The Multiple Roles of Visual Cortical Areas MT/MST in Remembering the Direction of Visual Motion

James W. Bisley1 and Tatiana Pasternak

Department of Neurobiology & Anatomy and Center for Visual Science, University of Rochester, Rochester, NY 14642, USA


    Abstract
 Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Notes
 References
 
Although the role of cortical areas MT and MST (MT/MST) in the processing of directional motion information is well established, little is known about the way these areas contribute to the execution of complex behavioral tasks requiring the use of such information. We tested monkeys with unilateral lesions of these areas on a visual working memory task in which motion signals not only had to be encoded, but also stored for brief periods of time and then retrieved. The monkeys compared the directions of motion of two random-dot stimuli, sample and test, separated by a temporal delay. By increasing the temporal delay and spatially separating the two stimuli, placing one in the affected visual field and the other in the intact visual field, we were able to assess the contribution of MT/MST to specific components of the task: encoding (sample), retention (delay) and encoding/retrieval/comparison (test). We found that the effects of MT/MST lesions on specific components depended upon the demands of the task and the nature of the visual motion stimuli. Whenever stimuli consisted of random dots moving in a broad range of directions, MT/MST lesions appeared to affect encoding. Furthermore, when the lesions affected encoding of the sample, retention of the direction of stimulus motion was also affected. However, when the stimulus was coherent and the emphasis of the task was on the comparison of small direction differences, the absence of MT/MST had major impact on the retrieval/comparison component of the task and not on encoding or storage.


    Introduction
 Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Notes
 References
 
Eye movements limit the brain's view of a visual scene to a series of disconnected samples. To maintain continuity of visual experience, features of the visual scene, such as the direction of motion of an object or its orientation, must be related across these temporal gaps. Thus, the ability to store visual information for brief periods is fundamental to the successful execution of visually guided behaviors.

Although the neural encoding of directional signals has been extensively studied, little is known about the storage of this information or about the cortical areas involved. Area MT, one of the more extensively studied extrastriate areas in monkey cortex, has been shown to be central to the processing of visual motion. Single-unit recordings have established that the majority of neurons in this area are directionally selective (Zeki, 1974Go; Maunsell and Van Essen, 1983Go; Albright, 1984Go), perform integration of local motion signals (Movshon et al., 1985Go; Rodman and Albright, 1989Go), and discriminate motion direction in the presence of noise with nearly the same sensitivity as monkeys and humans (Britten et al., 1992Go; Celebrini and Newsome, 1994Go). Moreover, Newsome and colleagues have shown that the perceptual decisions of monkeys performing psychophysical tasks can be biased by stimulating MT or area MST with low currents during the presentation of the visual stimulus (Salzman et al., 1992Go; Celebrini and Newsome, 1995Go). Lesion studies have also provided evidence that these areas play an important role in the perception of direction and speed of visual motion (Newsome and Paré, 1988Go; Schiller, 1993Go; Pasternak and Merigan, 1994Go; Orban et al., 1995Go; Rudolph and Pasternak, 1999Go).

In this study, we tested monkeys with unilateral lesions of areas MT and MST (MT/MST) on a complex visual discrimination task that required the monkeys not only to process information about the direction of stimulus motion, but also to briefly store this information for subsequent retrieval. This allowed us to examine both the contribution of MT/MST to encoding of visual motion signals and their possible role in the short-term storage of these signals.


    Materials and Methods
 Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Notes
 References
 
Subjects

Two young adult male monkeys (Macaca nemestrina), weighing 8–10 kg, were used in the study. On weekdays, water was restricted for a period of 22 h before testing and their daily water ration, in the form of fruit juice, was provided during the behavioral testing. On weekends, the monkeys were not tested behaviorally and received 100 ml/kg water per day. Food was continually available in the home cage and monkeys received supplements of fresh fruit and vitamins daily. Body weights were measured three times a week to ensure good health and normal growth. Monkeys also had scleral search coils and head restraint devices implanted to monitor their eye position. Prior to the present study, these monkeys were tested on a variety of visual discrimination tasks involving random dots and grating stimuli. The results of these measurements have been published elsewhere (Rudolph and Pasternak, 1999Go). Experiments were carried out in accordance with the guidelines published in the NIH Guide for the Care and Use of Laboratory Animals (NIH publication no. 86-23, revised 1987).

Lesions

Ibotenic acid lesions were made using procedures similar to those reported by Pasternak and Merigan (Pasternak and Merigan, 1994Go). Ibotenic acid (10 mg/ml) was injected at multiple sites along the superior temporal sulcus (STS) in one hemisphere. Placement of the injections was guided by magnetic resonance images (MRIs) taken prior to surgery and by direct visualization of the STS. Each injection (1.5 8ml) was made with a Hamilton syringe with ~2.5 mm separation at several depths at each location. Both monkeys received injections into the right hemisphere (monkey 1, 90 injections; monkey 2, 73 injections). The extent of the lesions was examined three ways: by MRI several months after surgery, by psychophysical mapping and by histology. The lesions were performed ~2 years prior to the initiation of this study. During this 2 year period the monkeys were tested on the tasks used in this study but only at a 0.2 s delay. The results of these experiments have been recently reported (Rudolph and Pasternak, 1999Go). Data for this study were acquired following the completion of these measurements.

Magnetic Resonance Imaging

Prior to placing the lesions, the brains were scanned on 2 and 1.5 T GE magnets. T2-weighted images with high signal-to-noise ratios were obtained with a small surface coil. Coronal and horizontal scans were performed with the following parameters: TE/TR 5000/90 or 3000/85; 1.5 mm thick slices 0.2 mm apart; 256 x 256 array; field of view 10 or 15 cm. This method provided sufficient gray matter/white matter contrast to visualize many of the anatomical details and the location and extent of the ibotenic acid lesions. The images were examined and analyzed with NIH Image software.

