Discrimination of Line Orientation in Humans and Monkeys

Pablo Vázquez, Mónica Cano, and Carlos Acuña

Laboratorios de Neurociencia y Computación Neuronal (asociados al Instituto Cajal-CSIC), Instituto Universitario de Ciencias Neurológicas P. Barrié, Servicio de Neurofisiología Clínica-Hospital Clínico Universitario, Universidad de Santiago de Compostela, E-15705 Santiago de Compostela, Spain


    ABSTRACT
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

Vázquez, Pablo, Mónica Cano, and Carlos Acuña. Discrimination of Line Orientation in Humans and Monkeys. J. Neurophysiol. 83: 2639-2648, 2000. Orientation discrimination, the capacity to recognize an orientation difference between two lines presented at different times, probably involves cortical processes such as stimuli encoding, holding them in memory, comparing them, and then deciding. To correlate discrimination with neural activity in combined psychophysical and electrophysiological experiments, precise knowledge of the strategies followed in the completion of the behavioral task is necessary. To address this issue, we measured human and nonhuman primates' capacities to discriminate the orientation of lines in a fixed and in a continuous variable task. Subjects have to indicate whether a line (test) was oriented to one side or to the other of a previously presented line (reference). When the orientation of the reference line did not change across trials (fixed discrimination task), subjects can complete the task either by categorizing the test line, thus ignoring the reference, or by discriminating between them. This ambiguity was avoided when the reference stimulus was changed randomly from trial to trial (continuos discrimination task), forcing humans and monkeys to discriminate by paying continuous attention to the reference and test stimuli. Both humans and monkeys discriminated accurately with stimulus duration as short as 150 ms. Effective interstimulus intervals were of 2.5 s for monkeys but much longer (>6 s) in humans. These results indicated that the fixed and continuous discrimination tasks are different, and accordingly humans and monkeys do use different behavioral strategies to complete each task. Because both tasks might involve different neural processes, these findings have important implications for studying the neural mechanisms underlying visual discrimination.


    INTRODUCTION
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

Neuronal responses to oriented lines first appear in the visual striate cortex (Hubel and Wiesel 1962, 1968), where orientation columns have been shown by many various techniques (Blasdel and Salama 1986; Bonhoeffer and Grinvald 1991; Hubel and Wiesel 1962, 1974). Although the great majority of electrophysiological studies on orientation have used single lines as visual stimuli, psychophysical studies devoted to orientation discrimination of lines in humans are sparser (e.g., Cheal et al. 1991; Downing 1988; Jastrow 1892; Matin and Drivas 1979; Orban et al. 1984; Vogels and Orban 1986a,b, 1987; Westheimer 1996; Westheimer et al. 1976). Oriented gratings have instead been used extensively in combined psychophysical and electrophysiological studies (Vogels and Orban 1990). Some experiments have reported differences between cell responses to bars and gratings (Born and Tootell 1991a,b; Maffei and Fiorentini 1976; von der Heydt et al. 1992), however, and moreover a direct comparison between the discrimination of oriented lines by monkeys and humans is missing.

The behavioral task chosen to study visual processing can be as important to the experiment as the choice of stimulus (Orban and Vogels 1998; Parker and Newsome 1998; Van Essen et al. 1992; Vogels and Orban 1994). Hernández et al. (1997) have shown in the somatosensory system that when a reference stimulus (mechanical sinusoids delivered to their hands) is kept constant from trial to trial, monkeys have the choice of determining the frequency of a test stimulus either by comparing the two stimuli (i.e.,: frank discrimination) or by ignoring the reference stimulus altogether. Moreover Orban and collaborators have shown that, using illusory contour patterns and oriented gratings as stimuli, changing the reference produced a drop in performance levels compared with a constant reference (Orban and Vogels 1998; Vogels and Orban 1986a,b). We decided to test if the preceding results from the somatosensory and visual systems can be generalized to the visual system using single long lines as stimulus and making a direct comparison between human and nonhuman primates. We also investigated the effect of temporal factors, such as stimulus duration and interstimulus duration times on subjects' performance. Previous short reports have been made elsewhere (Vázquez and Acuña 1997, 1998).


