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Retrieval of color and form during suppression of temporal cortex with cold
ELSEVIER
Behavioural Brain Research 65 (1994) 165-172
BEHAVIOURAL BRAIN RESEARCH
Research report
Retrieval of color and form during suppression of temporal cortex with cold James A. Horel* Department ~?['Anatomv and Cell Biology, SUNY Health Science Center, Syracuse, Syracuse, NY 13210, USA Received 3 January 1994; revised 15 June 1994; accepted 19 July 1994
Abstract
Five cryodes were implanted on each side over the dorsal aspect ofinferotemporal cortex (TEd) of three monkeys. They were trained on a form discrimination and three color discriminations. Suppression of TEd with cold disrupted retrieval of the color, but not the form discriminations. The animals could find the colors in a background of shifting values of gray, indicating that the suppression did not reduce their color perception to gray. They initially had great difficulty matching red to red and green to green, although that recovered with experience, The animals tended to respond to one or the other of the colors, indicating that they could perceive and discriminate them, but, either lost information about the correct stimulus, or something from past experience was interferring with performance. We suggested that cooling TEd suppresses new and recent learning of color discriminations, but it does not suppress some previous experience that intrudes upon performance of new tasks. TEd might contain episodic information about colors necessary for performance of the immediate task. Key words. Visual representation; Memory; Perception; lnferotemporal cortex
I. Introduction
lnferotemporal cortex (TE) has long been associated with object identification, but we have found that there is an important difference in this respect between the dorsal and ventral halves of TE: reversible suppression or ablation of the inferior temporal gyrus (TEv) disrupts performance of delayed match-to-sample, but suppression of dorsal TE (TEd) does not [15]. Also, TEv and TEd have different anatomical inputs from posterior visual areas [22]. TEd is the center of classical TE and is always included in the lesions that led to its hypothesized involvement in object identification. If TEd contains visual information about objects, then its suppression should disrupt retrieval of the information. However, we found that TEd suppression disrupts retrieval of some well-learned object discriminations, but not others, and different animals had difficulty with different objects, sometimes performing perfectly on them and sometimes below chance [17]. We interpreted this as indicating that TEd processes elements, or features of the visual image, not the entire image, an * Corresponding author. Fax: (1) (315) 464-8535; [email protected]; BITNET: horelj@snysyrvl.
INTERNET:
0166-4328/94%7.00 © 1994 Elsevier Science B.V. All rights reserved SSDI 0 1 6 6 - 4 3 2 8 ( 9 4 ) 0 0 0 9 4 - 8
idea derived from a formal theory of TE function by Gaffan et al. [6], however the theory did not specify what special features TE processed. We obtained evidence that stimulus size might be one feature because suppressing TEd disrupts retrieval of small, 1 ° stimuli, but not larger, 10 ° stimuli [ 10]. We suggested that TEd might be a continuation of the parvocellular system that processes detailed vision and colors [21]. Color is important for object recognition, and some neurons in TE selectively respond to color [ 19]. However, early studies found that TE destruction produces either no, or weak effects on preoperatively learned color discriminations [1,7,23,24,26]. The discriminations in these studies were very easy and did not control for differences in perceived brightness of the colors. It is often argued that deficits from TE lesions depend on the difficulty of the visual task [7,24]. Heywood et al. [9], found that TE lesions produce an impairment in postoperative learning of difficult hue discriminations; they made the discriminations difficult by using different values of the same hue, but TE animals had significant impairments on even the easiest discriminations. Heywood et al. suggested that the absence of deficits in earlier studies occurred because they did not control for reflected light, allowing the animals to
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make an intensity discrimination. That is plausible for postoperative learning where a lesion might leave the animal unable to discriminate hues and forces it to use alternatives. However, it seems unlikely for color discriminations that the animals learned initially without a lesion; colors are very salient cues for monkeys [4]. We consistently find it easier to obtain deficits on new learning with suppression in TE than on retrieval of previous learning [16,28] but we persist in using retrieval because what the animals lose from experience that they acquired with an intact brain should be a major clue to the information that TE normally contains. In contrast, new learning in the presence of a lesion can force the animals to use structures and strategies that they would not use normally. For example, monkeys can do color discriminations after removal of striate and circumstriate visual cortex [18], implicating the brainstem in functions that probably involve the cortex in normal animals. There is growing evidence of associative and memory mechanisms in TE [20,25,27] but deficits in postoperative learning of color discriminations suggest a perceptual effect that depends upon the difficulty of the discrimination, rather than an associative or memorial one that depends upon what the animals learn about colors. Also, if TE contained a representation of the associative components of a color discrimination, then TE lesions should prevent retrieval of a preoperatively learned discrimination, but that does not seem to be the case for simple color discriminations. Perhaps TE uses color to help identify objects and a simple visual discrimination might not capture the requirements of this role. This might be captured by a conditional discrimination, in which color provides the cue for the correct form. We attempted to test that idea here, but found that while TEd suppression did not affect retrieval of the form discrimination, it had unexpectedly strong effects on retrieval of a simple red-green discrimination, preventing its unambiguous use in the conditional task. This report is a further exploration of that result: we tested retrieval under T E d suppression of two additional easy color discriminations, determined whether the animals could distinguish red and green from a range of grays and whether they could match reds and greens. The results suggest that T E d might represent episodic information about colors necessary for the performance of the immediate task.