For this procedure, the monkeys were anaesthetized with sodium pentobarbitol (25 mg/kg i.v.), placed in a specially constructed MRI-compatible stereotaxic frame, intubated and continuously monitored by ECG. The ear bars were filled with water or vitamin E, which was visible on the MR images. This allowed the determination of stereotaxic coordinates in the Horsley–Clark coordinate system.

Histology

At the conclusion of behavioral testing, the monkeys were deeply anesthetized with an overdose of barbiturate and perfused with a saline rinse followed by 4% paraformaldehyde fixative solution. Two rinses of 10% and 30% sucrose solution were used to remove excess fixative and to help cryoprotect the tissue. The brain was removed, blocked and sectioned at a thickness of 50 mm with a freezing microtome. Triplets of adjacent sections at intervals of ~0.5 mm were stained for cytochrome oxidase (Wong-Riley, 1979Go), myelin (Gallyas, 1979Go) and with cresyl violet. Sections through the lesion were traced on computer to identify the regions affected by the ibotenic acid.

Stimuli and Behavioral Procedures

Random Dot Stimuli

We used a match-to-sample paradigm in which the monkeys viewed two stimuli, sample and test, separated by a temporal delay. Stimuli were generated online by a Macintosh computer and displayed on a 17 in. Nanao monitor that was placed 42 cm in front of the monkey. The random dot stimuli were identical to those used previously (Pasternak et al., 1990Go; Pasternak and Merigan, 1994Go; Rudolph and Pasternak, 1999Go) and consisted of dots placed randomly within a circular aperture, 3° or 4° in diameter. Each dot was displaced by a constant step size within a given temporal interval (13 ms) and the direction of motion for each dot was randomly chosen from a specified uniform distribution of directions. Three types of random-dot motion stimuli were used. Direction range stimulus: in each frame, the dots moved independently in any direction chosen at random from a uniform distribution that could range from 0° (all dots moving in parallel) to 360° (only random motion). For example, when the range of directions was 90° and the mean direction was rightwards (Fig. 1AGo, left), the dots appeared to flow towards the right. Motion signal stimulus: in each frame a set proportion of randomly selected dots (the % signal) was displaced in a single direction (i.e. the dots moved coherently) while the others were displaced in random directions (Fig. 1AGo, middle). Coherent motion stimulus: all of the dots were displaced in the same direction (Fig. 1AGo, right).



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Figure 1. Visual stimuli and the behavioral task. (A) Direction range task: the random dot stimulus consisted of dots displaced in directions chosen from a predetermined distribution. Motion signal task: the random dot stimulus consisted of a proportion of dots moving coherently in a single direction of motion and the remaining dots moving in random directions. Direction difference threshold task: the random dot stimulus was composed of coherently moving dots. (B,C) The diagrams outline the temporal sequences of the events in a single trial. The sample and test stimuli were either in the same location (B) or spatially separated (C) so that one was placed in the lesioned hemifield and the other in the corresponding location in the intact hemifield. Stimulus positions: centered 5° in the upper field and 5° on either side of the vertical meridian (monkey 1); 2° in the upper field and 8° on either side of the vertical meridian (monkey 2). Stimulus size: 4° dia. Stimulus speed: 5°/s (monkey 1); 10°/s (monkey 2). The direction of motion of the sample was chosen at random from a set of eight from trial to trial and the test moved in a direction that was the same as or different from the sample.

 
The lifetime of an individual dot was either equal to the duration of the stimulus presentation (350–500 ms) (motion signal threshold and direction difference threshold) or was set at 100 ms (direction range threshold). The dot density was 4.7 dots/deg2 and their speed was set to either 5°/s or 10°/s ({Delta}x = 0.065° or 0.13°) depending on the task. Individual dots were 0.03° in diameter and had a luminance set to about 3.5 log units above human detection threshold.

The visual stimuli were placed in one of two locations, either in the hemifield affected by the lesion or in the corresponding location in the intact visual field. In monkey 1 the testing site in the affected hemifield was at 5° to the left of the vertical meridian and 5° up (7.1° eccentricity), the corresponding intact site was at 5° up and 5° to the right of the vertical meridian. In monkey 2 the testing site in the affected hemifield was at 8° to the left of the vertical meridian and 2° up (8.2° eccentricity), the corresponding intact site was at 8° to the right of the vertical meridian and 2° up. These locations were selected on the basis of careful psychophysical mapping performed early in post-lesion training (Rudolph and Pasternak, 1999Go). Within a given testing session, the sample and test were presented either in the same (Fig. 1BGo) or in opposite locations (Fig. 1CGo), and these locations did not change during the course of that session.

Behavioral Procedures

The monkeys were seated in a primate chair with two pushbuttons for monkey 2 and three buttons for monkey 1. They were trained to fixate a small spot at the center of the display while performing the discrimination task in a chosen location of the visual field. A pair of stimuli, the sample and test, appeared sequentially with a set delay period between them. The monkeys were required to judge the directions of motion in the two stimuli as the ‘same’ or ‘different’ by pressing the right or left buttons respectively. The animal initiated the trial by fixating a small spot for 500–1000 ms, which resulted in a sample stimulus onset and a tone signaling the start of the trial. The duration of the sample was limited for monkey 2 (400–500 ms) and was terminated by the middle button press for monkey 1. During the delay there was no visual stimulus. After the test stimulus was presented (350–500 ms), the tone stopped, and the animal had to push the left or right button. An incorrect response resulted in a 3–6 s tone and no reward. A break in fixation or a response during the trial resulted in a brief tone and termination of the trial. A correct response was rewarded with a drop of fruit juice.