    METHODS
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

General

Experiments were carried out on two male monkeys (Macaca mulatta 3-5 kg, referred to as BMV1 and BMV2) and eight humans (6 females and 2 males, 18-22 yr). All subjects had normal emmetropic vision, with the exception of one human subject who wore her corrective lenses during the experiment. Subjects looked binocularly at a monitor screen placed at 114-cm from their eyes (1 cm subtended 0.5° to the eye), in an isolated, sound-proof room, illuminated from above with 40 lux. A chin rest and a headband supported the head of the human subjects. Monkeys had their head fixed, and their left arm restrained during the task. Their right arm operated a lever (elbow joint at ~90°). A panel with three switches situated at the vertices of a triangle (left, upper middle, and right) was in front of the right shoulder within hand reach. Left, upper middle, and right switches were at 60, 85, and 110 mm from the middle saggital plane, at 200 mm from the monkey's shoulder and 15 mm below eye level. Monkeys used the upper middle switch in the fixation task to signal the tilt of the fixation bar. The left and right switches were used in the discrimination task to signal orientations to the left and right, respectively. Eye movements were recorded with the magnetic eye search coil technique (C-N-C Engineering) (Robinson 1963), sampled at 740 Hz and acquired with BrainWave (Data Wave Technologies). All experiments were carried out in strict agreement with the guiding principles for research involving animals and human beings of the Declaration of Helsinki, European Union and of University of Santiago de Compostela. All human participants were paid.

Visual stimuli were created in a 90-MHz Pentium PC using a 4-MB Matrox MGA Millennium II PCI graphic card driven by MGL Libraries from SciTech and presented in a NOKIA multigraph 445× monitor, with 75-Hz vertical refresh rate, and 1,280 × 1,024 pixel resolution (pixel subtends 0.014° at 114 cm, 1 cm = 0.5°), and 8 bits/pixel color resolution. Line luminance was 24.5 cd/m2, line contrast 0.9 (Michelson). CORTEX (a freeware program developed in the Laboratory of Neuropsychology at the National Institute of Mental Health) was used for task control and to generate visual stimuli.

The stimuli (Fig. 1) were stationary bright lines, subtending 3° length (Fig. 1, beta ) and 0.03° width. The 3° line length was chosen because discrimination thresholds do not significantly change for longer bright lines (Orban and Vogels 1998; Westheimer and Wehrhahn 1994). Three different reference orientations were used, 90, 95, and 85°. Different test lines, 10 per reference stimulus, were presented clockwise or counterclockwise to the reference line in steps of 1° (Fig. 1, alpha ). To avoid the use of end points of the line as a cue, the test line was pseudorandomly displaced in both horizontal directions (Fig. 1, theta ). The amount of displacement was less than or equal to twice the value of the maximum separation of the two lines (reference and test) for minimum change in orientation. For example, the end point of +1° rotation of the test line will be mistaken for the end point of -1° rotation of the test line. This forces subjects to rely only on the orientation of the line to complete the task. These values are in BC of Fig. 1.



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Fig. 1. Experimental design. A: stimulus consisted of a stationary line segment (A-B; A'-C') subtending 3° of visual angle (dva, in the inset) (beta ). Reference stimulus (A-B) was presented with 3 different orientations. Test lines (A'-C'), 10 per reference, were presented rotated clockwise or counterclockwise to the reference line in steps of 1° (alpha ) in the frontoparallel plane and shifted in position (A to A' = C to C'). Amount of displacement (theta  = ±0.1 dva) was less than or equal to twice the value of the maximum separation of the 2 lines for a minimum change in orientation (B to C). Maximum separation between the 2 lines, for a minimum rotation (B to C = 1 mm, in the frontoparallel plane) subtends 0.05 dva (gamma ). B: schematic outline of the orientation discrimination tasks. Subjects were placed in a sound-proof room facing a monitor at 114 cm from the eyes. A trial was initiated with the presentation of the fixation target at the center of the monitor screen. Subjects were required to maintain the right hand on a key lever through a variable prestimulus delay until 2 stimuli (reference and test), each of 500 ms of duration, were presented in a temporal sequence with a fixed interstimulus interval of 1 s. Subjects had to indicate the end of the 2nd stimulus by releasing their hand from the key and pressing 1 of 2 switches at their hand level. Monkeys received a drop of water as a reward for correct discriminations. Fixed-reference task: subjects received 3 independent runs (100 trials per run) each with different reference stimuli: 85, 90, and 95°. For example, 1 run in which the reference stimulus of 90° was followed by test stimuli ranging from 85 to 95° in 1° steps. Variable-reference task: subjects received in each run 3 reference stimuli (85, 90, and 95°) presented pseudorandomly, followed by the test stimuli.

