,671. Thus, the identification of the homologue
these areas in the human brain. of MT in human cortex remains tentative.

Area MT Area V4
tiea MT in the monkey is characterized by a high pro- Area V4 in the monkey contains neurons selective for
portion of neurons selective for the direction of visual many different features relevant for object recogni-
motion [561. In Old World monkeys, the area is located tion, including color and shape [14,15,68,69’1. In Old
on the lateral bank and floor of the caudal superior World monkeys, the area is located dorsally in the
temporal sulcus, whereas in New World monkeys it is hemisphere (mainly on the prelunate gyrus), where
located in the middle part of the temporal lobe; in both the lower visual field is represented, and it extends
Old and New World monkeys, it is distinguished from ventrally into occipitotemporal cortex, where the up-
surrounding areas by heavy myelination (e.g. i57-611). per visual field is represented 1701. On the basis of
anatomical connections and receptive field properties,
PET studies have identified a region within the lateral
it has been proposed that the homologous area in New
occipitotemporoparietal cortex of humans that is selec-
World monkeys is DL, the dorsolateral area 171,721.
tively activated by the perception of motion [62,63,64**1
(Fig. 3). A det ai 1e d stu dy of the neuroanatomical loca- The perception of color in humans has been associated
tion of this area in 12 subjects, mapped onto structural with activation of a ventromedial occipital area (in the
MRI scans, showed that it is consistently located in the collateral sulcus or lingual gyrus) in three separate PET
ascending limb of the inferior temporal sulcus [64**1. studies [62,63,731 (Fig. 3). Because V4 contains color-
It has recently been reported that visual activation of selective cells, it has been speculated that this area is
presumably the same region can be detected using the homologue of V4 163,741. The location of this area
functional MRI (RBH Tootell, KK Kwong, JW Bel- agrees well with the location of lesions associated with
liveau, JR Baker, CE Stern, et al., Sot Neurosci Abstr achromatopsia [751, and is close but medial to the pos-
1993, 19:1500). Importantly, in this study, low con- terior fusiform area activated by faces (compare Figs.
trast stimuli were as effective as high contrast stimuli 2 and 3). That these color- and face-selective areas are
in activating the area, just as one would predict if the close to each other, but not identical, is supported by
area were MT, as the inputs to this area are derived recent studies of evoked potentials measured on the
from the magnocellular layers of the lateral geniculate cortical surface in presurgical epilepsy patients [76,771.
nucleus. Finally, a postmortem study of human brain The proximity of color- and face-selective areas would
has identified a heavily myelinated zone in the lateral explain the frequent association of achromatopsia with
occipitotemporoparietal cortex [651, providing further prosopagnosia 175,781.

Fig. 3. Human extrastriate cortical regions

(identified by PET-rCBF studies) associ-
ated with the perception of color, shape,
and motion. The two top diagrams de-
pict the left and right lateral views of
each of the two cortical hemispheres,
and the two bottom diagrams represent
the left and right ventral views. Numbers
in symbols indicate the study reporting
each activated focus: 1 - selective at-
tention to color, shape, and velocity [62];
Motion 2 - passive perception of color and mo-
tion [63]; and 3 - passive perception of
Color motion [64**]. In some instances, multi-
Shape ple nearby foci are shown as a single fo-
31994 Current Ooinion in Neurobdoev cus, representing their center of gravity.
162 Coenitive neuroscience

What is the evidence that the color-selective area in hu- streams for processing object identity and spatial lo-
mans is the homologue of monkey area V4? If it were, cation information. There is emerging evidence for
then the area should also be activated by shape, like hierarchical processing and functional specialization
V4 neurons. Of the two PET studies examining color within these two streams, although this work is still in
and shape, one found that shape perception also ac- an early stage and homologies with cortical areas in the
tivated this ventromedial occipitotemporal region 1621, monkey remain tentative. It is clear, however, that pro-
but the other did not 1731. Even more troublesome is cessing within extrastriate areas is strongly modulated
the finding of additional color-selective foci in lateral by selective attention, as it is in the monkey. Although
occipital cortex [621(Fig. 3). But perhaps the most brain imaging cannot reveal the workings of the cor-
compelling evidence against the idea that these ar- tex at the level of individual neurons, it can be used to
eas are homologous comes from the different effects test hypotheses generated by work in animals and to
of lesions. V4 lesions in monkeys do not produce the advance into areas of cognition that are unique to the
profound and permanent color impairment that is seen human brain.
in patients with achromatopsia (179,80,81*1; reviewed
in 182’1). Moreover, V4 lesions produce significant im-
pairments in form perception (180,81*,831; R Desimone,
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