The direction of motion in the sample stimulus was varied on a trial-to-trial basis, and was picked randomly from a set of eight directions. The sequence of presentation of same/different stimuli was also randomized from trial to trial. To avoid position biases, a correction procedure was used: after three consecutive errors on one button, the same trial was repeated until the animal made a correct response (which was not included in the data analysis). Each testing session consisted of 300–500 trials separated by a 3 s intertrial interval.

Psychophysical Measures

    Direction Range and Motion Signal Thresholds. Sample and test stimuli either moved in the same direction or in opposite directions. The discrimination difficulty was changed by varying the range of directions within which the dots moved (direction range task) or by varying the proportion of the dots moving coherently (motion signal task). In most cases only one of the two comparison stimuli consisted of the noncoherent motion. Specific stimulus configurations used in each portion of the study are illustrated in individual data figures.

    Direction Difference Threshold. All dots moved coherently in the same direction in sample and test stimuli and the discrimination difficulty was changed by varying the angle of difference between the directions of motion in the sample and the test.

Thresholds were measured after the monkey reached criterion performance on the easiest level of the task (three consecutive sessions >90% or four consecutive sessions >80%). A staircase procedure was used to measure the threshold: three correct responses resulted in a less discriminable stimulus (e.g. a broader range), and each incorrect response decreased the difficulty of discrimination. Thresholds were estimated by fitting the data with a Weibull function, weighted by the number of trials at each point, using the maximum likelihood method (Quick, 1974Go). The Weibull function W(x), was of the form:


where x was the varying stimulus parameter; {alpha}, the centering parameter of the function; ß, the steepness parameter of the function and {gamma} was the asymptotic maximum of the function. The thresholds were taken as the stimulus value corresponding to 75% correct. Psychophysical data were collected continuously for a period of 12–18 months and with the exception of the data labeled ‘lesion effect’ shown in Figure 3Go, the data presented in this paper represent stable performance measured in the lesioned field at the completion of the study. Each data point is based on at least three consecutive sessions in which there was no sign of continued improvement. The data labeled ‘lesion effect’ in Figure 3Go were collected during the first 2–4 sessions of post-lesion testing on each task. The ‘intact’ data were measured with stimuli placed in the corresponding location in the intact hemifield in parallel with the measurements in the lesion field, often on the same day.



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Figure 3. Effect of delay on motion thresholds. Lesion data collected early in post-lesion training (‘lesion effect’) and at the conclusion of testing (‘recovered’) are plotted separately. The data have been fitted by exponential functions to illustrate the loss of information over time. Error bars are SEM. The data were analyzed with univariate ANOVA to test for the interactions between the delay and the lesioned versus intact stimulus locations. The analysis was applied separately to the data labeled ‘lesion effect’ and to the data labeled ‘recovered’. Significant interactions between delay and location: *P < 0.05 and **P < 0.01. (A) Effect of delay on direction range thresholds measured for intact and lesioned hemifields. Normalized range thresholds were calculated by [(360 – range threshold)/360]. The corresponding direction range values are plotted on the right vertical axis. (B) Effect of delay on motion signal thresholds measured for intact and lesioned hemifields. (C) Effect of delay on direction difference thresholds measured for intact and lesioned hemifields. Only the point at 0.2 s delay is plotted to show performance during ‘early post-lesion training’, since at longer delays at the time of early training, the thresholds stabilized quickly at levels indicated by the ‘recovered’ curve.

 

    Results
 Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Notes
 References
 
Lesions

Ibotenic acid injections produced a uniform loss of neurons with an abrupt transition to normal appearing neuropil at the lesion edges. The lesions were reconstructed primarily from the CO sections, which clearly showed the extent of neuronal loss. Comparison with cresyl violet and myelin stains showed thinning of the cortical surface at lesion sites, with substantial gliosis but no apparent damage to fibers.

Figure 2Go shows computer traced images of coronal sections stained with cytochrome oxidase, taken every 2 mm (monkey 1) and every 1.5 mm (monkey 2) through, and either side of, the lesion (marked by *).



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Figure 2. Lesion reconstruction. Computer-traced images of 50 mm thick coronal sections stained for cytochrome oxydase through the entire extent of the lesion. The sections are separated by 2 mm (monkey 1) and 1.5 mm (monkey 2). Normal gray matter is shown in dark gray, light gray represents areas of heavy gliosis. The lesioned regions devoid of neurons seen in the right hemisphere are indicated by ‘*’. Abbreviations: ios, inferior occipital sulcus; ips, intraparietal sulcus, lat, lateral sulcus; ls, lunate sulcus; cs, central sulcus; sts, superior temporal sulcus.

 
Monkey 1

The damaged region of cortex included large portions of MT and MST in the right hemisphere. Cortex on the inferior parietal gyrus and inside the STS was damaged over a 12 mm region extending in the posterior and dorsal direction from the anterior margin of the lesion. The sparing evident in the STS appears to not be MT, but probably represents regions of MST on the posterior wall of the sulcus. There was also damage to some of the adjacent regions including portions of STP, FST and 7a. In addition, there was damage to a portion of the representation of the lower contralateral quadrant of the visual field in V4 and V4t.

Monkey 2

The damaged region of cortex extended ~12 mm along the STS of the right hemisphere. The lesion included all of areas MT and MST and the posterior portions of areas 7a and FST. Areas V4t, lower field representation in V4 and STP also appeared to be damaged. Finally, there was some damage to the portion of V1 that lies beneath the STS; this region probably represented visual fields at 20–40° eccentricity, well away from the fields tested in this study.

MRI scans performed shortly after the lesions showed that in both animals the lower quadrant representations of V4 and/or V4t appeared to have been damaged. Thus, all testing was performed in the upper field to reduce the chance that the deficits recorded were due to damage to these areas.

