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  • Temporal Dynamics of Binocular Disparity Processing in the Central VisualPathway

    Michael D. Menz and Ralph D. FreemanGroup in Vision Science, School of Optometry, and Helen Wills Neuroscience Institute, University of California,Berkeley, California 94720-2020

    Submitted 13 June 2003; accepted in final form 29 October 2003

    Menz, Michael D. and Ralph D. Freeman. Temporal dynamics ofbinocular disparity processing in the central visual pathway. J Neu-rophysiol 91: 17821793, 2004. First published December 10, 2003;10.1152/jn.00571.2003. To solve the stereo correspondence problem(i.e., find the matching features of a visual scene in both eyes), it isadvantageous to combine information across spatial scales. The de-tails of how this is accomplished are not clear. Psychophysical studiesand mathematical models have suggested various types of interactionsacross spatial scale, including coarse to fine, fine to coarse, averaging,and population coding. In this study, we investigate dynamic changesin disparity tuning of simple and complex cells in the cats striatecortex over a short time span. We find that disparity frequencyincreases and disparity ranges decrease while optimal disparity re-mains constant, and this conforms to a coarse-to-fine mechanism. Weexplore the origin of this mechanism by examining the frequency andsize dynamics exhibited by binocular simple cells and neurons in thelateral geniculate nucleus (LGN). The results suggest a strong role fora feed-forward mechanism, which could originate in the retina. How-ever, we find that the dynamic changes seen in the disparity range ofsimple cells cannot be predicted from their left and right eye monoc-ular receptive field (RF) size changes. This discrepancy suggests thepossibility of a dynamic nonlinearity or disparity specific feedbackthat alters tuning or a combination of both mechanisms.

    I N T R O D U C T I O N

    Stereoscopic depth perception has been studied from theo-retical, behavioral, and neurophysiological perspectives. Mostbehavior work has been aimed at establishing empirical pa-rameters of stereoscopic function and performance levels.Early neurophysiological studies neglected mechanisms andassumed that cells with responses that changed with retinaldisparity of the stimulus were depth detectors. More recentphysiological work has included theoretical proposals thatwere tested experimentally. The result is a modified energymodel that accounts for basic features of the neural mechanismof stereopsis (e.g., Freeman and Ohzawa 1990; Ohzawa et al.1990; Qian and Andersen 1994; Qian et al. 1994).

    An early theoretical proposal was concerned with the corre-spondence problem in stereopsis (Marr and Poggio 1979). Thisrefers to the ambiguity of correspondence between left and rightimages that occurs from binocular viewing. The brain mustchoose the correct depth plane from several possible ones toprocess appropriate stereoscopic information. To solve this prob-lem, coarse scale disparity matches were proposed to occur first.This would be followed by fine scale matches (Marr and Poggio1979). In other words, a coarse-to-fine scaling process could beused to provide correct stereoscopic matching. Other theoretical

    ideas envisioned similar coarse scale disparity matches that werefollowed by fine scale adjustments (Anderson and Van Essen1987; Nishihara and Kimura 1987; Quam 1987).

    These theoretical notions have been explored in behavioralstudies. Sensitivity has been found to improve for line length,orientation, curvature and stereoscopic depth over a period of1 s (Watt 1987). The interpretation of these findings may bemade in terms of a coarse-to-fine temporal analysis of spatialfeatures. Another study was aimed at determining if differentspatial scales interact in stereopsis (Rohaly and Wilson 1993;Wilson et al. 1991). Diplopia threshold was determined at twoseparate spatial scales. Results suggested that coarse scaledisparity processing constrains that of fine levels within a givenrange. Two experiments were performed in another study inwhich spatially filtered targets were used. In one, temporalsequences were shown in which full-bandwidth targets werecompared with those in which selected frequencies were pre-sented first. In a second experiment, a human face was used ina similar way. Results of both experiments provide clear evi-dence for anisotropic temporal processing. Specifically, themost efficient perceptual processing occurs when spatial infor-mation is presented temporally in a low-to-high spatial fre-quency sequence. (Parker et al. 1997)

    Other psychophysical investigations of stereopsis suggest thatthere is also a fine-to-coarse process. In one study, an ambiguouscoarse scale stimulus was presented that could be perceived witheither crossed or uncrossed disparity. When a fine scale stimuluswas added, the ambiguity at coarse scale was removed, suggestinga fine-to-coarse disambiguation process (Smallman 1995). How-ever, this study also showed that a coarse scale stimulus coulddisambiguate that of a fine scale. Therefore results of the studysupport both coarse-to-fine and fine-to-coarse processes.