Surgery

A head holder was implanted on the monkeys' skull to fix the head during the experiments. A three-turn monocular scleral eye coil was implanted to measure gaze direction (Judge et al. 1980). All surgical procedures were carried out under general anesthesia and aseptic conditions. The animals first were anesthetized with ketamine (10 mg/kg im). This was followed by pentobarbital sodium (15 mg/kg iv) for induction and maintained with a continuous intravenous infusion of pentobarbital sodium (3.5 mg · kg-1 · h-1) and fentanyl (5.25 µg · kg-1 · h-1) in saline, at 10 ml/h. Animals were intubated and artificially ventilated with a mixture of oxygen and air. Expiratory CO2, electroencephalogram (ECG), and temperature were monitored continuously during surgery. Antibiotics and analgesics were administered after surgery.

Eye-fixation task

Monkeys were trained to perform eye fixation on a target presented on the monitor screen in front of them. The fixation stimulus was a short vertical line subtending 0.20° length and 0.05° width (luminance: 14.6 cd/m2). A masking white noise signaled the beginning of the trial. The monkeys fixated on the fixation target, pressed the lever key with his right hand, and waited until there was a small change in the angle of the vertical line. The monkeys then released the key and projected his hand to the upper middle switch. Correct performance was rewarded with a drop of water. During the fixation period, eye movements larger than 0.5° aborted the task.

Discrimination tasks

Humans and monkeys were trained to discriminate line orientations presented fovealy (Fig. 2). The stimuli were presented in the center of the monitor screen, and eye movements were restricted to a 1 × 1° window. The orientation discrimination task was a modified 2 alternative forced choice (2AFC). A trial was initiated with the presentation of the fixation target (FT, Fig. 1). Subjects pressed a lever key with the right hand through a variable prestimulus delay (PSD: 600-900 ms). Then, two stimuli (reference and test), each of 500 ms of duration, were presented in sequence, with a fixed interstimulus interval (ISI: 1 s). At the end of the second stimulus, the subject released the key, in a 1,200-ms time window, and pressed one of the two lateral switches, indicating whether the orientation of the second stimulus was clockwise or counterclockwise to the first stimulus. Monkeys were rewarded with a drop of water for correct discrimination. Humans did not receive a reward for correct discriminations although a modulation of the masking noise signaled the errors. Human's eye movements were not recorded.



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Fig. 2. Eye position during the discrimination task. Lines, subtending 3°, are presented in the center of the monitor screen (an 85° oriented line is shown here). Monkeys should maintain their gaze in a 1 × 1° window (dotted square, not displayed to the monkeys), otherwise the trial is aborted. Eye positions, sampled at 740 Hz, during stimuli presentation (4 trials) are plotted for 1 of the monkeys.

FIXED-REFERENCE TASK. We used three different runs (100 trials/run), corresponding to three different reference stimuli: 85, 90, or 95° of orientation. A reference stimulus of, e.g., 90°, was followed by a test stimulus ranging from 85 to 95° in steps of 1° for 100 trials in a randomized fashion. Then, another reference stimulus of, e.g., 95°, was followed by a test stimulus ranging from 90 to 100° in 1° steps for 100 trials, and so on. Monkeys learned this task in ~4 months. We found no transfer of discrimination learning between orientations, and for that reason we limited the reference stimulus (RS) to 85, 90, and 95°.

CONTINUOUS VARIABLE TASK. Subjects received three reference stimuli (85, 90, and 95°) presented pseudorandomly and followed by the corresponding test stimuli. Humans trained in the fixed-reference task began to perform successfully in this new task after a few trials, but monkeys needed extensive training to perform the new task successfully.

In both tasks (fixed and variable tasks), subjects classified the test stimulus as "to the right" or "to the left" of the reference stimulus. Subjects made four possible decisions that we classified as hits, misses, false alarms, and correct rejections (Macmillan and Creelman 1991). Because we have assumed that our task is symmetrical (task optimal criterion is 0), we have classified decisions as correct (hits and correct rejections) or incorrect (miss and false alarms). The criteria used by the subjects do not have to be symmetrical.

