Elsevier

Neuroscience Research

Volume 48, Issue 2, February 2004, Pages 155-167
Neuroscience Research

Architecture of binocular disparity processing in monkey inferior temporal cortex

https://doi.org/10.1016/j.neures.2003.10.008Get rights and content

Abstract

Neurons in the inferior temporal (IT) cortex respond not only to the shape, color or texture of objects, but to the horizontal positional disparity of visual features in the right and left retinal images. IT neurons with similar shape selectivity cluster in columns. In this study, we examined how IT neurons are spatially arranged in the IT according to their selectivity for binocular disparity. With a single electrode, we simultaneously recorded extracellular action potentials from a single neuron and those from background multiple neurons at the same sites or recorded multineuronal responses at successive sites along electrode penetrations, while monkeys performed a fixation task. For neurons at each recording site, effective shapes were first determined from a set of 20 shapes presented at the zero-disparity plane. The most effective shape was then presented with varying amounts of disparity. Single neuron responses and background multiunit responses recorded at the same sites showed a similar ability of disparity discrimination and tended to share the preferred disparity, suggesting that neurons with similar disparity selectivity are clustered in the IT. We estimated from sequential recordings along electrode penetrations that the size of the neuronal clusters with similar disparity selectivity was smaller than the size of clusters with similar shape selectivity.

Introduction

Horizontal binocular disparity provides an important visual cue for the perception of depth and three-dimensional (3-D) scenes (Wheatstone, 1838). In the primate visual cortex, neurons selective for binocular disparity are found already in the first and lower cortical stages, V1, V2, and V3. In higher cortical processing stages, these neurons are found along the “dorsal” pathway, including the middle temporal area (MT), the medial superior temporal area and the posterior parietal cortex, and also along the “ventral” pathway in area V4 and the inferior temporal (IT) cortex (Hubel and Wiesel, 1970, Poggio and Fischer, 1977, Maunsell and Van Essen, 1983, Burkhalter and Van Essen, 1986, Felleman and Van Essen, 1987, Hubel and Livingstone, 1987, Poggio et al., 1988, Roy et al., 1992, Eifuku and Wurtz, 1999, Taira et al., 2000, Uka et al., 2000, Hinkle and Connor, 2001, Watanabe et al., 2002). In both area V4 and the IT, most disparity-selective neurons show position invariance of their disparity selectivity (Uka et al., 2000, Watanabe et al., 2002). The disparity preference of most disparity-selective IT neurons does not change depending on the stimulus shape (Uka et al., 2000). In addition to neurons sensitive to position-in-depth, area V4 contains neurons selective for bars oriented in depth (Hinkle and Connor, 2002), and the IT contains both neurons selective for particular 3-D surfaces defined by disparity gradients and curvature (Janssen et al., 2000, Janssen et al., 2001) and neurons selective for the shape of surfaces defined solely by disparity (Tanaka et al., 2001).

The degree of disparity tuning and the preferred range of disparity differ among neurons within each of the above-mentioned areas. Previous studies suggest that disparity-selective neurons are clustered according to these tuning properties. In cat and monkey V1, neurons show weak clustering based on disparity selectivity (Blakemore, 1970, LeVay and Voigt, 1988, Prince et al., 2002). In V2, disparity-selective neurons are found more abundantly in the thick cytochrome oxidase (CO) stripes than in the thin and pale stripes (Hubel and Livingstone, 1987, Peterhans and von der Heydt, 1993, Roe and Ts’o, 1995). It has been suggested that clustering of disparity-selective neurons in the thick stripes takes a columnar form (Roe and Ts’o, 1995, Ts’o et al., 2001). Area V3 is reported to consist of columns of neurons selective for similar disparities (Adams and Zeki, 2001). The most compelling evidence for columnar clustering of disparity-selective neurons comes from MT where neurons with similar sensitivity to disparity and preferred range of disparity are arrayed vertically across the cortical layers, and the preferred disparity gradually shifts in tangential direction across the cortical surface (DeAngelis and Newsome, 1999).

We have previously demonstrated that V4 neurons are clustered according to disparity discrimination ability and preferred disparity (Watanabe et al., 2002). Less is known about the spatial organization of disparity-selective neurons in the IT, except for evidence that disparity tuning curves are correlated between nearby IT neurons (Uka et al., 2000). In this study, we extended this previous finding by quantitatively comparing the disparity tuning curves, the ability of disparity discrimination, and the preferred range of disparity between a single neuron and its nearby multiple neurons in the IT. We also estimated the size of clusters of disparity-selective neurons by recording multi-neuronal responses at 0.2 mm intervals along electrode penetrations. Parts of these results have been previously reported in abstract form (Yoshiyama et al., 2000).

Section snippets

Materials and methods

The general procedures for surgery and animal care have been previously described in detail (Uka et al., 2000). All animal care and experimental procedures were performed in accordance with the NIH Guide for the Care and Use of Laboratory Animals and were approved by the animal experiment committee of Osaka University. Extracellular action potentials (“spikes”) were recorded from single neurons or a small group of neurons in the IT of five hemispheres in three male Japanese monkeys (Macaca

Recording site

Our recording chambers covered the posterolateral part of the inferior temporal cortex straddling or anterior to the posterior middle temporal sulcus (pmts) (shaded areas in Fig. 1). Within this area, recordings were made mostly from the posterior part of area TEd, and partly from area TEOd, the ventral bank of the superior temporal sulcus (sts), and the posterior part of area TEv (blackened areas). Because we did not observe obvious differences among the areas, we have combined the data and

Discussion

SU and MU responses recorded at the same site showed positive correlations in their disparity tuning curves and in their DDIs, and tended to share the preferred disparity. These results suggest that nearby neurons are similar in their selectivity for binocular disparity. Consecutive recordings at regular intervals along electrode penetrations indicate that neurons with similar disparity preference were clustered in local regions of 0.2–0.4 mm. Neurons in the IT are thus organized according to

Acknowledgements

This work was supported by grants to I.F. from Core Research for Evolutional Science and Technology (CREST) of the Japan Science and Technology Corporation, the Ministry of Education, Culture, Science, Sports and Technology (13308046 and 15016067), and Toyota Physical and Chemical Institute. We thank Seiji Tanabe for helpful comments on this manuscript, and Masayuki Watanabe for help in data analysis. K.Y. is grateful to Professors Masatoshi Takeda and Yoshiro Sugita for their continuous

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