    Considered together, results of the behavioral studies sug-gest that both coarse-to-fine and fine-to-coarse processes mayapply to stereopsis. Surprisingly, until our recent study (Menzand Freeman 2003), no physiological data on this issue havebeen available. Neuronal temporal analysis on a fine time scalehas become possible with relatively recent techniques such asreverse correlation analysis (DeAngelis et al. 1993a,b; Free-man and Ohzawa 1990; Jones and Palmer 1987). Results oforientation (Ringach et al. 1997) and spatial frequency (Bred-feldt and Ringach 2002) tuning studies using this techniqueshow prominent changes as responses evolve over time. Thistype of information is important because it provides cluesabout neural circuitry. In ideal cases, for example, it may be

    Address for reprint requests and other requests: R. D. Freeman, 360 MinorHall, Berkeley, CA 94720-2020 (E-mail: [email protected]).

    The costs of publication of this article were defrayed in part by the paymentof page charges. The article must therefore be hereby marked advertisementin accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

    J Neurophysiol 91: 17821793, 2004.First published December 10, 2003; 10.1152/jn.00571.2003.

    1782 0022-3077/04 $5.00 Copyright 2004 The American Physiological Society www.jn.org

  • possible to obtain evidence consistent with feed-forward orfeedback models of visual processing.

    We have carried out a temporal analysis over a brief timescale (i.e., 40 ms) for a population of neurons in lateral genic-ulate nucleus (LGN) and visual cortex. In addition to deter-mining specific temporal features relevant to stereoscopic pro-cessing, our aim was to obtain information concerning thetheoretical proposal of a coarse-to-fine sequence as outlined inthe preceding text. Our results provide clear evidence that isconsistent with this hypothesis.

    M E T H O D S

    Experiments are conducted using anesthetized, paralyzed cats. Theequipment and procedures for surgery, animal maintenance, single-unit recording, receptive field (RF) mapping, and some data-analysistechniques have been described in detail in previous papers (e.g.,Anzai et al. 1999a,b). The description provided here emphasizesspecific procedures that are relevant to this study.

    Surgical procedures and animal maintenance

    Following standard preanesthetic procedures, isoflurane is used toanesthetize the animal. Femoral veins are cannulated, a tracheal tubeis placed, and a craniotomy and durotomy are performed (H-C P4 L2for visual cortex and A6 L8 for LGN). After surgery, thiopental isused to maintain anesthesia. Each animal is assessed individually todetermine an adequate level of anesthesia, which generally rangesfrom 1.52.5 mg kg1 h1. After anesthesia level is stabilized over1 h, a muscle relaxant (gallamine triethiodide, 10 mg kg1 h1) isused to prevent eye movements during visual stimulation. Pupils aredilated, nictitating membranes are retracted, and contact lenses with4-mm artificial pupils are positioned. A reversible direct ophthalmo-scope is used to image the optic discs on a tangent screen to inferareae centrales locations (Bishop et al. 1962). Core body temperature,electroencephalogram (EEG), electrocardiogram (ECG), heart rate,intratracheal pressure, and expired CO2 are all monitored continu-ously throughout each experiment.

    Recording procedure

    Visual stimuli are generated by a computer with two high-resolu-tion graphics boards that runs custom software as described previ-ously (DeAngelis et al. 1993a,b). To map cortical RFs, a dichopticone-dimensional binary m-sequence noise stimulus is used (Anzai etal. 1999a,b). A monocular stimulus is used for LGN cells. Sixteenlong adjacent bars are presented to each eye at optimal orientation(Fig. 1A). The width of the bars is approximately one-fourth the

    period of the optimal frequency. This square pattern is centered overthe RF. Each of the 16 bars is either bright or dark, and the back-ground is the mean luminance of the bars.

    Nonlinear binocular disparity tuning and monocular RFs are deter-mined simultaneously. Each spike train is cross-correlated with thestimulus sequence by means of a fast m-transform (Sutter 1991) toobtain space-time RF maps (Fig. 1B). This is repeated for all timedelays of interest (0200 ms) in increments of 5 ms to obtain aspace-time RF. A nonlinear binocular interaction map is obtained by

    FIG. 1. Method for obtaining disparity-tuning curves and monocular recep-tive fields. A: dichoptic m-sequence dense noise stimulus presented at optimalorientation for each eye. The binocular view field is a representation of thebinocular combination of stimuli with either bright bar