The extent and location of the visual field representation affected by the lesions were mapped psychophysically and the visual stimuli were placed in the maximally affected portions of the upper visual field and in the corresponding location in the intact visual field (Rudolph and Pasternak, 1999Go).

Effects of Lesions on Retention of Directional Information

To examine the effects of MT/MST lesions on the storage component of the match-to-sample task, both the sample and test stimuli were placed in the same retinotopic locations (see Fig. 1BGo) and the delay between presentations was varied between 0.2 and 4.0 s. Psychophysical testing was performed in the portion of the visual field that was maximally affected by the lesion and in the corresponding location in the intact visual field [details of psychophysical mapping are given elsewhere (Rudolph and Pasternak, 1999Go)]. Both monkeys had previously been trained on these tasks using a 0.2 s delay, as described previously (Rudolf and Pasternak, 1999). Thus, although the ‘lesion effect’ thresholds were measured during the first few weeks of training at longer delays, the data for 0.2 s represent performance that had previously undergone substantial recovery.

Direction Range Thresholds

Figure 3AGo shows the effect of delay on direction range thresholds measured in the intact and lesion locations. The data are plotted as normalized range thresholds [(360 – range threshold)/360], where a value of 0 represents a direction range of 360° and a value of 1 represents 0° range (i.e. coherent motion). The thresholds were computed in this way to allow the fitting of exponential functions, which were found to best approximate the loss of information over time in this and the other two tasks. The corresponding direction range values are plotted on the right vertical axis. During the initial testing period (‘lesion effect’ data in Fig. 3AGo) both monkeys showed moderate deficits at the shortest delay of 0.2 s. The deficit increased dramatically when the delay was increased from 2 to 4 s. With continued training, the performance at longer delays improved for both monkeys (‘recovered’ data in Fig. 3AGo), but remained proportionally greater than at the shorter delays, suggesting that the mechanism involved in the recovery could not maintain the information as well as the normal mechanism in the intact hemifield. A univariate analysis of variance was used to test for interactions between the delay and the location of the stimulus (i.e. in the intact or lesioned hemifield). The interactions were tested for the lesion effects and the recovered effects separately. In both animals the interactions were significant for both the initial effects of the lesions (P < 0.001 for both monkeys) and for the post-recovery effects of the lesion (P < 0.01, monkey 1; P < 0.05, monkey 2). This permanent delay-specific effect allowed us to continue testing the animals with this task and examine the effect of the lesion.

Motion Signal Thresholds

Figure 3BGo shows that the effects of the lesions in both monkeys were similar to those seen with the direction range task. During the initial period of testing (‘lesion effect’ data in Fig. 3BGo), the deficits increased dramatically at longer delays, with a significant interaction between delay and stimulus location in both monkeys (P < 0.001, monkey 1; P < 0.01, monkey 2). With continued testing, the interactions in both monkeys were no longer significant, although the thresholds measured in the lesion field remained abnormally high (‘recovered’ data in Fig. 3BGo). This permanent residual deficit in the ability to extract motion from noise in the absence of MT/MST allowed continued use of the task to study lesion effects on the performance of specific components of our task. However, the recovery of the storage component of the task meant that this mechanism could no longer be tested.

Direction Discrimination Threshold

The data in Figure 3CGo show the effect of the lesions on the accuracy of direction discrimination. The data indicated by the filled circle show the direction threshold measured early in training at 0.2 s delay (‘lesion effect’ in Fig. 3CGo). With continued testing, this threshold improved and stabilized at a level that was significantly higher than normal (ANOVA, P < 0.01, monkey 1; P < 0.001, monkey 2). We then immediately extended the measurements to longer delays. In contrast to the previous two tasks, this initial improvement transferred to longer delays (‘recovered’ in Fig. 3CGo). Both animals were less accurate in discriminating direction with stimuli placed in the lesioned field, but there were no interactions between delay and stimulus location. These results suggest that MT/MST appears to be important for accurate direction discrimination measured with coherently moving dots but may not play a unique role in storage of this type of information.

Effects of Lesions on the Encoding and Retrieval/Comparison Components of the Task

The experiments above demonstrated that MT/MST are likely to be involved in the performance of match-to-sample tasks which require integration of complex motion (non-coherent sample), storage of this information (delay) as well as accurate direction discrimination. However, they could only provide insight into the specific role of storing information, and not differentiate effects due to the encoding or retrieval/comparison components of the task. We examined these roles by spatially separating the sample and the test stimuli and presenting them in corresponding locations in the two hemifields, so that only the sample or only the test stimulus had to be processed by the hemisphere with the MT/MST lesion (see Fig. 1CGo). By comparing thresholds measured in this way to normal performance (i.e. both stimuli in the intact hemifield), we could determine whether the lesioned areas would normally play a role in processing the sample or in the retrieval/comparison component of the task. These data are shown in Figures 4–7GoGoGoGo on the right of each plot (shaded columns). Thresholds measured with both stimuli placed in the intact (white) or lesion location (black) are plotted for comparison on the left of each plot. Since these experiments were performed after the completion of experiments examining the effect of delay (Fig. 3Go), all the data represent stable performance equivalent to the ‘recovered’ data presented in Figure 3Go.



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Figure 4. Normalized direction range thresholds measured at 0.2 and 3 s delays. Only the sample stimulus was composed of dots moving in a range of directions. Normal thresholds (open columns, ‘intact to intact’) were measured when both sample and test were placed in the intact hemifield; affected thresholds (filled columns, ’lesion to lesion’) were measured when both sample and test were placed in the lesioned hemifield. Shaded columns show data from experiments when the sample and test were placed on either side of the vertical meridian. ‘Intact to lesion’ indicates that the sample was placed in the intact hemifield while the test was placed in the lesioned hemifield; ’lesion to intact’ indicates that the sample was placed in the lesioned hemifield while test was placed in the intact hemifield. Error bars are SEM. Normalized thresholds were calculated by [(360-range threshold)/360]. Statistical differences (ANOVA) between adjacent columns: *P < 0.05 and **P < 0.01.