Reaction time (RT) was measured starting the termination time of the test stimulus (TS) until the key was released (Spoehr and Lehmkuhle 1982). Movement time (MovT) was measured starting from the time of key release until the target switch was pressed. RT and MovT were framed in the choice period. RT and MovT were examined only after the monkeys reached a stable performance.

We studied the effect of time factors on discrimination performance in the continuous variable task. Three new experimental blocks were introduced without previous training, each with different time duration for the RS, TS, and ISI. Reference and test stimuli duration varied independently or together, from 500 ms (the standard duration) to 300, 150, and 50 ms. The ISI was increased from 1 to 6 s, in 500-ms steps.

Data analysis

We obtained psychometric functions for humans' and monkeys' discriminations between different orientations. We plotted the percentage of test stimuli identified as oriented to the left of the reference stimuli against the orientation of the test stimulus. Data were fitted to a sigmoid curve (y = 100/{1 + exp[-(x - a0)/a1]}). Difference limen (DL), or threshold, was calculated as the value of the minimum angle that elicits 75% of correct responses.


    RESULTS
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

We found that humans and monkeys had similar capacities to discriminate the orientation of a line. The fixed-reference task proved to be ambiguous because it could be completed either by paying attention to the first stimulus or by ignoring it (i.e., categorization), and it was never known when it was completed in one way or the other. Discrimination (i.e., a judgment based on a continuous test of the reference and test stimulus) took place only when the reference and the test stimulus continuously varied through the experiment. Monkeys showed little capacity to generalize discriminations across different orientations as also was reported for grating discrimination (Vogels and Orban 1990). For that reason, humans and monkeys were required to discriminate orientations in the range of 80-100° only.

Discrimination in the fixed-reference task: human and monkey results

Human (n = 8) performance in the fixed-reference task is showed in the psychometric functions of Fig. 3A. Signal detection theory analysis was applied, obtaining sensitivities (d') and criterion (c) used by subjects. Sensitivity (d') is a measure of the signal discriminability and subjects sensory acuity. Criterion (c), "a particular magnitude of central neural effect" that the subject uses for reaching a decision (D'Amato 1970), is a measure of subjects decision bias. The inset shows the DL, sensitivity values (d'), and the criterion (c) used by the subjects. The positive values of c suggested a slight bias to assign the TS counterclockwise from the RS of 85 and 95° compared with the task optimal criterion obtained for 90° (symmetric response).



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Fig. 3. Psychometric functions obtained in the fixed-reference task. A: average results for 8 human subjects in the fixed-reference task. Data points are means of 60-90 trials and indicate the percent of trials in which the test stimulus was identified as oriented to the left of the reference stimuli. Data were fitted to a sigmoid curve, obtaining the different limen (DL). Signal detection theory analysis was applied, obtaining sensitivities (d') and criterion (c) used by subjects (d' and c data in the insets is for ±1° and ±2° for humans and monkeys, respectively). B and C: monkey BMV1 (B) and BMV2 (C) capacities to discriminate in the fixed-reference task. D: human capacity to discriminate in the fixed task when the reference stimulus was removed. E and F: monkey BMV1 (E) and BMV2 (F) capacities to discriminate in the fixed task with the reference stimulus removed.

Figure 3, B and C, shows the psychometric functions of monkeys BMV1 and BMV2 for the fixed-reference task. The DL and d' data suggest that monkeys have much higher discriminating thresholds and lower sensitivities than humans do. The criterion (c) indicates that monkeys performance is almost symmetrical (no bias).

Discrimination in the fixed-reference task with the reference removed: human and monkey results

When a signal is kept constant, subjects have a tendency to ignore it (Davies and Parasuraman 1982). We wondered whether subjects were ignoring the first stimulus in the fixed-reference task and thus categorizing the second stimulus as clockwise or counterclockwise without comparing it with the first one. To answer this question, we studied human and monkey performances in the fixed-reference task with the reference line removed so only the test stimulus was presented in each trial.

Human performance in this task was correct (unaffected by the reference stimulus) from the beginning (Fig. 3D, data in the inset). Human subjects (n = 8) were able to categorize the single TS as clockwise or counterclockwise without needing the display of a previous RS. This could suggest they were using an "internal RS representation as reference." We observed little changes in the threshold (DL) and in sensitivity (d') for 85° and 95° (without changing for 90°) when we compared the data in this task with the data obtained for the fixed-reference task. The criterion (c) that the subjects used was to decide that the TS was clockwise from the RS of 85° and counterclockwise from the RS of 95°.