we used only two because we lost one animal. They sat in a restraining chair facing a computer monitor with a touch screen, and touched the images on the screen for a response. A feeder automatically delivered food pellets to a cup at their mouth for reward. Details of the cooling method are presented elsewhere [ 12]. Cooling was accomplished by pumping cooled methanol through loops of stainless steel tubing implanted bilaterally along the middle temporal gyrus (TEd). The cryodes were placed under sterile surgery with Telazol anesthesia, Ten cryodes, five per side, were inserted between the skull and the dura with their dorsal edge aligned along the superior temporal sulcus and their ventral extent reaching across the middle temporal gyrus. In this experiment we cooled with the anterior four cryodes, bilaterally. They were brought to 0 °C during experimental blocks, The temperature in the cortex directly under the cryodes is about 4 C at that cryode temperature and this tapers off to normal within 3 to 4 m m [ 12]. This should suppress the function of the dorsal half of the inferotemporal gyms, TEd. Fig. 1 illustrates the area estimated to be cooled by this. The cryodes are illustrated in the previous publication [ 10]. The animals were tested in alternating blocks of control and cooling trials with 6 rain intervening for the cool down or warm up periods. Pattern discrimination. A plus and a circle were used for the visual patterns. They were formed of gray on a black background. The length of the bars and the dianaeter of the circle were 33 ram, which was 8.6: of visual angle. The lines making the plus and the circle were 4 mm thick ( 1.04 ° ). The two figures appeared at eye level, 6.5 cm apart (1.7°), alternating in left-right position according to a Gellerman series [5]. The plus was designated correct. A touch to the correct stimulus was rewarded, extinguished the stimuli, and was followed by a 15-s intertrial interval. A response to the circle was not rewarded and produced a 35-s intertrial interval. Color discrimination. The colors were square patches 33 mm (8.6 °) on a side, 6.5 cm (16.9 '~) apart. At this point
2. Methods The subjects, apparatus, cooling methods and surgery have all been described in the previous publication [ 10: previous article in this issue]. Briefly we used three monkeys (Macacafascicularis) although in the final experiment
Fig. 1. Diagram of monkey brain with shaded area indicating area suppressed by cold in this experiment.
J.A.Horel / Behavioural Brain Research 65 ~1994) 165-172
we made no attempt to control for stimulus brightness. Application of the maximum values to the red, green or blue guns of the monitor produced the red, green and blue stimuli. Application of maximum values to the red and green guns produced yellow, maximum values in the red and blue guns produced magenta, and maximum values on the green and blue guns produced cyan. The first discrimination was between red and green with red correct. The second discrimination was between yellow and cyan, with yellow correct. The third discrimination was between magenta and blue with magenta correct. The animals were run in four 30-trial blocks, starting with a warm block and alternating with cold blocks. Find the color. In this experiment we attempted to determine if the animals could see the colors against a background of gray by displaying them on a range of gray backgrounds. Red or green or gray 33 mm (8.6 °) square patches were used. Red and green were 19.4 and 48.9 c d m 2 respectively, and the gray patch was 41.9 cd'\m 2. The task was to touch the patch when it appeared randomly in one of 8 positions against a background that changed in steps from white through gray to black or black through gray to white. The 8 positions were in two rows of 4 centered before the animal. The animals were tested separately on the red, green, and gray patches. The task started with the background either white or black. When it started with white, the intensity of the gray background was reduced each trial by applying equal amounts to all three color guns; when it started with black, the intensity was increased by adding equal amounts to all three guns. The range from black (zero in all three guns) to white (maximum value in all three guns) was divided into 100 steps. If the animal touched the patch, it was rewarded, the patch disappeared and the background was incremented one step (if starting with white) or decremented (if starting with black). If the animal touched the screen outside the patch, the patch disappeared, an error was recorded and the background did not change. The values of the background gray are shown in Fig. 2. The luminance measures were made with a Tektronix J 16 digital photometer with a J 6523-2, 1 = narrow angle luminance probe. A 32 bit display configuration was used for this experiment. The animals were generally run for 400 trials in which the cold was applied throughout. In one case, the animal was stopped after 300 trials. If an animal made more than 10 errors in a row, the program was stopped and switched to the opposite background series, i.e., starting at white or black. This only occurred with the gray patch. Color discrimination replication. We replicated the redgreen discrimination to see if this additional experience with these colors under cold produced some recovery. However, the intensity of the colors varied randomly from trial to trial. The luminance values for red were 19.4 and
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8.6 cd/m 2, and the two values for green were 20.8 and 8.7 cd/m 2. Everything else was exactly the same. Color matching. In this experiment we attempted to determine if the animals could match red and green. We used only the red and green stimuli, the correct stimulus varying from trial to trial according to a Gellerman series [5]. The stimulus to be matched appeared as a colored patch in the center of the screen. Upon response to it, the matching and non-matching stimuli appeared to either side, the side chosen according to a different Gellerman series from the one that chose the stimulus. The patches were 6.5 cm (16,9 °) high and 5.6 cm (14.5 °) wide with 5 mm (1.3 °) between adjacent patches when they all appeared together. The background was black. The animal's task was to respond to the patch on either side that matched the one in the middle. The sample stimulus that appeared in the middle was always at maximum brightness for that stimulus. However, the matching and non-matching stimuli, placed to either side of the sample, varied randomly in intensity, using the same values as in the red-green discrimination replication described above. At the beginning of this experiment, we lost one of the animals and results are reported for the remaining two.
3.