 


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Figure 5. Normalized direction range thresholds measured at 0.2 and 3 s delays. (A) Only the test stimulus was composed of dots moving in a range of directions. (B) Both sample and test stimuli were composed of dots moving in a range of directions. Normal thresholds (open columns) were measured when both sample and test were placed in the intact hemifield; affected thresholds (black columns) were measured when both sample and test were placed in the lesioned hemifield. Shaded columns show data from experiments when the sample and test were placed on either side of the vertical meridian. For other details see Figure 4Go.

 


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Figure 6. Motion signal thresholds measured at 0.2 and 3 s delays. Normal thresholds (open columns) were measured when both sample and test were placed in the intact hemifield; affected thresholds (black columns) were measured when both sample and test were placed in the lesioned hemifield. Shaded columns show data from experiments when the sample and test were placed on either side of the vertical meridian. For other details see Figure 4Go.

 


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Figure 7. Direction difference thresholds measured at 0.2 and 3 s (for monkey 1) delays. Normal thresholds (open columns) were measured when both sample and test were placed in the intact hemifield; affected thresholds (filled columns) were measured when both sample and test were placed in the lesioned hemifield. Shaded columns show data from experiments when the sample and test were placed on either side of the vertical meridian. Error bars are SEM. Statistical differences (ANOVA) between adjacent columns: *P < 0.05 and **P < 0.01. In monkey 1, ‘lesion to intact’ thresholds measured at both delays were not different from thresholds measured in the intact field. In monkey 2 the ‘lesion to intact’ threshold was significantly higher than the normal threshold (P < 0.01). For other details see Figure 4Go.

 
Discriminating Opposite Directions of Motion

    Direction Range Thresholds. The data in Figure 4Go show normalized thresholds for the direction range task. In this experiment the test was always coherent while the direction range of the sample was manipulated to measure the direction range threshold. When the sample was placed in the intact and the test in the lesioned hemifields, the performance of both animals was as good as if both stimuli were placed in the intact hemifield (i.e. normal). Conversely, placing the sample in the lesioned hemifield and the test in the intact hemifield resulted in the performance that was significantly worse than normal. This asymmetry was true for both 0.2 and 3 s delays. These results suggest that normal processing of a non-coherent motion stimulus requires the presence of MT/MST, as a performance decrement was only revealed with the non-coherent sample placed in the lesioned hemifield. To assess the generality of this conclusion, we measured direction range thresholds with a coherently moving sample and non-coherent test (Fig. 5AGo). This manipulation resulted in a reversal of the asymmetry (compare Fig. 5AGo with Fig. 4Go) such that the deficit was present only when the test was placed in the lesioned hemifield, irrespective of the location of the coherent sample. Thus, the deficit was revealed whenever the stimulus being processed in the lesioned hemifield required motion integration, regardless of whether it served as the sample or test. Furthermore, in neither of these tasks did the encoding of coherent motion appear to be affected.

In a subsequent control (Fig. 5BGo) we used non-coherent motion in both sample and test stimuli and found no asymmetry in the results, as the above interpretation predicts. This not only confirms the observation that the lesioned areas play a role in encoding this information, but also implies that there is no retrieval/comparison deficit. This would have been evident by an asymmetry in performance, when the two stimuli were symmetrical and placed in opposite hemifields (i.e. inferior performance with test in the lesioned hemifield).

    Motion Signal Thresholds. In this experiment, the test was always coherent and motion signal thresholds were measured by varying the coherence level (proportion of coherently moving dots) in the sample. The data in Figure 6Go show an asymmetry in motion signal thresholds similar to that found for direction range thresholds. The deficit was present only when the non-coherent sample was presented in the lesioned hemifield. These data suggest that MT/MST would normally play a role in encoding the direction of motion from complex motion stimuli consisting of small proportion of coherent dots in the presence of motion noise.

Accuracy of Direction Discrimination

In this task, spatial separation of sample and test also resulted in an asymmetry despite the fact that both stimuli moved coherently. Direction difference thresholds were worse only if the test stimulus was presented in the lesioned hemifield, irrespective of the location of the sample stimulus. The data from monkey 1 show this effect for both 0.2 and 3 s delays. Unfortunately, in monkey 2 we were unable to measure the same function at 3 s delay since his thresholds were very high even at a 1.5 s delay (see Fig. 3CGo).

These data suggest that the deficit measured with both stimuli placed in the lesion (see Fig. 3CGo and left columns in Fig. 7Go) was most likely due to the retrieval/comparison component of the task not being performed optimally in the absence of MT/MST. Furthermore, it appears that the loss of MT/MST did not affect the encoding of information about direction from a coherent stimulus (in contrast to complex motion), as monkey 1’s performance was no different from normal when only the sample was placed in the lesioned hemifield.

Effect of Delay

Our data show that for the first two tasks the lesion of MT/MST affected encoding of information about the direction of noncoherent motion, and that for the same two tasks it also affected storage of that information. This finding suggests the hypothesis that the mechanism involved in encoding may also play a role in storing the information it has encoded. We tested this hypothesis by comparing the effect of delay on direction range thresholds measured with only the sample or the test containing noncoherent motion.

Figure 8Go shows the results of these two variations of the direction range task. The thresholds have been normalized relative to the performance at the shortest delay (0.2 s) to illustrate the loss of information in the two variations. The data show that in both monkeys the delay had an effect only when the sample was non-coherent and consisted of a broad range of directions. This result supports the hypothesis that the mechanism involved in encoding of stimulus direction may also play a role in storing the information it encodes.



