Department of Neurobiology & Anatomy and Center for Visual Science, University of Rochester, Rochester, NY 14642, USA
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Abstract |
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Introduction |
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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, 1974; Maunsell and Van Essen, 1983
; Albright, 1984
), perform integration of local motion signals (Movshon et al., 1985
; Rodman and Albright, 1989
), and discriminate motion direction in the presence of noise with nearly the same sensitivity as monkeys and humans (Britten et al., 1992
; Celebrini and Newsome, 1994
). 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., 1992
; Celebrini and Newsome, 1995
). 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, 1988
; Schiller, 1993
; Pasternak and Merigan, 1994
; Orban et al., 1995
; Rudolph and Pasternak, 1999
).
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.
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Materials and Methods |
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Two young adult male monkeys (Macaca nemestrina), weighing 810 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, 1999). 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, 1994). 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, 1999
). 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 HorsleyClark 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, 1979), myelin (Gallyas, 1979
) 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., 1990; Pasternak and Merigan, 1994
; Rudolph and Pasternak, 1999
) 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. 1A
, 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. 1A
, middle). Coherent motion stimulus: all of the dots were displaced in the same direction (Fig. 1A
, right).
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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, 1999). Within a given testing session, the sample and test were presented either in the same (Fig. 1B
) or in opposite locations (Fig. 1C
), 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 5001000 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 (400500 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 (350500 ms), the tone stopped, and the animal had to push the left or right button. An incorrect response resulted in a 36 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 300500 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, 1974). The Weibull function W(x), was of the form:
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where x was the varying stimulus parameter; , the centering parameter of the function; ß, the steepness parameter of the function and
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 1218 months and with the exception of the data labeled lesion effect shown in Figure 3
, 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 3
were collected during the first 24 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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Results |
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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 2 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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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 2040° 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, 1999).
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. 1B) 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, 1999
)]. 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 3A 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. 3A
) 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. 3A
), 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 3B 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. 3B
), 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. 3B
). 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 3C 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. 3C
). 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. 3C
). 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. 1C). 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 47
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. 3
), all the data represent stable performance equivalent to the recovered data presented in Figure 3
.
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Direction Range Thresholds.
The data in Figure 4 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. 5A
). This manipulation resulted in a reversal of the asymmetry (compare Fig. 5A
with Fig. 4
) 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. 5B) 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 6 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. 3C).
These data suggest that the deficit measured with both stimuli placed in the lesion (see Fig. 3C and left columns in Fig. 7
) 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 1s 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 8 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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Discussion |
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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, 1989; Baker et al., 1991
; Pasternak and Merigan, 1994
; Vaina and Cowey, 1996
; Braun et al., 1998
; Rudolph and Pasternak, 1999
). 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., 1985
; Rodman and Albright, 1989
; Britten et al., 1992
). 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, 1994). 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, 1981
; Magnussen et al., 1996
). 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, 1984
) 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., 1999
). 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, 1994). 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. 3C, 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, 1985; Magnussen et al., 1990
) others degrade with time (Vogels and Orban, 1986
; Fahle and Harris, 1992
; Lee and Harris, 1996
; Magnussen et al., 1996
). Only two studies have explored temporary storage of motion information, and both reported perfect retention of thresholds for direction (Blake et al., 1997
) and velocity (Magnussen and Greenlee, 1992
) 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. 3B, recovered data). Second, although range thresholds showed some improvements at longer delays, the delay-specific deficit never fully recovered (Fig. 3A
, 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., 1990; Pasternak and Merigan, 1994
; Rudolph and Pasternak, 1996
) 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., 1994; Skottun et al., 1994
; Gegenfurtner et al., 1996
) as well as such areas as FST, STP and 7a representing much more advanced stages of visual processing (Desimone and Ungerleider, 1986
; Oram et al., 1993
; Siegel and Read, 1997
). 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, 1993). 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, 1988
; Fuster, 1990
; Miller et al., 1993
; Gibson and Maunsell, 1997
). Similar activity has been observed in neurons in prefrontal and entorhinal cortical areas (Kojima and Goldman-Rakic, 1982
; Funahashi et al., 1993
; Miller et al., 1996
; Suzuki et al., 1997
; Rainer et al., 1998
). 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, 1996, 1997
). Nevertheless, a few studies suggest such a role for area V4 (Desimone et al., 1990
; Ferrera et al., 1994
; Motter, 1994
), 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., 1994
; Seidemann et al., 1998
) 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., 1998
). 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 (200540 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., 1994
).
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., 2000). 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, 1999
). 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., 1991; Magnussen and Greenlee, 1992
; Blake et al., 1997
). Evidence supporting this view has also been provided by imaging (Courtney et al., 1996
) and lesion studies in humans (Greenlee et al., 1995
). Similar observations have been reported for other sensory systems (Bodner et al., 1996
; Zhou and Fuster, 1996
). 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.
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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.