Results
In all of the tasks, the animals were trained until they achieved 90~°o or better in two successive days. On the color discriminations they achieved this on the first day. Since this produced no trials to criterion, Table 1 presents
J.A.Horel
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Behavioural Brain Research 65 (1994) 165-172
Table 1 Number of errors made in achieving criterion during original learning
ANIMAL
+/O
RED/GRN
YELL/CY
MAG/BL
DMS
735 824 840
80 23 13
1 5 10
3 9 8
2 2 2
171 278
the errors made in achieving criterion. On the discrimination between the plus and circle, the mean scores obtained during cooling were identical to those obtained during warm trials: 79.67 out of a possible 80 (Fig. 3). This confirms our previous finding that suppressing TEd has no effect on a visual discrimination of relatively large forms [ 10]. However, this contrasts sharply with the effects of TEd suppression on the red green discrimination. They averaged 79.33 correct out of 80 trials during the warm condition, but during cooling they averaged below chance: 36.67 out of 80 (Fig. 3, t= 9.7599, df= 2, P<0.01). We were surprised by the strength of this effect. In the experiment that preceded this one [ 10], all of the stimuli were green and two of the animals responded initially only to green during the cold, which could account for their below chance performance, so we trained and tested them on two different color discriminations. They were also impaired on a discrimination between yellow and cyan (t= 4.84, df= 2, P < 0 . 0 5 ) and between magenta and blue (t= 9.7599, df= 2, P<0.01). It is noteworthy that these
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color discriminations were easier to learn initially than the pattern discrimination where no deficit occurred during cooling (Table 1). This is yet another violation of the rule that the effects of TE lesions relate to task difficulty. Humans with achromatopsia from cortical lesions sometimes complain that the world appears to be in shades of gray, without hue [3]. To see if the animals perceived the red and green as shades of gray, we placed patches of red or green in random positions on backgrounds of varying levels of gray. If the color patch looked gray, there should be some level of background gray where they could not see it. The animals made very few errors on this task. The larger animal tended to spread its hand over the image, occasionally making careless errors by touching outside the patch first. However, errors were not clustered around some point where the luminance of the gray and the hue would match (Fig. 4). It is possible that our steps of gray were not fine enough and there was no point where luminance of the gray matched the hue. We tested that without the cold, and with a gray patch randomly placed in the same way as for the colored patches. The gray patch should disappear at some point; to the human eye it disappeared at 42 cd/m 2 and one step each side of that. Fig. 4 shows the errors made with the red, green and gray patches. They made errors on the gray patch over several steps around 42 cd/m2, but there were no similar clusters around some luminance levels for the red or green patch. With further training they would probably find the gray patch at less noticable differences, but for the present purposes, it illustrates that if the color patches resembled gray to them at all, they should have shown errors in locating it at some gray background level, and they did not. This and the matching experiment (below) suggests that the animals were distinguishing hue during TEd suppression, and their errors are due to some other phenomenon. We then replicated the red green discrimination to see if this additional experience with colors facilitated performance on the discrimination. However, this time we randomly varied the intensity of the colors (see section 2: Methods) to discourage the use of intensity to make the discrimination. Before cooling, the animals were run one day without the cold for 160 trials. Two of the animals made no errors and one animal made two on this day, but made none until 60 trials had passed. This excellent transfer to these stimuli that randomly varied in intensity, demonstrates that hue and not brightness was the significant cue in these experiments. Performance improved during cooling, averaging 78.67 out of 80 warm and 63 out of 80 cold. This difference was not significant (t = 2.17, df= 2, P>0.05). Presumably, if we had continued to test the animals during cooling, they would eventually recover completely. This confirms our impression that the differ-
J.A.Horel / Behavioural Brain Research 65 (1994) 165-172
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red and green to green. The matching and non-matching stimuli randomly varied in brightness as before. Only two animals were run on this experiment. They showed improvement over successive 30 trial blocks; to illustrate that, Fig. 5 shows the data in the 4 successive 30 trial blocks. These were run interspersed with 30 trial control blocks as before, but the four control blocks are averaged and shown separately to better show the experimental blocks. In the first 30 trials, the animals performed very poorly, but the interesting finding was that one of them consistently chose red, the stimulus that was correct in the visual discrimination, choosing green only twice in 30 trials (binomial test, P = 0.006). However, the other consistently chose green, choosing red only six times (P = 0.002.). In the first visual discrimination, they both followed green during TEd suppression, which might result from their extensive exposure to green in a previous experiment. In this experiment, red was correct in the visual discriminations, but in the matching task, where red and green randomly alternated as the correct stimulus, one animal initially followed red and the other green. It is not possible to determine whether this prior experience created the bias during TEd suppression without further experiment, but such biases do affect recall during TEd suppression [ 13 ], and it is also difficult to imagine how else to account for this below chance behavior. Nevertheless, the animals could distinguish between the colors during TEd suppression, even while performing poorly.
