RIKEN Brain Research Institute, Wako-shi, Saitama 351-0198, Japan
Address correspondence to Keiji Tanaka, RIKEN Brain Research Institute, Wako-shi, Saitama 351-0198, Japan. Email: keiji{at}postman.riken.go.jp.
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Abstract |
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Introduction |
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Area TE of the inferotemporal cortex represents the final purely visual stage of the occipitotemporal pathway, which is thought to be essential for visual object recognition. The occipitotemporal pathway starts at the primary visual cortex (V1) and leads to TE after relays at V2, V4 and TEO. Although skipping projections also exist, such as those from V2 to TEO and those from V4 to the posterior part of TE, the step-by-step projections are more numerous. TE projects to various polymodal brain sites, including the perirhinal cortex, the prefrontal cortex, the amygdala and the striatum of the basal ganglia. The projections to these targets are more numerous from TE, particularly from the anterior part of TE, than from the areas at earlier stages (Ungerleider et al., 1989; Yukie et al., 1990
; Barbas, 1992
; Suzuki and Amaral, 1995
). Therefore, there is a sequential cortical pathway from V1 to TE, and outputs from the pathway mainly originate from TE. In monkeys, bilateral TE ablation or complete deafferentation resulted in severe and selective deficits in learning tasks that required visual recognition of objects (Gross, 1973
; Dean, 1976
; Yaginuma et al., 1993
).
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Moderately Complex Features |
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Examples of the reduction in complexity of images for 12 TE cells are shown in Figure 1. The pictures to the left of the arrows are the original images of the most effective object stimuli and those to the right are the critical features determined after the reduction process. It should be noted that, even for the same object image, the directions of reduction and the final critical features were usually different from cell to cell. Some of the critical features were moderately complex shapes, while others were combinations of such shapes with color or texture. After determining the critical features for hundreds of cells in TE, we concluded that most cells in TE required moderately complex features for their maximal activation. The critical features for TE cells were more complex than just orientation, size, color or simple textures, which are known to be extracted and represented by cells in V1, but at the same time not sufficiently complex to represent the image of a natural object through the activity of single cells. The combined activation of multiple cells, which represent different features contained in the object image, is necessary.
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Faces and Other Extensively Learned Objects |
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There are suggestions that responses to whole objects will develop in TE if the subject is extensively trained in fine discrimination of similar objects. Logothetis and colleagues (Logothetis et al., 1995) trained adult monkeys to recognize wire-frame objects against many other similar wire-frame objects and recorded from cells in TE of the monkeys during the same task. About 20% of cells responded to wire-frame objects more strongly than to any other tested objects. Some of the neurons responded to parts of the objects as well as to the entire images of the objects, while others did not respond to parts of the objects (Logothetis, 1998
). Based on these results, it was proposed (Logothetis, 1998
) that some TE cells respond to whole objects which the subjects have used to conduct fine discriminations, while a majority of TE cells respond to features present in images of multiple different objects. However, this remains to be further studied, because the examination of selectivity described for object parts was rather preliminary (Logothetis, 1998
).
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Depth Structure |
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The horizontal disparity between images projected to the left and right eyes is a strong cue for perception of depth. Although it was once assumed that the selectivity for disparity is more predominant in the occipitoparietal (or dorsal visual) pathway, which is responsible for visuomotor control or spatial vision, than the occipitotemporal (or ventral visual) pathway, recent studies have shown that many cells in TE are selective to the disparity of stimuli, as well as their 2D shapes in the frontoparallel plane.
Uka et al. (Uka et al., 2000) recorded from TE cells in monkeys performing a fixation task and examined their responses to 2D shape stimuli presented at different depths. The depth was defined relative to that of the fixation point, as in other such experiments. Cells that responded to at least one of the 11 2D shapes at zero disparity were examined for disparity selectivity. Responses of more than one-half (63%) of the cells showed statistically significant dependency on disparity. Most of the disparity-selective cells were either near or far neurons according to the classification of Poggio and Fischer (Poggio and Fischer, 1977
). This is in contrast to the primary visual cortex and area MT, in which tuned excitatory cells constitute a large part (2/3 in V1 and 2/5 in MT) of the disparity-selective cells (Poggio and Fischer, 1977
; Maunsell and Van Essen, 1983
; Cumming and DeAngelis, 2001
).