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Figure 8. The effect of delay on performance for two direction range tasks. The effect was measured when both sample and test were in the intact (open symbols) or in the lesioned hemifields (solid circles). (A) Normalized direction range thresholds when the sample was composed of non-coherent motion and the test was composed of coherent motion. (B) Normalized direction range thresholds when the sample was composed of coherent motion and the test was composed of non-coherent motion. Pre-normalized data are shown in Figures 4 and 5GoGo. Thresholds measured at 0.2 and 3 s delay were normalized to the data measured at 0.2 s delay. Error bars are SEM. Note that a delay-specific lesion effect was only apparent when the sample stimulus contained non-coherent motion.

 
    Psychometric Functions. The data in Figures 3 and 8GoGo show that the lesion effect was most pronounced when the sample contained a range of directions and had to be stored for several seconds. To ascertain whether this deficit could have been due to factors other than motion processing we analyzed daily psychometric functions obtained from both monkeys and determined the peak performance for that task, i.e. the asymptotic performance. This value is described by the parameter g of the Weibull function that we used to fit the daily psychometric functions. The data in Figure 9AGo show four typical psychometric functions measured in monkey 2. In these examples, increasing the duration of the delay did not affect the peak performance, irrespective of whether the stimuli were presented in the lesioned or intact hemifields. The data in Figure 9BGo show mean asymptotic performance derived from all of the psychometric functions measured in the intact and lesioned hemifields in the two monkeys. The mean asymptotic values for monkey 1 were similar when stimuli were placed in the intact and lesioned fields and for both delays. The mean asymptotic values for monkey 2 were also similar at the short and long delays, however the lesion produced a significant (P < 0.05, ANOVA) drop in peak performance under both conditions.



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Figure 9. Analysis of psychometric functions. (A) Representative psychometric functions showing the performance of monkey 2 measured in the intact (left panel) and the lesioned (right panel) hemifields at 0.2 s (open and filled circles) and 3 s delays (open and filled squares). The data were fitted with Weibull functions that were weighted by the number of trials at each point (solid and broken lines). (B) Mean asymptotic performance determined from daily psychometric functions for the two monkeys, plotted for the intact (open columns) and lesioned hemifields (filled columns) for both 0.2 and 3 s delays. Error bars are SEM.

 

    Discussion
 Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Notes
 References
 
Although a number of previous lesion studies have shown that MT/MST play a role in the performance of motion discrimination tasks (Newsome and Paré, 1988Go; Schiller, 1993Go; Pasternak and Merigan, 1994Go; Orban et al., 1995Go; Rudolph and Pasternak, 1999Go), the emphasis of these studies has been primarily on encoding the direction or speed of various types of motion stimuli. In the present study, we used a motion discrimination task that, in addition to the extraction of information about stimulus direction, imposed a requirement of storing and retrieving information. In this task, we separated the two comparison motion stimuli both spatially and temporally. This allowed us to examine not only the contribution of these cortical areas to encoding various aspects of motion information but also to the storage and retrieval/comparison of this information. The use of two types of discrimination, in which animals either had to discriminate between opposite directions of motion or accurately discriminate between two similar directions of motion, highlights the individual roles that MT/MST play under specific controlled conditions.

We found that the effects of MT/MST lesions on the performance of match-to-sample tasks depended on the properties of the visual motion stimuli and on the type of visual discrimination. A contribution of MT/MST neurons to the encoding and storage aspects of the task was revealed with non-coherent motion stimuli. On the other hand, the absence of MT/MST did not affect encoding or storage of directional information when the stimulus was composed of coherently moving dots, irrespective of the task. The contribution of MT/MST to the retrieval/comparison stage of the task was revealed when monkeys were required to accurately discriminate differences in the direction of motion of coherently moving stimuli.

Effects of MT/MST Lesions on Direction Discrimination Tasks

Processing of Non-coherent Motion

Previous studies have suggested that in the absence of MT/MST non-coherent motion stimuli pose a challenge to the residual encoding mechanism (Vaina, 1989Go; Baker et al., 1991Go; Pasternak and Merigan, 1994Go; Vaina and Cowey, 1996Go; Braun et al., 1998Go; Rudolph and Pasternak, 1999Go). Single-unit recording studies have also provided evidence that neurons in area MT are capable of both integrating local motion signals, and extracting coherent motion from noise (Movshon et al., 1985Go; Rodman and Albright, 1989Go; Britten et al., 1992Go). By showing a lesion deficit during a portion of the task in which the monkeys were only encoding information about direction from non-coherent motion, we have provided further support for a role of MT in motion integration.

Accuracy of Direction Discrimination

    Normal Thresholds. The direction difference thresholds measured in the intact field in both monkeys was about a factor of two or three higher than that we reported in a previous study (Pasternak and Merigan, 1994Go). There are several factors that could account for this difference, all related to differences in the nature of the behavioral task used in this study. Firstly, this task had to be performed under conditions of high uncertainty as to the direction of motion in the sample since it changed on each trial (Ball and Sekuler, 1981Go; Magnussen et al., 1996Go). Secondly, in this study the monkeys viewed the stimuli peripherally rather than foveally. Other factors that were likely to contribute to the relatively low accuracy of discrimination are the relatively low stimulus speeds used in this study (Pasternak and Merigan, 1984Go) as well as the presence of temporal delays. This last factor appeared to play a more pronounced role in monkey 2, who could not perform the task at threshold levels with delays >2 s. Another difference between the animals was that monkey 2 was consistently less accurate whenever the sample and test were separated by the vertical meridian, regardless of their placement with respect to the lesion. We have observed a similar decrease in accuracy when non-lesioned monkeys performed the same task with sample and test placed in opposite hemifields (Zaksas et al., 1999Go). Furthermore, we found that with training, some monkeys, but not all, learn to transfer the information across the vertical meridian more efficiently and reach a level of performance comparable to the level measured with two stimuli in a single location.