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A LUMINANCE e d / m z Fig. 4. Errors made in locating a red, green or gray patch on a gray background for all three animals combined. An error on each abscissa marks the approximate location of the luminance of the patch. ence between these findings and the earlier results was not because o f the failure to control intensity. The task was identical with the + O discrimination where the animals performed indistinguishably from normal, which suggests that it is not the rules o f visual discrimination tasks that TEd represents, but something specifically related to the colors. In the final experiment, we used a simultaneous matchto-sample to determine if the animals could match red to
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.I.A.Harel / Behavioural Brain Research 65 (1994) I65-172
4. Discussion In these experiments we obtained positive, but temporary effects on the retrieval of previously learned color discriminations and color matching, but completely normal performance on a form discrimination 8 ° in size during suppression of the dorsal half of TE (TEd). This normal performance on the form discrimination seems to rule out the possibility that TEd suppression interferes with the task rules of visual discriminations and suggests that it has something to do with color perception. However, simple color perception, or discrimination does not appear to be impaired. The animals could find either the red or green stimulus when it appeared against a gray background. Also, in the color matching task where the correct color alternated randomly, they consistently responded to one of the two colors initially, which means that even when impaired, they could discriminate between the stimuli. This result is consistent with the deficits on postoperative learning of color discrminations with TE lesions [8], but not with the findings on postoperative retrieval [ 1,7,23,24,26]. It has been proposed that the failure to see impairments in these early experiments was due to uncontrolled brightness cues. That cannot account for our impairment, nor for the eventual recovery that occured. Our animals were severely impaired on stimuli that differered widely in brightness, and they transferred almost without error to the same color discrimination in which brightness varied randomly. The acute nature of our lesions is an important feature of our experiment which is different from the earlier retrieval experiments. We suppressed TEd while the animals were in the midst of using it normally. We used short blocks of trials during suppression that were interspersed with blocks without suppression to encourage the normal use of TE. For the same reason, we left one full day between any two testing days on which they were run as though they were being cooled, but without the cold. The deficit obtained under these conditions suggests that color discrimination information is normally handled by TEd, but permanent removal of TE causes other areas to take over this function. However, this is not a sufficient explanation for the difference between our results and the earlier retrieval experiments: If information important for the performance of the task is in TE, it should be lost by its removal. However, close inspection of the early results reveal some important inconsistencies. For example, Meyer [ 23 ] trained four animals preoperatively on a green vs. blue discrimination. One of the animals died, so he replaced it by rushing a new one through training by giving it two sessions per day. Except for the rushed training, this ani-
real seemed identical to the others, but postoperatively, fl failed to retrieve the discrimination and showed i1o improvement over seven more weeks of training. Of the remaining three animals, two of them showed excellent retention and one lost the discrimination, but relearned it easily. This suggests that it may have been the preoperative experience that led to the sparing or loss rather than extraneous brightness cues. There are several experiments that directly addressed the question of preoperative e x p e rience: Both Orbach and Fantz [26] and Chow and Survis [l] trained monkeys on both color and simple pattern discriminations prior to TE lesions and found that postoperative retention depended upon whether they overtrained them preoperatively. We were unable to replicate this with cooling of TE, but we used complex object discriminations rather than the colors or simple patterns they used [211. We subsequently found that if we gave 4 days of experience on one of two well-known lace discriminations prior to TEd cooling that it is recalled normally, but the discrimination that was not given recent exposure could not be recalled [13]. In contrast, a few trials of prior exposure did not affect recall of object discrminations: with or without prior exposure, they retrieved some discriminations normally and others not at all [17]. These results leave a lot of unanswered questions, but they do suggest that there is something very important about the experience of the animals with the stimuli that determines whether a T t 5 lesion will disrupt its performance. Recent physiological studies also point to the importance of experience on the responsiveness of TE neurons [20,25,27]. The below chance behavior in the initial part of the red-green discrimination and the matching task is a puzzling effect that is emerging as a consistent finding with some stimuli during TEd suppression [13,17]. It is not helpful to suggest that the animals simply prefer one of the stimuli as there must be some reason for these preferences to appear with TEd suppression. One likely reason for these preferences is that they can develop from past experience with the stimuli, or past reinforcement associations. Wilson et al. [29] in a tbrm of delayed match to sample with colors, found that anterior TE lesions increased intrusion errors from previous trials, and we found that temporal pole suppression greatly increased the effects of interferring stimuli [ 16]. Also, we consistently find that new learning is more easily disrupted by TE suppression than retrieval of past learning [ 16,28]. This suggests that T E d might be representing the new task and not older ones. These findings, together with the results of prior experience discussed above, suggest that TEd might normally represent episodic information important for the task at hand, and important for learning new discriminations, and its loss incurs the use of older well-established
J.A.140rel / Behavioural Brain Research 65 (1994) 165-172
reference m e m o r y that can interfere with performance of the new task. T E d suppression p r o d u c e s extremely variable effects in the retreival o f complex images that differ in both form and color, with different animals impaired on different stimuli and the impairment sometimes changing within an animal. However, in this experiment and its c o m p a n i o n , color alone or form alone p r o d u c e d consistent and uniform results across the same animals with the same cyrodes. This suggests that in complex images the animals attend to some elements o f the figure, and the deficit will only occur if T E d represents those elements. Two o f these elements a p p e a r to be the size o f the form and its color. The picture that gradually emerges from the complex pattern o f results with T E d suppression is of a cortical visual system that has some flexibility in where it will handle information about a complex object, but some specificity as well. Similarly, neurons in T E display both stimulus selectivity with complex images, and r e s p o n d differentially to experience with them [25], Different elements o f a single complex image, and information about what to do with it, can potentially scatter widely over visual cortex. This is m o s t clearly illustrated in findings that show T E d suppression [17] or destruction [6] strongly affects performance of some complex object discriminations and have no effect on others, with different animals deficient with different stimuli. This and the recovery, suggests that, in acquisition and retrieval of a visual discriminaton, some o f the stimuli, or some features o f a complex image, are p r o c e s s e d within T E d and some outside o f it. The same animals with the same cryodes that d e m o n s t r a t e d this great variability r e s p o n d e d consistently and uniformly to colors and to small and large forms during suppression. Small forms, or details about forms, a p p e a r to be processed in T E d [10], but not larger forms. Also, it seems that T E d is the first choice for newly learned color discriminations, although other areas are cabable o f performing these functions. Whether these other areas take on this task as a result o f lesion or suppression, or whether by way o f normal experience requires determination by further research, but experience with stimuli is a m a j o r determinant o f whether T E or T E d lesion or suppression will affect retrieval o f information about them. While we failed in our attempt to determine if T E d represents colors used for object identification, the results provide promising leads as to what it does represent.
Acknowledgements This work was s u p p o r t e d by G r a n t N S 18291 from the National Institutes o f Neurological and C o m m u n i c a t i v e D i s o r d e r s and Stroke. The authors thank Connie Endres
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and D o r o t h y Joiner for their assistance in training the animals, making the cryodes and assisting in surgery.