The stimuli used by Uka et al. (Uka et al., 2000) were flat in the depth direction, i.e. there were no depth structures within their contours. Many objects in nature have surfaces tilted or curved in the depth direction and such depth gradient of the surface is an important feature of the object image. Janssen et al. (Janssen et al., 1999
, 2000a
,b
) used a stimulus set composed of stimuli having several different depth profiles in combination with several different 2D shapes. About one-half of the cells recorded from the ventral bank of the anterior part of the superior temporal sulcus exhibited selectivity for depth profile. Some of them responded to a linear gradient of depth, some to a combination of opposite linear gradients (or wedge profile) and others to a smooth concave or a convex depth curvature. They were selective for both 2D shape and depth profile. The selectivity for the depth profile was not explained by the selectivity for the depth position of a particular part of the stimulus, because the stimuli of the opposite depth profile did not activate the cells at any depth. The proportion of such cells was much lower (
10%) in the ventrolateral surface (i.e. area TE) than in the ventral bank of the superior temporal sulcus.
Because previous cytoarchitectural studies distinguished the ventral bank of the anterior part of the superior temporal sulcus (TEa and TEm) from the ventrolateral surface (TE) (Seltzer and Pandya, 1978), we have to consider the possibility that the two regions are functionally differentiated. However, H. Tanaka and I. Fujita (personal communication) found that cells in the ventral bank were as selective for complex 2D shapes as cells in TE. Moreover, the cells in the ventral bank were much more sensitive to the direction of the disparity gradient or curvature, e.g. concave versus convex, than the quantitative values of curvature or gradient (Janssen et al., 2000b
). Therefore, the responses of cells in the ventral bank of the superior temporal sulcus do not represent a full reconstruction of the 3D structure of the objects. Rather, it may be the case that the representation there is still mainly 2D and the qualitative information of disparity gradient or curvature just makes the 2D representation richer. It should be also noted that the representation of 2D shapes in TE may also not be fully quantitative. The number of features represented in TE may be limited by the number of TE columns (see the section entitled Columnar Organization in TE) and the invariance of responses of TE cells to certain types of shape deformations makes it difficult to reconstruct the input images from responses of TE cells (see next section). Only the features useful for discrimination of objects may be selectively represented in TE.
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Invariance of Responses |
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The effects of changes in stimulus size varied among cells (Tanaka et al., 1991; Ito et al., 1995
). Twenty-one percent of the TE cells tested responded to a size range of more than four octaves of the critical features with >50% maximum responses, whereas 43% responded to a size range of less than two octaves. TE cells with considerable invariance for the location and size of stimuli have also been found by Lueschow et al. and Logothetis et al. (Lueschow et al., 1994
; Logothetis et al., 1995
). The tuned cells may only function in the process of making invariant responses: those responding to various sizes of the same shape converge to a target cell to yield the size-invariant responses with sharp shape selectivity. Alternatively, both size-dependent and -independent processing of images may occur in TE.
A number of TE cells tolerated reversal of the contrast polarity of the shapes. Contrast reversal of the critical feature evoked >50% of the maximum responses in 40% of tested cells (Ito et al., 1994). Other workers (Sary et al., 1993
) found that some TE cells responded similarly to shapes defined by differences in luminosity, direction of motion of texture components and the coarseness of texture, while maintaining their selectivity for shape. Tanaka et al. (Tanaka et al., 2001
) found that about a quarter of TE cells responded similarly to shapes defined by difference in horizontal disparity of texture components, to those defined by differences in size of texture components and to those defined by differences in luminosity.