    Effect of MT/MST Lesions. Both animals were less accurate in discriminating direction differences when both sample and test were placed in the lesioned field. This deficit confirmed our previous report of the reduced accuracy of direction discrimination resulting from lesions of areas MT/MST (Pasternak and Merigan, 1994Go). The present study examined the mechanism underlying this deficit. By spatially separating the two comparison stimuli, we found that the effect of the lesion on performance of this task is governed primarily by the location of the test stimulus. That is, only the portion of the task that took place at the time of test presentation could not be performed at normal levels. It remains to be seen which of the individual components of this process were affected by the loss of MT/MST (i.e. encoding of the test stimulus, retrieval of the sample stimulus from storage, transfer of one or both stimuli to a comparator mechanism or the comparison between the sample and test).

The lack of a deficit when only the sample stimulus was placed in the affected field suggests that the successful encoding of coherent motion could take place in the absence of areas MT/MST. This also suggests that the deficit seen when the test was placed in the lesioned hemifield was not due to encoding of the test stimulus, as the two stimuli were identical. This finding does not necessarily suggest that areas MT/MST do not normally participate in processing of this type of stimulus. Rather, it shows that this type of stimulus does not pose a challenge to the residual motion mechanism.

One possibility is that the repeated use of the same eight directions as the sample masked the encoding deficit by the animals learning the eight standard directions and using them as indicators as to which one of these directions to use. However, the use of such strategy would produce no delay effect — once cued the animal would not need to remember the actual stimulus. Contrary to this prediction, our data clearly show a strong delay effect even in the normal field (see Fig. 3CGo, monkey 2).

Measuring Short-term Retention of Visual Motion Information

We measured the ability of the animals to retain directional information by varying stimulus discriminability and measuring changes in thresholds with delay. Only a handful of studies used a similar approach to examine the short-term storage of visual information. These studies, performed in humans, showed that while some stimulus attributes appear to be perfectly preserved for many seconds (Regan, 1985Go; Magnussen et al., 1990Go) others degrade with time (Vogels and Orban, 1986Go; Fahle and Harris, 1992Go; Lee and Harris, 1996Go; Magnussen et al., 1996Go). Only two studies have explored temporary storage of motion information, and both reported perfect retention of thresholds for direction (Blake et al., 1997Go) and velocity (Magnussen and Greenlee, 1992Go) with delays as long as 10 s.

A number of factors could account for the difference between the perfect preservation of directional information observed in the human study and the gradual loss in thresholds observed in our monkeys. These include species differences and differences in the psychophysical procedures. For example, it is possible that humans and monkeys may be using different strategies in retaining information about stimulus direction. Humans may be encoding the information by aligning a direction of motion to a position on an imaginary clock face, so the delay time becomes irrelevant. Although we cannot poll our animals about the approach they use, the presence of delay effects in all of our tasks makes it unlikely that monkeys use the same kind of strategy.

Effects of MT/MST Lesions on Working Memory

We found a greater loss of information over time when the stimulus was composed of non-coherent motion and was placed in the lesioned hemifield than when the same stimulus was presented in the intact hemifield. The greater deficits at a longer delay were not the result of an overall decline in performance associated with factors other than motion processing since their asymptotic performance with the easiest stimuli was similar at long and short delays. Rather, the greater lesion effect at the longer delay was more likely the reflection of a deficit in the ability to store information about complex motion.

This conclusion is strengthened by the absence of the delay-specific deficit when a coherent sample was placed in the lesioned hemifield, irrespective of the task the animal had to perform. Thus, the delay deficits appeared to coincide with the encoding deficits, suggesting the possibility that MT/MST may not only play a role in encoding but may also be involved in mechanisms underlying storage of such information. An alternative explanation of this result would have to involve the existence of an independent storage mechanism, which in the absence of MT/MST receives poorly encoded information that degrades more rapidly over time. Two observations argue against this possibility. First, the permanent deficit in motion signal thresholds seen in both monkeys was not accompanied by a deficit in storing the poorly encoded information (Fig. 3BGo, ‘recovered’ data). Second, although range thresholds showed some improvements at longer delays, the delay-specific deficit never fully recovered (Fig. 3AGo, ‘recovered’ data). Encoding of the information was degraded in both cases, yet retention was permanently affected in only one case, and it is unlikely that an independent storage mechanism would handle the extracted directional information differently.

Finally, the presence of the delay-specific deficit in only one of the tasks suggests that this deficit cannot be explained by such non-specific factors as decreased ability to maintain attention as that would require separate mechanisms of attention for the two tasks.

Training-induced Improvements

One of the more surprising results in this study was the difference in the extent of recovery of delay-specific deficits measured with the direction range and motion signal stimuli. Although the initial lesion effects showed greater deficits at longer delays with both types of stimuli, only the retention of direction of stimuli containing a broad range of directions remained permanently affected. We previously observed dissociation in susceptibility of the two types of stimuli to brain lesions (Pasternak et al., 1990Go; Pasternak and Merigan, 1994Go; Rudolph and Pasternak, 1996Go) with motion signal thresholds being more susceptible to disruption than range thresholds. Surprisingly, the present study revealed the opposite pattern of results: storage of the stimulus used to measure motion signal thresholds was affected less by the lesion than storage of the stimulus consisting of a broad distribution of directions. One possible explanation of this difference stems from our hypothesis that the encoding mechanism may play a role in storing the encoded information. After the loss of neurons normally involved in processing both types of motion, separate sets of neurons could begin to perform the two operations. In the ‘motion signal’ stimulus, the direction of coherently moving dots may be detected by directionally selective neurons residing in various cortical areas outside MT/MST. On the other hand, calculating the mean direction from the ‘direction range’ stimulus may require a more complicated cooperative network of neurons, each preferring different directions of motion. We hypothesize that these two mechanisms may not be equally well equipped to play a role in storing the encoded information. With post-lesion training, the encoding may improve, but the effect of a delay would be dependent on the storage capacity of the newly recruited encoding mechanism.