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[28]
[29]
of complex visual forms by single neurons of monkey temporal cortex, Neuropsychologia, 31 (1993) 1t 19-1993. Orbach, J. and Fantz, R., Differential effects of temporal neocortical resections on overtrained and non-overtrained visual habits, J. Comp. Physiol. Psychol., 51 (1958) 126-129. Sobotka. S. and Ringo, J.L., Investigation of long term recognition and association memory in unit responses from inferotemporat cortex, Exp. Brain Res., 86 (1993) 28-38. Voytko, M.L., Visual learning and retention examined with reversible cold lesions of the anterior temporal lobe, Behm. Bra#l Res,, 22 (1986) 25-39. Wilson, M., Kaufman, H.M., Zieler. R.E. and Leib, J.P. Visual identification and memory in monkeys with circumscribed inferotemporal lesions, J. Comp. Physiol P~ychol., 78 (1972) 173-I78.
Behavioural Brain Research 65 (1994) 165-172
BEHAVIOURAL BRAIN RESEARCH
Research report
Retrieval of color and form during suppression of temporal cortex with cold James A. Horel* Department ~?['Anatomv and Cell Biology, SUNY Health Science Center, Syracuse, Syracuse, NY 13210, USA Received 3 January 1994; revised 15 June 1994; accepted 19 July 1994
Abstract
Five cryodes were implanted on each side over the dorsal aspect ofinferotemporal cortex (TEd) of three monkeys. They were trained on a form discrimination and three color discriminations. Suppression of TEd with cold disrupted retrieval of the color, but not the form discriminations. The animals could find the colors in a background of shifting values of gray, indicating that the suppression did not reduce their color perception to gray. They initially had great difficulty matching red to red and green to green, although that recovered with experience, The animals tended to respond to one or the other of the colors, indicating that they could perceive and discriminate them, but, either lost information about the correct stimulus, or something from past experience was interferring with performance. We suggested that cooling TEd suppresses new and recent learning of color discriminations, but it does not suppress some previous experience that intrudes upon performance of new tasks. TEd might contain episodic information about colors necessary for performance of the immediate task. Key words. Visual representation; Memory; Perception; lnferotemporal cortex
I. Introduction
lnferotemporal cortex (TE) has long been associated with object identification, but we have found that there is an important difference in this respect between the dorsal and ventral halves of TE: reversible suppression or ablation of the inferior temporal gyrus (TEv) disrupts performance of delayed match-to-sample, but suppression of dorsal TE (TEd) does not [15]. Also, TEv and TEd have different anatomical inputs from posterior visual areas [22]. TEd is the center of classical TE and is always included in the lesions that led to its hypothesized involvement in object identification. If TEd contains visual information about objects, then its suppression should disrupt retrieval of the information. However, we found that TEd suppression disrupts retrieval of some well-learned object discriminations, but not others, and different animals had difficulty with different objects, sometimes performing perfectly on them and sometimes below chance [17]. We interpreted this as indicating that TEd processes elements, or features of the visual image, not the entire image, an * Corresponding author. Fax: (1) (315) 464-8535; [email protected]; BITNET: horelj@snysyrvl.
INTERNET:
0166-4328/94%7.00 © 1994 Elsevier Science B.V. All rights reserved SSDI 0 1 6 6 - 4 3 2 8 ( 9 4 ) 0 0 0 9 4 - 8
idea derived from a formal theory of TE function by Gaffan et al. [6], however the theory did not specify what special features TE processed. We obtained evidence that stimulus size might be one feature because suppressing TEd disrupts retrieval of small, 1 ° stimuli, but not larger, 10 ° stimuli [ 10]. We suggested that TEd might be a continuation of the parvocellular system that processes detailed vision and colors [21]. Color is important for object recognition, and some neurons in TE selectively respond to color [ 19]. However, early studies found that TE destruction produces either no, or weak effects on preoperatively learned color discriminations [1,7,23,24,26]. The discriminations in these studies were very easy and did not control for differences in perceived brightness of the colors. It is often argued that deficits from TE lesions depend on the difficulty of the visual task [7,24]. Heywood et al. [9], found that TE lesions produce an impairment in postoperative learning of difficult hue discriminations; they made the discriminations difficult by using different values of the same hue, but TE animals had significant impairments on even the easiest discriminations. Heywood et al. suggested that the absence of deficits in earlier studies occurred because they did not control for reflected light, allowing the animals to
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make an intensity discrimination. That is plausible for postoperative learning where a lesion might leave the animal unable to discriminate hues and forces it to use alternatives. However, it seems unlikely for color discriminations that the animals learned initially without a lesion; colors are very salient cues for monkeys [4]. We consistently find it easier to obtain deficits on new learning with suppression in TE than on retrieval of previous learning [16,28] but we persist in using retrieval because what the animals lose from experience that they acquired with an intact brain should be a major clue to the information that TE normally contains. In contrast, new learning in the presence of a lesion can force the animals to use structures and strategies that they would not use normally. For example, monkeys can do color discriminations after removal of striate and circumstriate visual cortex [18], implicating the brainstem in functions that probably involve the cortex in normal animals. There is growing evidence of associative and memory mechanisms in TE [20,25,27] but deficits in postoperative learning of color discriminations suggest a perceptual effect that depends upon the difficulty of the discrimination, rather than an associative or memorial one that depends upon what the animals learn about colors. Also, if TE contained a representation of the associative components of a color discrimination, then TE lesions should prevent retrieval of a preoperatively learned discrimination, but that does not seem to be the case for simple color discriminations. Perhaps TE uses color to help identify objects and a simple visual discrimination might not capture the requirements of this role. This might be captured by a conditional discrimination, in which color provides the cue for the correct form. We attempted to test that idea here, but found that while TEd suppression did not affect retrieval of the form discrimination, it had unexpectedly strong effects on retrieval of a simple red-green discrimination, preventing its unambiguous use in the conditional task. This report is a further exploration of that result: we tested retrieval under T E d suppression of two additional easy color discriminations, determined whether the animals could distinguish red and green from a range of grays and whether they could match reds and greens. The results suggest that T E d might represent episodic information about colors necessary for the performance of the immediate task.