Another kind of invariance of TE cells was found with regards to the aspect ratio of shapes. The aspect ratio is the ratio of the size along one axis of the stimulus to that along the orthogonal axis. When an object rotates in depth, the features contained in the image change their shapes. Unless occlusion occurs, changes occur in the aspect ratio. For individual TE cells, we first determined the critical feature using the reduction method and then tested the effects of changes in the aspect ratio of the critical feature. We observed that 51% of cells responded to an aspect ratio range of more than three octaves with >50% of the maximum responses (Hossein and Tanaka, 1998).
In Figure 1 and our previous studies, we drew the features determined to be critical for the activation of individual TE cells as 2D images. However, this was for the sake of description and it does not necessarily mean that the cells were tuned to 2D images. Selectivity can only be defined in terms of a list of tested stimulus deformations and their associated response reductions. The above-described invariances of TE cells suggest that they are actually more sensitive to certain types of deformations than others. The types of deformations that often occur when an object moves around appear to be more tolerated. A related discussion has been presented elsewhere (Vogels et al., 2001
).
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Columnar Organization in TE |
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To determine the spatial extent of the clustering of cells with similar selectivities, we examined the responses of cells recorded successively along long penetrations vertical or oblique to the cortical surface (Fujita et al., 1992). The critical feature for a cell located at the middle of the penetration was first determined. A set of stimuli was then constructed, including the critical feature for the first cell, its rotated versions and ineffective control stimuli; cells recorded at different positions along the penetration were then tested with the fixed set of stimuli. As in the example shown in Figure 2
, cells recorded along the vertical penetrations commonly responded to the critical feature for the first cell or some related stimuli. The commonly responsive cells spanned nearly the entire cortical thickness from layers 2 to 6. In the case of penetrations that were made oblique to the cortical surface, however, the cells that were commonly responsive to the critical feature of the first cell or related stimuli were limited to within a short span around the first cell. The horizontal extent of the span was, on average, 400 µm. Cells outside the span did not respond to any of the stimuli included in the set, or responded to some stimuli that were not effective in activating the first cell and were included in the set as ineffective control stimuli. Based on these results, we proposed that TE is composed of columnar modules, in each of which cells respond to similar features (Fig. 3
).
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Spatial Arrangement of Columns |
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The partial overlapping of columns responding to different but related features was most clearly observed for faces presented in different views (Fig. 6). This experiment was also guided by a unit-recording experiment. We recorded five cells in one electrode penetration around the center of the imaged region; all of these cells selectively responded to faces. Three of them responded maximally to the front view of the face, whereas the remaining two responded to the profile, i.e. the lateral view of the face. In an optical imaging session, five different views of the face of the same doll were presented in combination with 14 non-face features. All of the faces evoked activation spots around the center of the illustrated 3 x 3 mm region. However, their center positions were slightly different. The contours of the dark spots are superimposed at the bottom. The activation spot moved in one direction as the face was rotated from the left profile to the right profile through the front view of the face. Individual spots were 0.40.8 mm in diameter and the overall region was 1.5 mm. These regions were not activated by the 14 non-face features. Similar results, namely selective activation by faces and systematic shift of the activation spot with the rotation of the face, were obtained for three other monkeys. In these three monkeys, optical imaging was not guided by unit recording. The recording chamber, with an inner diameter of 18 mm, was placed in the same part of TE and the face-selective activation was found at approximately the same location (approximately the posterior third of TE on the lateral surface, close to the lip of the superior temporal sulcus).
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The data for the non-face features are fewer, but I hypothesize that there are similar structures for representing non-face objects and I propose a modified model of the columnar organization of neurons in TE as shown in Figure 7. The borders between neighboring columns are not necessarily distinct. Instead, multiple columns that represent different but related features partially overlap with one another and as a whole compose a larger-scale unit. At least in some cases, some parameter of the features is continuously mapped along the cortical surface.