Monkeys (n = 2) performance in this task was also correct (unaffected by the RS) from the beginning (Fig. 3, E and F, data in the inset). Monkeys, like humans, could be using an internal RS representation as reference because they did not need the RS to complete this task. DL and d' also indicated that thresholds and sensitivities changes very weakly in test to the fixed-reference task. The criterion showed a general bias to decide that the TS was counterclockwise from the RS, although for the RS of 95° the criterion was almost symmetrical (c < 0.001, Fig. 3, E and F). The subjects complete the fixed-reference task with the reference stimulus present or removed without significant changes in DL or d'. These results suggested that the fixed-reference task was ambiguous because it could be completed either by paying attention to the RS or not, and it is never known the strategy followed by the subjects to complete it.

Discrimination in the variable-reference task: human and monkey results

The preceding results suggested that if the two stimuli (RS and TS) were to change their orientation from trial to trial, subjects would have to compare both stimuli complete the task. We tested humans and monkeys discrimination of orientations in the variable-reference task without previous training. When they are faced for the first time with this new task, they failed to discriminate, and they seemed to ignore the reference stimulus, trying to categorize the test stimulus as to the left or right without comparing it to the reference. These results suggested that the mechanisms previously reported by Hernández et al. (1997) in the somatosensory systems also might operate in the visual system. These results also confirmed an earlier theoretical prediction (Johnson 1980).

Humans learned the new task in a few trials. Human psychometric functions in this condition are shown in Fig. 4A. DL and sensitivity (d') indicated a slight decreased in performance in test with the fixed-reference task (data in the inset, Fig. 4A). The criterion (c) indicated an almost complete lack of bias to decide if the TS was clockwise or counterclockwise from the RS.



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Fig. 4. Psychometric functions obtained in the variable-reference task. A: humans' capacity to discriminate between orientations when the orientation of the reference stimulus changed from trial to trial (variable-reference task). Data points are means of 120 trials and indicated the percent of trials on which the orientation of test stimulus was identified as to the left of the reference stimulus. Subject's performance was clearly decreased at orientations different from 90° (d' and c data in the insets is for ±1° for humans) in comparison with the fixed-reference task (Fig. 2A). B and C: monkey BMV1 (B) and BMV2 (C) capacities to discriminate between 2 oriented lines in the variable-reference task. Data points are means of 120 trials. ° (d' and c data in the insets is for ±2° for monkeys). D: results for the variable-reference task with the reference stimulus removed. Humans failed to perform discriminations in this situation. Data points (means of 30 trials) indicate that there is a tendency to decide that the test stimuli are located to both sides of an "internal reference" of 90°. E and F: data points for monkeys BMV1 (E) and BMV2 (F) in the same situation as in D. Data points are means of 30 trials. Monkeys were also unable to discriminate in this situation.

The two monkeys needed extensive training in the variable-reference task (>11 months) to learn the task. At the end of the training, monkeys performance in the variable-reference task was slightly better than in the fixed-reference task, however. This could be due to the additional training the monkeys received. In fact, the DL decreased and the d' increased (Fig. 4, B and C, inset). Figure 4, B and C, shows psychometric functions for monkeys BMV1 and BMV2 during the variable-reference task. Criterion (c) (obtained for 2°) indicates a bias to decide that the TS was clockwise from the RS of 90 and 85° and counterclockwise from the RS of 95°. The bias was nevertheless greatest for those TS that belonged to the RS of 95 and 85°. Nonoverlapped TS (from 80 to 85° and from 95 to 100°) were more accurately discriminated than overlapped TS (from 86 to 94°).

Discrimination in the variable-reference task with the reference removed: human and monkey results

Psychophysically, the fixed and the variable tasks seem qualitatively similar, as is clear when we compared the results shown in Fig. 3, A-C, with Fig. 4, A-C, respectively. In looking for differences between both tasks, we chose to remove the first stimulus (the reference) in the fixed and variable tasks and present only the test one. The rationale was that if, with this manipulation, humans and monkeys were able to complete both tasks, this would imply that the first stimulus (the reference) does not have a role to play. Nevertheless if the task were not completed in one of the versions, that would mean that the reference stimulus is necessary to complete it.