we used only two because we lost one animal. They sat in a restraining chair facing a computer monitor with a touch screen, and touched the images on the screen for a response. A feeder automatically delivered food pellets to a cup at their mouth for reward. Details of the cooling method are presented elsewhere [ 12]. Cooling was accomplished by pumping cooled methanol through loops of stainless steel tubing implanted bilaterally along the middle temporal gyrus (TEd). The cryodes were placed under sterile surgery with Telazol anesthesia, Ten cryodes, five per side, were inserted between the skull and the dura with their dorsal edge aligned along the superior temporal sulcus and their ventral extent reaching across the middle temporal gyrus. In this experiment we cooled with the anterior four cryodes, bilaterally. They were brought to 0 °C during experimental blocks, The temperature in the cortex directly under the cryodes is about 4 C at that cryode temperature and this tapers off to normal within 3 to 4 m m [ 12]. This should suppress the function of the dorsal half of the inferotemporal gyms, TEd. Fig. 1 illustrates the area estimated to be cooled by this. The cryodes are illustrated in the previous publication [ 10]. The animals were tested in alternating blocks of control and cooling trials with 6 rain intervening for the cool down or warm up periods. Pattern discrimination. A plus and a circle were used for the visual patterns. They were formed of gray on a black background. The length of the bars and the dianaeter of the circle were 33 ram, which was 8.6: of visual angle. The lines making the plus and the circle were 4 mm thick ( 1.04 ° ). The two figures appeared at eye level, 6.5 cm apart (1.7°), alternating in left-right position according to a Gellerman series [5]. The plus was designated correct. A touch to the correct stimulus was rewarded, extinguished the stimuli, and was followed by a 15-s intertrial interval. A response to the circle was not rewarded and produced a 35-s intertrial interval. Color discrimination. The colors were square patches 33 mm (8.6 °) on a side, 6.5 cm (16.9 '~) apart. At this point
2. Methods The subjects, apparatus, cooling methods and surgery have all been described in the previous publication [ 10: previous article in this issue]. Briefly we used three monkeys (Macacafascicularis) although in the final experiment
Fig. 1. Diagram of monkey brain with shaded area indicating area suppressed by cold in this experiment.
J.A.Horel / Behavioural Brain Research 65 ~1994) 165-172
we made no attempt to control for stimulus brightness. Application of the maximum values to the red, green or blue guns of the monitor produced the red, green and blue stimuli. Application of maximum values to the red and green guns produced yellow, maximum values in the red and blue guns produced magenta, and maximum values on the green and blue guns produced cyan. The first discrimination was between red and green with red correct. The second discrimination was between yellow and cyan, with yellow correct. The third discrimination was between magenta and blue with magenta correct. The animals were run in four 30-trial blocks, starting with a warm block and alternating with cold blocks. Find the color. In this experiment we attempted to determine if the animals could see the colors against a background of gray by displaying them on a range of gray backgrounds. Red or green or gray 33 mm (8.6 °) square patches were used. Red and green were 19.4 and 48.9 c d m 2 respectively, and the gray patch was 41.9 cd'\m 2. The task was to touch the patch when it appeared randomly in one of 8 positions against a background that changed in steps from white through gray to black or black through gray to white. The 8 positions were in two rows of 4 centered before the animal. The animals were tested separately on the red, green, and gray patches. The task started with the background either white or black. When it started with white, the intensity of the gray background was reduced each trial by applying equal amounts to all three color guns; when it started with black, the intensity was increased by adding equal amounts to all three guns. The range from black (zero in all three guns) to white (maximum value in all three guns) was divided into 100 steps. If the animal touched the patch, it was rewarded, the patch disappeared and the background was incremented one step (if starting with white) or decremented (if starting with black). If the animal touched the screen outside the patch, the patch disappeared, an error was recorded and the background did not change. The values of the background gray are shown in Fig. 2. The luminance measures were made with a Tektronix J 16 digital photometer with a J 6523-2, 1 = narrow angle luminance probe. A 32 bit display configuration was used for this experiment. The animals were generally run for 400 trials in which the cold was applied throughout. In one case, the animal was stopped after 300 trials. If an animal made more than 10 errors in a row, the program was stopped and switched to the opposite background series, i.e., starting at white or black. This only occurred with the gray patch. Color discrimination replication. We replicated the redgreen discrimination to see if this additional experience with these colors under cold produced some recovery. However, the intensity of the colors varied randomly from trial to trial. The luminance values for red were 19.4 and
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8.6 cd/m 2, and the two values for green were 20.8 and 8.7 cd/m 2. Everything else was exactly the same. Color matching. In this experiment we attempted to determine if the animals could match red and green. We used only the red and green stimuli, the correct stimulus varying from trial to trial according to a Gellerman series [5]. The stimulus to be matched appeared as a colored patch in the center of the screen. Upon response to it, the matching and non-matching stimuli appeared to either side, the side chosen according to a different Gellerman series from the one that chose the stimulus. The patches were 6.5 cm (16,9 °) high and 5.6 cm (14.5 °) wide with 5 mm (1.3 °) between adjacent patches when they all appeared together. The background was black. The animal's task was to respond to the patch on either side that matched the one in the middle. The sample stimulus that appeared in the middle was always at maximum brightness for that stimulus. However, the matching and non-matching stimuli, placed to either side of the sample, varied randomly in intensity, using the same values as in the red-green discrimination replication described above. At the beginning of this experiment, we lost one of the animals and results are reported for the remaining two.
3.