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Baker C, Hess RF, Zihl J (1991) Residual motion perception in a motion-blind patient, assessed with limited-lifetime random dot stimuli. J Neurosci 11:454461.[Abstract]
Ball K, Sekuler R (1981) Cues reduce direction uncertainty and enhance motion detection. Percept Psychophys 30:119128.[ISI][Medline]
Bisley JW, Pasternak T (1999) Microstimulation in area MT: an effect on a memory for motion task. Soc Neurosci Abstr 25:275.
Blake R, Cepeda NJ, Hiris E (1997) Memory for visual motion. J Exp Psychol Hum Percept Perform 23:353369.[ISI][Medline]
Bodner M, Kroger J, Fuster JM (1996) Auditory memory cells in dorsolateral prefrontal cortex. NeuroReport 7:19051908.[ISI][Medline]
Braun D, Petersen D, Schonle P, Fahle M (1998) Deficits and recovery of firstand second-order motion perception in patients with unilateral cortical lesions. Eur J Neurosci 10:21172128.[ISI][Medline]
Britten KH, Shadlen MN, Newsome WT, Movshon JA (1992) The analysis of visual motion: a comparison of neuronal and psychophysical performance. J Neurosci 12:47454765.[Abstract]
Celebrini S, Newsome WT (1994) Neuronal and psychophysical sensitivity to motion signals in extrastriate area MST of the macaque monkey. J Neurosci 14:41094124.[Abstract]
Celebrini S, Newsome WT (1995) Microstimulation of extrastriate area MST influences performance on a direction discrimination task. J Neurophysiol 73:437448.
Courtney SM, Ungerleider LG, Keil K, Haxby JV (1996) Object and spatial visual working memory activate separate neural systems in human cortex. Cereb Cortex 6:3949.[Abstract]
Desimone R, Li L, Lehky S, Ungerleider LG, Mishkin M (1990) Effects of V4 lesions on visual discrimination performance and responses of neurons in inferior temporal cortex. Soc Neurosci Abstr 16:621.
Desimone R, Ungerleider LG (1986) Multiple visual cortical areas in the caudal superior temporal sulcus of the macaque. J Comp Neurol 248:164189.[ISI][Medline]
Droll JA, Bisley JW, Pasternak T (2000) Delay activity in area MT neurons during a visual working memory task. IOVS 41:S721 (Abstract).
Fahle M, Harris JP (1992) Visual memory for vernier offsets. Vis Res 32:10331042.[ISI][Medline]
Ferrera VP, Rudolph KK, Maunsell JH (1994) Responses of neurons in the parietal and temporal visual pathways during a motion task. J Neurosci 14:61716186.[Abstract]
Funahashi S, Chafee MV, Goldman-Rakic PS (1993) Prefrontal neuronal activity in rhesus monkeys performing a delayed anti-saccade task. Nature 365:753756.[ISI][Medline]
Fuster JM (1990) Inferotemporal units in selective visual attention and short-term memory. J Neurophysiol 64:681697.
Gallyas F (1979) Silver staining of myelin by means of physical development. Neurol Res 1:203209.[Medline]
Gegenfurtner KR, Kiper DC, Fenstemaker SB (1996) Processing of color, form, and motion in macaque area V2. Vis Neurosci 13:161172.[ISI][Medline]
Gibson JR, Maunsell JH (1997) Sensory modality specificity of neural activity related to memory in visual cortex. J Neurophysiol 78:12631275.
Greenlee MW, Lang H-J, Mergner T, Seeger W (1995) Visual short-term memory of stimulus velocity in patients with unilateral posterior brain damage. J Neurosci 15:22872300.[Abstract]
Kojima S, Goldman-Rakic PS (1982) Delay-related activity of prefrontal cortical neurons in rhesus monkeys performing delayed response. Brain Res 248:4349.[ISI][Medline]
Lee B, Harris J (1996) Contrast transfer characteristics of visual short-term memory. Vis Res 36:21592166.[ISI][Medline]
Magnussen S, Greenlee MW (1992) Retention and disruption of motion information in visual short-term memory. J Exp Psychol Learn Mem Cog 18:151156.[ISI][Medline]
Magnussen S, Greenlee MW, Asplund R, Dyrnes S (1990) Perfect visual short-term memory for periodic patterns. Eur J Cog Psychol 2:345362.
Magnussen S, Greenlee MW, Asplund R, Dyrnes S (1991) Stimulus specific mechanisms of visual short-term memory. Vis Res 31:12131219.[ISI][Medline]
Magnussen S, Greenlee MW, Thomas JP (1996) Parallel processing in visual short-term memory. J Exp Psychol Hum Percept Perform 72:202212.
Maunsell JH, Van Essen DC (1983) Functional properties of neurons in middle temporal visual area of the macaque monkey. I. Selectivity for stimulus direction, speed, and orientation. J Neurophysiol 49:11271147.
Merigan WH, Maunsell JHR (1993) How parallel are the primate visual pathways. Annu Rev Neurosci 16:369402.[ISI][Medline]
Miller EK, Li L, Desimone R (1993) Activity of neurons in anterior inferior temporal cortex during short-term memory task. J Neurosci 13:14601478.[Abstract]
Miller EK, Erickson CA, Desimone R (1996) Neural mechanisms of visual working memory in prefrontal cortex of the macaque. J Neurosci 16:51545167.