We removed the first stimulus (RS)---presenting only the second (TS)---to test whether a comparison between the second and the first stimuli was being carried out in the variable-reference task. In this situation, the second stimulus could be any one of the TS corresponding to any of the three RSs. Humans and monkeys were unable to discriminate in this condition (Fig. 4, D-F, respectively), indicating that this task can only be completed if the two stimuli are compared continuously. It can be predicted that humans and monkeys would be able to discriminate successfully between those nonoverlapped TS to the right of the RS of 85° and to the left of the RS of 95°, as we proved (Fig. 4, D-F). As expected, humans showed a high number of errors for those overlapped TSs belonging to the RS pairs of 90-95° and 90-85°; in fact all data points fall inside the chance area (Fig. 4D). The psychometric functions for monkeys showed that because most of the data points fall outside the chance area, they had the tendency to categorize the overlapped TS to the right and to the left of a---nonpresented---reference line of 90° (Fig. 4, E and F). In conclusion, because these results could only be partially predicted from the previous ones, the only way to reveal the strategy of humans and monkeys is to test them in this version of the task with the reference removed. With this manipulation, we have learned that the variable discrimination task only can be completed if the two stimuli are compared continuously on a trial-by-trial basis. This result shows fundamental differences between both tasks.

Reaction and movement times

We obtained the RTs and MovTs during the variable-reference task. Mean RT was faster for monkeys (191 ms) than for humans (233 ms) as was the mean MovT (223 ms in monkeys vs. 493 ms in humans).

RT AND MOVT DEPEND ON HIT AND MISS. RT was faster for a hit than for a miss in both primates. Humans' RT was 229 ms for a hit and 303 ms for a miss, whereas monkeys RT was 185 ms for a hit and 224 ms for a miss on average. Differences between RTs for hits and misses were statistically significant (P < 0.05, ANOVA). Humans' MovT did not vary for a hit or a miss (493 and 490 ms), but monkeys' MovT was statistically faster for a hit than for a miss (204 and 225 ms on average, respectively, P < 0.05 ANOVA). These results might indicate that decision process is extended to the movement time in monkeys but not in humans.

Influence of time factors on task performance

We addressed the question, not previously studied in monkeys, of the minimal stimulus duration required for discrimination. To get at this, we decreased the presentation time of the RS and the TS independently or both together. We tested four presentation times: 500 (standard task), 300, 150, and 50 ms. We found that human performance is very stable for all stimulus duration times (Fig. 5). Monkeys mean DLs increases by 43% for 50 ms, however (Fig. 5). The decrease in monkeys' performance for stimulus duration time of 150 and 50 ms (Fig. 6) produced an increase in standard deviation shown in Fig. 5. For 50 ms of stimulus duration time, the decreased in performance (Fig. 6) produced the DL increase shown in Fig. 5.



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Fig. 5. Discrimination capacity measured as DL of 8 humans and the 2 monkeys as a function of stimulus duration time. Data averaged over 150 trials for each stimulus duration time. Human DLs are very stable for all stimulus duration times, but monkeys' mean DLs increase from 1.5 to 2.15 (43%) for the shortest stimulus duration.



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Fig. 6. Orientation discrimination in humans (n = 8) and monkeys (n = 2) as a function of stimuli duration (500, 300, 150, and 50 ms) in the variable-reference task. Percentage of time that a test stimulus was judged as "to the left" of the reference stimulus is plotted as a function of stimuli duration. We presented orientation pairs in which the difference between the reference and test orientation was ±2°. Each line connects the orientation of the test stimuli for each reference stimulus orientation. Humans' performance was not affected by stimulus duration (data averaged over 50 trials for each subject and orientation). Monkeys showed a decrease in performance for ±2° discrimination and stimulus duration time of 150 and 50 ms.

RT increased as stimuli presentation time decreased from 500 to 50 ms (Fig. 7). The RT for a hit was shorter than for a miss in both humans and monkeys. The ratio hit RT/miss RT informs us of what relationship is between the hits and misses' RT and stimuli duration time. Because the ratio is held constant (0.213 ± 0.022) in humans and monkeys for stimuli presentation times from 500 to 150 ms, it is independent of stimulus duration time. The ratio decreased for 50 ms in monkeys but not in humans. MovT was not significantly affected by decreasing the stimuli presentation times in humans or monkeys, however. Monkeys' movement time was faster for a hit than for a miss, and these differences were similar for various stimulus presentation times.