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Representation of Features and of Objects |
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Previously, the synchronization of spiking activity between cells was proposed as the mechanism for binding the features belonging to one object. Some experiments found a correspondence between cortical spike synchronization and perception of object borders (Singer, 1999), while others did not (Lamme and Spekreijse, 1998
). Another possible means of avoiding erroneous feature combination is to have features partially overlapping with one another (Mel and Fiser, 2000
). Suppose we are to represent four-letter strings. There will be an erroneous combination if we use only representation units coding single letters (e.g. ABCD is not discriminated from BADC, CDAB and so on, if units code A, B and C), while there will be no erroneous combinations if we use units specifying two consecutive letters and those specifying letters at the top and end of three consecutive letters (e.g. ABCD is the only four-letter string that contains AB, CD and A_C). The spatial relation between the units does not need to be represented.
Tsunoda et al. (Tsunoda et al., 2001) compared activation of the inferotemporal cortex by object images and activation by features included in the object images using a combination of optical imaging and single-cell recordings. The image of an object usually activated several spots within the imaged region (6 x 8 mm) and a feature contained in the object image activated a subset of the spots, as in the case shown in Figure 8A
. This result was consistent with the idea that different spots were activated by different features contained in the object image. However, activation by a feature often included new spots that had not been activated by the whole-object image, as illustrated in Figure 8B
. Single-cell recordings revealed that cells within such spots were activated by one feature while inhibited by another feature included in the object image. Previous single-cell recording studies had also shown that the response of inferotemporal cells to the optimal stimulus was suppressed by the simultaneous presentation of a second stimulus (Sato, 1989
, 1995
; Missal et al., 1997
, 1999
). These results indicate that the stimulus selectivity of inferotemporal columns should be described by both the simplest feature for maximum activation and the features that suppress activation. Even with the same optimal feature for excitation, the range of features that suppresses excitation can vary from column to column and probably also from cell to cell. This complexity of the overall stimulus selectivity of inferotemporal columns and cells may help to reduce the chance of erroneous detection of non-existing objects.
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Intrinsic Horizontal Connections within TE |
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Functions of TE Columns |
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Clusters of cells having overlapping and slightly differing selectivities may work together to confer object recognition abilities that are invariant to viewing conditions. Although single cells in TE tolerate some changes in size, contrast polarity and aspect ratio, these invariant properties at the single-cell level are not sufficient to explain the entire range of flexibility of object recognition. In particular, the responses of TE cells are generally selective for the orientation of the shape in the frontoparallel plane. Cells preferring different orientations and other parameters of the same 3D shape may be combined in a column to provide invariant outputs. Whether signals from these selective cells converge to a group of single cells that show invariant responses is a matter for further investigation. One possibility is that outputs of cells preferring different orientations, sizes, aspect ratios and contrast polarities of the same shape overlap in the target structure, thereby evoking the same effects. An anatomical study with an injection of anterograde tracer into a focal site in TE suggested that projections from TE to the ventrocaudal striatum of the basal ganglia exhibit this property (Cheng et al., 1997). Another possibility is that activation of cells is transmitted to other cells within a column and to nearby columns that represent related features through horizontal excitatory connections, in the presence of top-down signals from other brain sites, the prefrontal cortex for example. Multiple, but a limited number of, ways of activation transmission are hardwired in the network within a column and the arrangement of columns at nearby positions, and the top-down signals select one from them according to the behavioral context. Clusters of cells having overlapping and slightly differing selectivities may also serve to extract common features, but disregard differences between individual members in a category of objects when the system is directed to categorical object recognition.
Representation by multiple cells with overlapping selectivities can be more precise than a mere summation of representations by individual cells. A subtle change in a particular feature, which does not markedly change the activity of individual cells, can be coded by the differences in the activities of cells with overlapping and slightly different selectivities. Projections from the ventroanterior part of TE to the perirhinal cortex extensively diverge (Saleem and Tanaka, 1996). Projection terminals from a single site of ventroanterior TE cover
50% of the perirhinal cortex. This divergence in projections may distribute the subtle differences over a larger area of the perirhinal cortex, so that objects recognized at individual levels can be distinctively associated with other kinds of information. The subtle differences can also be emphasized by mutual inhibition between cells or nearby columns for winner-take-all-type selection. The inhibition may also be under the top-down control.
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