Results
In all of the tasks, the animals were trained until they achieved 90~°o or better in two successive days. On the color discriminations they achieved this on the first day. Since this produced no trials to criterion, Table 1 presents
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Behavioural Brain Research 65 (1994) 165-172
Table 1 Number of errors made in achieving criterion during original learning
ANIMAL
+/O
RED/GRN
YELL/CY
MAG/BL
DMS
735 824 840
80 23 13
1 5 10
3 9 8
2 2 2
171 278
the errors made in achieving criterion. On the discrimination between the plus and circle, the mean scores obtained during cooling were identical to those obtained during warm trials: 79.67 out of a possible 80 (Fig. 3). This confirms our previous finding that suppressing TEd has no effect on a visual discrimination of relatively large forms [ 10]. However, this contrasts sharply with the effects of TEd suppression on the red green discrimination. They averaged 79.33 correct out of 80 trials during the warm condition, but during cooling they averaged below chance: 36.67 out of 80 (Fig. 3, t= 9.7599, df= 2, P<0.01). We were surprised by the strength of this effect. In the experiment that preceded this one [ 10], all of the stimuli were green and two of the animals responded initially only to green during the cold, which could account for their below chance performance, so we trained and tested them on two different color discriminations. They were also impaired on a discrimination between yellow and cyan (t= 4.84, df= 2, P < 0 . 0 5 ) and between magenta and blue (t= 9.7599, df= 2, P<0.01). It is noteworthy that these
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color discriminations were easier to learn initially than the pattern discrimination where no deficit occurred during cooling (Table 1). This is yet another violation of the rule that the effects of TE lesions relate to task difficulty. Humans with achromatopsia from cortical lesions sometimes complain that the world appears to be in shades of gray, without hue [3]. To see if the animals perceived the red and green as shades of gray, we placed patches of red or green in random positions on backgrounds of varying levels of gray. If the color patch looked gray, there should be some level of background gray where they could not see it. The animals made very few errors on this task. The larger animal tended to spread its hand over the image, occasionally making careless errors by touching outside the patch first. However, errors were not clustered around some point where the luminance of the gray and the hue would match (Fig. 4). It is possible that our steps of gray were not fine enough and there was no point where luminance of the gray matched the hue. We tested that without the cold, and with a gray patch randomly placed in the same way as for the colored patches. The gray patch should disappear at some point; to the human eye it disappeared at 42 cd/m 2 and one step each side of that. Fig. 4 shows the errors made with the red, green and gray patches. They made errors on the gray patch over several steps around 42 cd/m2, but there were no similar clusters around some luminance levels for the red or green patch. With further training they would probably find the gray patch at less noticable differences, but for the present purposes, it illustrates that if the color patches resembled gray to them at all, they should have shown errors in locating it at some gray background level, and they did not. This and the matching experiment (below) suggests that the animals were distinguishing hue during TEd suppression, and their errors are due to some other phenomenon. We then replicated the red green discrimination to see if this additional experience with colors facilitated performance on the discrimination. However, this time we randomly varied the intensity of the colors (see section 2: Methods) to discourage the use of intensity to make the discrimination. Before cooling, the animals were run one day without the cold for 160 trials. Two of the animals made no errors and one animal made two on this day, but made none until 60 trials had passed. This excellent transfer to these stimuli that randomly varied in intensity, demonstrates that hue and not brightness was the significant cue in these experiments. Performance improved during cooling, averaging 78.67 out of 80 warm and 63 out of 80 cold. This difference was not significant (t = 2.17, df= 2, P>0.05). Presumably, if we had continued to test the animals during cooling, they would eventually recover completely. This confirms our impression that the differ-
J.A.Horel / Behavioural Brain Research 65 (1994) 165-172
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red and green to green. The matching and non-matching stimuli randomly varied in brightness as before. Only two animals were run on this experiment. They showed improvement over successive 30 trial blocks; to illustrate that, Fig. 5 shows the data in the 4 successive 30 trial blocks. These were run interspersed with 30 trial control blocks as before, but the four control blocks are averaged and shown separately to better show the experimental blocks. In the first 30 trials, the animals performed very poorly, but the interesting finding was that one of them consistently chose red, the stimulus that was correct in the visual discrimination, choosing green only twice in 30 trials (binomial test, P = 0.006). However, the other consistently chose green, choosing red only six times (P = 0.002.). In the first visual discrimination, they both followed green during TEd suppression, which might result from their extensive exposure to green in a previous experiment. In this experiment, red was correct in the visual discriminations, but in the matching task, where red and green randomly alternated as the correct stimulus, one animal initially followed red and the other green. It is not possible to determine whether this prior experience created the bias during TEd suppression without further experiment, but such biases do affect recall during TEd suppression [ 13 ], and it is also difficult to imagine how else to account for this below chance behavior. Nevertheless, the animals could distinguish between the colors during TEd suppression, even while performing poorly.