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Fig. 7. Evolution of reaction time (RT), averaged over 150 trials, for hits and misses as a function of stimulus duration time. RT increases for both humans (n = 8) and monkeys (n = 2) as stimulus duration decreases until 150 ms. A further decrease of stimulus duration time (50 ms) increases RT in humans but not in monkeys. RT for misses is longer than for hits, and these differences decrease with reduction in stimulus duration time.

When humans and monkeys performed the variable-reference task, they seemed to pay attention to the first stimulus and store that information during the ISI to compare it with the second stimulus. This might involve a short-term or working memory process that deteriorates when using longer ISIs. We increased ISIs from 1,000 to 6,000 ms in 500-ms steps (Fig. 8). All subjects were tested without previous training with ISI 1 s. Humans' mean DL slowly increases with increments in ISI duration from 1 to 6 s, but these changes are not statistically significant (ANOVA = 0.560; Fig. 8). Monkeys performed well as ISI increased from 1 to 2.5 s in 500-ms steps, but when the ISI was increased further, they could not longer perform the task (Fig. 8). These results indicate that the mechanism that stored information about the reference stimulus with an ISI of 1 s failed to do so for longer ISIs in the monkeys.



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Fig. 8. Discrimination capacity of humans (n = 8) and monkeys (n = 2) as a function of the duration of interstimulus interval (ISI). Humans' mean DL slowly increases as ISI increases from 1 to 6 s, but these changes are not statistically significant (ANOVA = 0.560). Monkeys' DL does not change significantly (ANOVA = 0.915). With ISI longer than 2.5 s monkeys stopped working on the task.


    DISCUSSION
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

These results indicate that although humans and monkeys can complete both tasks successfully, a discrimination of the orientation of lines can only be achieved when the reference stimulus is changed randomly from trial to trial throughout the experiment. When the first stimulus did not change---and only the test stimulus varied---both humans and monkeys could complete the task by categorizing the orientation of the second stimulus without needing to pay attention to the first one, and it is unknown which strategy they followed. We are nevertheless confident that the monkeys used true discrimination and not recognition, scaling, or any other strategy (Werner 1980) because we continuously changed the orientation of the stimuli (Orban et al. 1995). Our results agree with data from the somatosensory system, where Hernández et al. (1997) showed that monkeys only "truly" discriminate the frequencies of two vibratory stimuli when both stimuli changed randomly from trial to trial. Thus differences in stimuli presentation may involve different behavioral mechanisms that are consistent in various sensory systems. Differences in task design may result in activation of neurons in different cortical areas may depend on task design, such as has been shown in the visual (Dupont et al. 1993) and somatosensory systems (Hernández et al. 1997; Mountcastle et al. 1990). These findings could have important implications for studying the brain mechanisms involved in visual discrimination and memory. To study these mechanisms, a precise knowledge of how stimuli are used by primates to complete the task becomes necessary to correlate neural activity with behavior. Our results emphasize the importance of evaluating the different strategies that subjects may use to perform a given behavioral task.

We found that human discrimination thresholds for oriented lines are between 0.4 and 1° in the variable task. Discrimination thresholds for humans for lines have been previously reported to be in the range of 0.25-1° (Orban et al. 1984; Paradiso et al. 1989; Vogels and Orban 1984; Westheimer 1996; Westheimer and Ley 1996; Westheimer and Li 1996; Westheimer and Wehrhahn 1994). These small differences between our results could be explained by the fact that we used vertical and oblique orientations, whereas Westheimer used horizontal and vertical lines with thresholds of 0.25, and 0.3-0.5°, respectively. Orban et al. (Orban et al. 1984; Vogels and Orban 1984) obtained thresholds of 0.57° for horizontal and 0.71° for vertical line orientations, and Paradiso et al. obtained thresholds between 0.55° and 1° (Paradiso et al. 1989). Our monkeys' discrimination thresholds for oriented lines are in the range of 1.5-2.3°, which is higher than the range for humans (1.5-6 times higher). To our knowledge, there are no other studies of discrimination of oriented lines in behaving monkeys for comparison. Thresholds for discrimination of orientated gratings in monkeys (1.5-4.8°) (Vogels and Orban 1990, 1994; Vogels et al. 1997) are up to six times higher than in humans (0.8-1.5°) (Heeley et al. 1997; Regan and Beverley 1985) and higher than the threshold range we found for lines. Monkeys' vernier acuity for gratings has nevertheless lower thresholds (0.03°) (Kiorpes 1992; Kiorpes et al. 1993). To sum up, discrimination thresholds for orientation in monkeys always have been found to be higher than for humans. Taking into account the similarity of retinal elements of humans and monkeys (e.g., Polyak 1957), the close morphological similarity, and the similar representation of visual space in both species (e.g., Crawford et al. 1990), other factors probably account for the above differences.