Miyashita Y, Chang HS (1988) Neuronal correlate of short-term memory in the primate temporal cortex. Nature 331:6870.[ISI][Medline]
Motter BC (1994) Neural correlates of feature selective memory and pop-put in extrastriate area v4. J Neurosci 14:21902199.[Abstract]
Movshon JA, Adelson EH, Gizzi MS, Newsome WT (1985) The analysis of moving visual patterns. In: Pattern recognition mechanisms (Chagas C, Gattas R, Gross CG, eds), pp. 117151. Vatican City: Ponticifica Academia Scientiarum.
Newsome WT, Paré EB (1988) A selective impairment of motion perception following lesions of the middle temporal visual area (MT). J Neurosci 8:22012211.[Abstract]
Oram MW, Perrett DI, Hietanen JK (1993) Directional tuning of motion-sensitive cells in the anterior superior temporal polysensory area of the macaque. Exp Brain Res 97:274294.[ISI][Medline]
Orban GA, Saunders RC, Vandenbussche E (1995) Lesions of the superior temporal cortical motion areas impair speed discrimination in the macaque monkey. Eur J Neurosci 7:22612276.[ISI][Medline]
Pasternak T, Merigan WH (1984) Effects of stimulus speed on direction discriminations. Vis Res 24:13491355.[ISI][Medline]
Pasternak T, Merigan WH (1994) Motion perception following lesions of the superior temporal sulcus in the monkey. Cereb Cortex 4:247259.[Abstract]
Pasternak T, Albano JE, Harvitt D (1990) The role of directionally selective neurons in the perception of global motion. J Neurosci 10:30793086.[Abstract]
Quick RF (1974) A vector-magnitude model of contrast detection. Kybernetik 16:6567.[ISI][Medline]
Rainer G, Asaad WF, Miller EK (1998) Selective representation of relevant information by neurons in the primate prefrontal cortex. Nature 393:577579.[ISI][Medline]
Regan D (1985) Storage of spatial-frequency information and spatial frequency discrimination. J Opt Soc Am A 2:619621.[ISI]
Rodman HR, Albright TD (1989) Single-unit analysis of pattern-motion selective properties in the middle temporal visual area (MT). Exp Brain Res 75:5364.[ISI][Medline]
Rudolph KK, Pasternak T (1996) Lesions in cat lateral suprasylvian cortex affect the perception of complex motion. Cereb Cortex 6:814822.[Abstract]
Rudolph K, Pasternak T (1999) Transient and permanent deficits in motion perception after lesions of cortical areas MT and MST in the macaque monkey. Cereb Cortex 9:90100.
Salzman CD, Mirasugi CM, Britten KH, Newsome WT (1992) Microstimulation of visual area MT: effects on direction discrimination performance. J Neurosci 12:23312356.[Abstract]
Schiller PH (1993) The effects of V4 and middle temporal (MT) area lesions on visual performance in the rhesus monkey. Vis Neurosci 10:717746.[ISI][Medline]
Seidemann E, Zohary E, Newsome WT (1998) Temporal gating of neural signals during performance of a visual discrimination task. Nature 394:7275.[ISI][Medline]
Siegel RM, Read HL (1997) Analysis of optic flow in the monkey parietal area 7a. Cereb Cortex 7:327346.[Abstract]
Skottun BC, Zhang J, Grosof DH (1994) On the directional selectivity of cells in the visual cortex to drifting dot patterns. Vis Neurosci 11:885897.[ISI][Medline]
Suzuki WA, Miller EK, Desimone R (1997) Object and place memory in the macaque entorhinal cortex. J Neurophysiol 78:10621081.
Vaina LM (1989) Selective impairement of visual motion interpretation following lesions of the right occipito-parietal area in humans. Biol Cybernet 61:347359.[ISI][Medline]
Vaina LM, Cowey A (1996) Impairment of the perception of second order motion but not first order motion in a patient with unilateral focal brain damage. Proc R Soc B Biol Sci 263:12251232.[ISI][Medline]
Vogels R, Orban GA (1986) Decision processes in visual discrimination of line orientation. J Exp Psychol Hum Percept Perform 12:115132.[ISI][Medline]
Wong-Riley M (1979) Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry. Brain Res 171:1128.[ISI][Medline]
Zaksas D, Bisley JW, Pasternak T (1999) Interhemispheric transfer of directional motion information in macaque monkeys. Soc Neurosci Abstr 25:398.
Zeki SM (1974) Functional organization of a visual area in the posterior bank of the superior temporal sulcus of the rhesus monkey. J Physiol 236:549573.[ISI][Medline]
Zhou YD, Fuster JM (1996) Mnemonic neuronal activity in somatosensory cortex. Proc Natl Acad Sci USA 93:1053310537.
Zhou YD, Fuster JM (1997) Neuronal activity of somatosensory cortex in a cross-modal (visuo-haptic) memory task. Exp Brain Res 116:551555.[ISI][Medline]