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A LUMINANCE e d / m z Fig. 4. Errors made in locating a red, green or gray patch on a gray background for all three animals combined. An error on each abscissa marks the approximate location of the luminance of the patch. ence between these findings and the earlier results was not because o f the failure to control intensity. The task was identical with the + O discrimination where the animals performed indistinguishably from normal, which suggests that it is not the rules o f visual discrimination tasks that TEd represents, but something specifically related to the colors. In the final experiment, we used a simultaneous matchto-sample to determine if the animals could match red to
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.I.A.Harel / Behavioural Brain Research 65 (1994) I65-172
4. Discussion In these experiments we obtained positive, but temporary effects on the retrieval of previously learned color discriminations and color matching, but completely normal performance on a form discrimination 8 ° in size during suppression of the dorsal half of TE (TEd). This normal performance on the form discrimination seems to rule out the possibility that TEd suppression interferes with the task rules of visual discriminations and suggests that it has something to do with color perception. However, simple color perception, or discrimination does not appear to be impaired. The animals could find either the red or green stimulus when it appeared against a gray background. Also, in the color matching task where the correct color alternated randomly, they consistently responded to one of the two colors initially, which means that even when impaired, they could discriminate between the stimuli. This result is consistent with the deficits on postoperative learning of color discrminations with TE lesions [8], but not with the findings on postoperative retrieval [ 1,7,23,24,26]. It has been proposed that the failure to see impairments in these early experiments was due to uncontrolled brightness cues. That cannot account for our impairment, nor for the eventual recovery that occured. Our animals were severely impaired on stimuli that differered widely in brightness, and they transferred almost without error to the same color discrimination in which brightness varied randomly. The acute nature of our lesions is an important feature of our experiment which is different from the earlier retrieval experiments. We suppressed TEd while the animals were in the midst of using it normally. We used short blocks of trials during suppression that were interspersed with blocks without suppression to encourage the normal use of TE. For the same reason, we left one full day between any two testing days on which they were run as though they were being cooled, but without the cold. The deficit obtained under these conditions suggests that color discrimination information is normally handled by TEd, but permanent removal of TE causes other areas to take over this function. However, this is not a sufficient explanation for the difference between our results and the earlier retrieval experiments: If information important for the performance of the task is in TE, it should be lost by its removal. However, close inspection of the early results reveal some important inconsistencies. For example, Meyer [ 23 ] trained four animals preoperatively on a green vs. blue discrimination. One of the animals died, so he replaced it by rushing a new one through training by giving it two sessions per day. Except for the rushed training, this ani-
real seemed identical to the others, but postoperatively, fl failed to retrieve the discrimination and showed i1o improvement over seven more weeks of training. Of the remaining three animals, two of them showed excellent retention and one lost the discrimination, but relearned it easily. This suggests that it may have been the preoperative experience that led to the sparing or loss rather than extraneous brightness cues. There are several experiments that directly addressed the question of preoperative e x p e rience: Both Orbach and Fantz [26] and Chow and Survis [l] trained monkeys on both color and simple pattern discriminations prior to TE lesions and found that postoperative retention depended upon whether they overtrained them preoperatively. We were unable to replicate this with cooling of TE, but we used complex object discriminations rather than the colors or simple patterns they used [211. We subsequently found that if we gave 4 days of experience on one of two well-known lace discriminations prior to TEd cooling that it is recalled normally, but the discrimination that was not given recent exposure could not be recalled [13]. In contrast, a few trials of prior exposure did not affect recall of object discrminations: with or without prior exposure, they retrieved some discriminations normally and others not at all [17]. These results leave a lot of unanswered questions, but they do suggest that there is something very important about the experience of the animals with the stimuli that determines whether a T t 5 lesion will disrupt its performance. Recent physiological studies also point to the importance of experience on the responsiveness of TE neurons [20,25,27]. The below chance behavior in the initial part of the red-green discrimination and the matching task is a puzzling effect that is emerging as a consistent finding with some stimuli during TEd suppression [13,17]. It is not helpful to suggest that the animals simply prefer one of the stimuli as there must be some reason for these preferences to appear with TEd suppression. One likely reason for these preferences is that they can develop from past experience with the stimuli, or past reinforcement associations. Wilson et al. [29] in a tbrm of delayed match to sample with colors, found that anterior TE lesions increased intrusion errors from previous trials, and we found that temporal pole suppression greatly increased the effects of interferring stimuli [ 16]. Also, we consistently find that new learning is more easily disrupted by TE suppression than retrieval of past learning [ 16,28]. This suggests that T E d might be representing the new task and not older ones. These findings, together with the results of prior experience discussed above, suggest that TEd might normally represent episodic information important for the task at hand, and important for learning new discriminations, and its loss incurs the use of older well-established
J.A.140rel / Behavioural Brain Research 65 (1994) 165-172
reference m e m o r y that can interfere with performance of the new task. T E d suppression p r o d u c e s extremely variable effects in the retreival o f complex images that differ in both form and color, with different animals impaired on different stimuli and the impairment sometimes changing within an animal. However, in this experiment and its c o m p a n i o n , color alone or form alone p r o d u c e d consistent and uniform results across the same animals with the same cyrodes. This suggests that in complex images the animals attend to some elements o f the figure, and the deficit will only occur if T E d represents those elements. Two o f these elements a p p e a r to be the size o f the form and its color. The picture that gradually emerges from the complex pattern o f results with T E d suppression is of a cortical visual system that has some flexibility in where it will handle information about a complex object, but some specificity as well. Similarly, neurons in T E display both stimulus selectivity with complex images, and r e s p o n d differentially to experience with them [25], Different elements o f a single complex image, and information about what to do with it, can potentially scatter widely over visual cortex. This is m o s t clearly illustrated in findings that show T E d suppression [17] or destruction [6] strongly affects performance of some complex object discriminations and have no effect on others, with different animals deficient with different stimuli. This and the recovery, suggests that, in acquisition and retrieval of a visual discriminaton, some o f the stimuli, or some features o f a complex image, are p r o c e s s e d within T E d and some outside o f it. The same animals with the same cryodes that d e m o n s t r a t e d this great variability r e s p o n d e d consistently and uniformly to colors and to small and large forms during suppression. Small forms, or details about forms, a p p e a r to be processed in T E d [10], but not larger forms. Also, it seems that T E d is the first choice for newly learned color discriminations, although other areas are cabable o f performing these functions. Whether these other areas take on this task as a result o f lesion or suppression, or whether by way o f normal experience requires determination by further research, but experience with stimuli is a m a j o r determinant o f whether T E or T E d lesion or suppression will affect retrieval o f information about them. While we failed in our attempt to determine if T E d represents colors used for object identification, the results provide promising leads as to what it does represent.
Acknowledgements This work was s u p p o r t e d by G r a n t N S 18291 from the National Institutes o f Neurological and C o m m u n i c a t i v e D i s o r d e r s and Stroke. The authors thank Connie Endres
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and D o r o t h y Joiner for their assistance in training the animals, making the cryodes and assisting in surgery.
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