We believe that these differences reflect---aside from task design and stimulus used---the different strategies that humans and monkeys follow to complete the task. A fundamental factor is the meaning of the behavioral task for humans and monkeys. Humans were briefed at the beginning of the training sessions on how to complete the task, whereas monkeys were trained to discriminate differences in orientation to obtain a reward. We have found that both monkeys and humans usually tried to avoid a discrimination (i.e., a comparison between the 1st and the 2nd stimuli) when possible, and tried to adopt simpler strategies to complete the task, in agreement with other authors (Orban and Vogels 1998; Vogels and Orban 1993). Monkeys tried to use the more separated orientations, which are easier to discriminate than the closer ones, to get the reward. We tried to manipulate the strategy monkeys used by increasing the reward when they discriminated correctly those more difficult, closer orientations during the daily training sessions. Our psychometric functions clearly show that monkeys can discriminate orientations and that they are well trained to do that, but in the end, the strategy followed by the monkeys is reflected in the task performance. In spite of these differences, our results show that humans and monkeys have similar capacities to discriminate the orientation of lines and that both species complete the two tasks in the same qualitative way.

Some of the differences described in the preceding text between humans and monkeys also can be explained by the higher memory demand of the discrimination task. In our experiments, the variable-reference task certainly imposes a greater working load on the short-term memory than the fixed-reference task; it is also well known that attention has a profound influence on modulation of neuronal activity, and the more demanding tasks have the greatest influence (Desimone and Duncan 1995; Luck et al. 1997; Posner et al. 1978; Rees et al. 1997; Whang et al. 1991). The drop in monkeys' performance reported by Orban and Vogels (1998) when the reference grating stimulus changed during the task agrees with these results.

Humans and monkeys discriminated differences on stimuli orientations with presentation times as short as 150 ms. Monkeys' performance dropped with presentation times <150 ms. Psychometric curves and DL indicate that subjects were really making discriminations, and experimental data on human visual processing has shown that discrimination could be achieved in <150 ms (Thorpe et al. 1996).

It was our constant observation that monkeys showed no transfer in learning to discriminate line orientations, as it was reported previously for grating discrimination (Vogels and Orban 1990). In the somesthetic system, however, transfer for detection of flutter or direction of movements applied to the skin is achieved rapidly (Hernández et al. 1997; Mountcastle et al. 1972; Romo et al. 1998). One possible explanation would be that somesthetic stimuli are codified early in the primary afferent fibers (Phillips et al. 1988; Talbot et al. 1968) but orientation selectivity appears first in the primary visual cortex (Hubel and Wiesel 1962; Hubel et al. 1978).


    ACKNOWLEDGMENTS

We thank J. M. Alonso, M. J. Blanco, S. Martínez-Conde, S. L. Macknick, and R. Romo for helpful comments on reading different versions of the manuscript and S. Cendán for technical assistance.

This work was supported by Ministerio de Educación y Cultura Grants PB83-0347 and PM96-0027 to C. Acuña. P. Vázquez, and M. Cano are Formación de Personal Investigador-MEC fellows. S. Cendán is a Técnico de Formación Profesional-2 fellow, Xunta de Galicia, Spain.


    FOOTNOTES

Address for reprint requests: C. Acuña, Laboratorios de Neurociencia y Computación Neuronal, Facultad de Medicina, C/San Francisco No. 1, E-15705 Santiago de Compostela, Spain.

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

Received 4 August 1999; accepted in final form 27 January 2000.


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0022-3077/00 $5.00 Copyright © 2000 The American Physiological Society




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