There are a number of cortical areas with directionally selective neurons that are likely to respond to moving random dot stimuli, and thus may play a role in recovery by signaling stimulus direction to the animal in the absence of MT. These areas include both earlier stages of cortical analysis (e.g. areas V1, V2, V3 and V4) (Ferrera et al., 1994Go; Skottun et al., 1994Go; Gegenfurtner et al., 1996Go) as well as such areas as FST, STP and 7a representing much more advanced stages of visual processing (Desimone and Ungerleider, 1986Go; Oram et al., 1993Go; Siegel and Read, 1997Go). Although the latter three areas sustained some unintended damage in both monkeys, this was relatively limited.

Is MT/MST Involved in Working Memory For Motion?

Much of the physiological work on neural mechanisms of visual working memory has focused on inferotemporal cortex, which represents a relatively advanced stage of processing within the ventral visual stream (Merigan and Maunsell, 1993Go). Such studies reported that a subset of neurons in the inferotemporal cortex of monkeys trained to remember visual properties of objects, maintain an elevated firing rate during the delay after a specific color, shape or location is presented (Miyashita and Chang, 1988Go; Fuster, 1990Go; Miller et al., 1993Go; Gibson and Maunsell, 1997Go). Similar activity has been observed in neurons in prefrontal and entorhinal cortical areas (Kojima and Goldman-Rakic, 1982Go; Funahashi et al., 1993Go; Miller et al., 1996Go; Suzuki et al., 1997Go; Rainer et al., 1998Go). These results have been interpreted as evidence that these neurons may be involved in the short-term storage of information about stimulus form, color or location.

Considerably less attention has been devoted to a possible role of earlier stages of cortical processing in visual memory, although there is evidence for such involvement in other sensory systems (Zhou and Fuster, 1996Go, 1997Go). Nevertheless, a few studies suggest such a role for area V4 (Desimone et al., 1990Go; Ferrera et al., 1994Go; Motter, 1994Go), which provides major inputs to inferotemporal cortex. Of the numerous physiological studies of area MT neurons in monkeys performing motion discrimination tasks, only two (Ferrera et al., 1994Go; Seidemann et al., 1998Go) used a delay. In the experiment by Seidemann et al., the delay period was introduced to postpone the response to the previous visual stimulus, rather than to force the monkey to remember the visual stimulus (Seidemann et al., 1998Go). Under these conditions, delay-period activity was not observed in any of the recorded neurons. Ferrera et al. used a task in which the monkeys were required to briefly store information about stimulus direction: a number of stimuli were presented during a brief delay (200–540 ms) only one of which matched the remembered stimulus. Although some cells had a significant increase in activity during the latter part of the delay this activity did not appear to carry information about the remembered direction. Furthermore, the data showed no enhanced excitability of MT neurons to motion stimuli during retention of the cued stimulus. The authors concluded that MT neurons are unlikely to be involved in storing the directional information (Ferrera et al., 1994Go).

We recently began recording from MT neurons during the performance of the task identical to that used in the present study. Unlike Ferrera et al., we found that a significant proportion of MT neurons show transient activity during the delay and that in some neurons this activity is modulated by the direction of the sample stimulus (Droll et al., 2000Go). We also recently found that microstimulation of direction-selective columns in MT during the delay period of the same task produced severe deficits in performance, suggesting that MT maintains an active connection with areas underlying working memory during the retention period of the task (Bisley and Pasternak, 1999Go). These recent physiological results provide further support for the possibility that area MT neurons participate in the circuitry underlying the short-term storage of visual motion information.

The idea that the neural mechanisms involved in encoding of the visual stimulus may also be involved in its storage has previously been suggested by a number of psychophysical studies (Magnussen et al., 1991Go; Magnussen and Greenlee, 1992Go; Blake et al., 1997Go). Evidence supporting this view has also been provided by imaging (Courtney et al., 1996Go) and lesion studies in humans (Greenlee et al., 1995Go). Similar observations have been reported for other sensory systems (Bodner et al., 1996Go; Zhou and Fuster, 1996Go). The present study provides strong support for this idea by showing that areas MT/MST, which represent an important stage in the analysis of motion information, are not only involved in processing of complex motion, but also in temporary storage of this information.


    Notes
 Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Notes
 References
 
We thank Judy Gesner, Noelle Landauer, Debbie Moore and Dan Zaksas for excellent technical assistance and Anand Bahirwani for software development. We are grateful to Drs Scott Kennedy and Edmond Kwok for MRI scanning and to Tracy Montag for the histology. We also thank Bill Merigan and John Reynolds for the comments on the manuscript. This work was supported by the grants from the National Eye Institute, R01 EY05911 (T.P.) and in part by P30 EY01319 (Center for Visual Science).

Address correspondence to: Tatiana Pasternak, Department of Neurobiology and Anatomy, Box 603, University of Rochester, Rochester, NY 14642, USA. Email: tania{at}cvs.rochester.edu.


    Footnotes
 
1 Current address: Laboratory of Sensorimotor Research, National Eye Institute, 49 Convent Drive, Building 49, Bethesda, MD 20892, USA Back


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