Crossmodal training reduces behavioral deficits in rats after either auditory or visual cortex lesions

Physiology& Behavior,Vol. 55, No. 2, pp. 293-300, 1994 Copyright© 1994ElsevierScienceLtd Printed in the USA. All fightsreserved 0031-9384/94 $6.00 + .00

Pergamon

Crossmodal Training Reduces Behavioral Deficits in Rats After Either Auditory or Visual Cortex Lesions EUGENE R. D E L A Y l A N D T H E O D O R

L. R U D O L P H

Department o f Psychology, Regis University, 3333 Regis Blvd., Denver, CO 80221 R e c e i v e d 17 A u g u s t 1992 DELAY, E. R. AND T. L. RUDOLPH. Crossmodal training reduces behavioral deficits in rats after either auditory or visual cortex lesions. PHYSIOL BEHAV 55(2) 293-300, 1994.--Rats were trained with either visual or auditory intensity cues until they emitted nine avoidance responses in 10 trials (9/10) prior to bilateral ablation of the corresponding sensory neocortex. Six days after surgery, rats were trained to 5/10 criterion in one of the following conditions: within-modality direct, within-morality reversal, crossmodality direct, crossmodality reversal, or no training control. The next day all rats were retrained to 9/10 on their preoperative tasks. For visual decorticate rats, the no training and the visual within-modality direct groups relearned the discrimination at the same rate as preoperative learning. Auditory crossmodal direct training enhanced relearning more than other forms of training and visual within-modality reversal training hindered retraining. For auditory decorticate rats, similar postoperative auditory within-modality and visual crossmodality training effects were seen during retraining of the auditory discrimination. These findings suggest crossmodality training facilitates functional recovery through relational information and learning sets transferred from experimental training to the relearning task. Visual cortex

Auditory cortex

Lesion

Crossmodal transfer

ONE of the most reliable effects of visual decortication in rats was described by Lashley in 1935 (19). A visual decorticate rat will emit about the same n u m b e r of responses to reach criterion on a brightness discrimination after the lesion as it did before the lesion, whereas an intact rat will show good retention of the task from one condition to the next. Research has shown that this deficit can be the result of any one of several potential costs of the lesion. For example, after visual decortication the rat may show a disturbance of luminance discriminability (12,30), a loss of associative value of a cue (amnestic sensory agnosia) (2,3), or a shift in neural control from the visual system to intact systems which interferes with behavioral functions requiring the injured visual system (20,21). An important outcome of this research is the development of techniques to reduce or alleviate behavioral deficits produced by this lesion. One potential intervention technique involves discrimination training with another sensory modality before the lesion rat relearns the visual discrimination. In a study (9) employing a preoperatively learned avoidance response, visual decorticate rats were given 20 trials of auditory intensity training the day before the brightness task was relearned. These rats reached criterion on the brightness discrimination in fewer trials than other lesion rats given 20 additional trials with the brightness task. It was thought that the auditory training enhanced the

t To whom requests for reprints should be addressed.

293

Recovery of function

Rat

performance of the lesion rats through the transfer of either a nonspecific response set or specific information regarding a c o m m o n sensory attribute (e.g., relative intensity) from the auditory system to the visual system. Unfortunately, these results can be questioned because the experimental groups did not emit an equivalent n u m b e r of avoidance responses during intervention training. For example, lesion rats that exhibited the poorest recovery of the brightness discrimination averaged about three avoidance responses during the 20 trials of intervention training, while the lesion rats with the best recovery averaged nine avoidance responses. These differences may have resulted in nonequivalent levels of learning during intervention training and, consequently, may have had a differential impact on brightness discrimination performance that was independent of sensory modality. One intent of the present study was to compare the effectiveness of postoperative visual and auditory training on recovery of visual behavior by replicating this experiment, but with each lesion rat trained to the same level of learning during intervention training. It is often assumed that conclusions derived from studies of recovery of visual functions can be generalized to the rest of the cortex, or at least to other sensory areas such as the auditory neocortex [e.g., (2,18,20,22,23)]. Yet, a recent review of the literature (15) noted that few researchers have studied the effects

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of lesions of the auditory neocortex in the rat. As a result, relatively little is known about the behavioral functions afl}ected by auditory decortication or whether recovery of these functions is similarly affected by variables known to influence recovery of functions of other sensory cortices. In an early study that followed Lashley's design (28), rats learned to localize sound prior to ablation of the auditory cortex, After surgeu, these rats exhibited relearning deficits that appeared to be due to disturbances in associational rather than basic sensory functions (2.28). In view of these data, one might presume that if auditory cortex lesions alter associational functions, then factors that affect recovery of associative behavior after visual cortex ablation, such as crossmodal transfer training, also can alter behavioral functions after auditory, decortication. However, it is possible that visual crossmodal training may not be able to affect recovery alter auditory cortex lesions because in the rat, lesions of the temporal cortex can produce retention deficits of a preoperatively acquired visual discrimination (24), or, if the lesion is made before any training, transfer of learning from a visual to an auditory intensity discrimination can be blocked (32). Thus, an intact temporal neocortex may be important for accessing visual memory or for transfer of information from the visual to the auditory, modality. Theretbre, a second intent of this study was to determine whether postoperative visual crossmodal transfer training can aid recovery' of an auditory discrimination or whether the effects of this training are blocked by the cortical lesion. The present study reexamined the effects of postoperative visual and auditory intensity discrimination training on the performance of a brightness discrimination learned before surgery. If earlier findings are accurate, then rats given auditory crossmodal transfer training should show better recovery of the brightness discrimination than lesion rats trained to the same level of learning with visual cues. in addition, if crossmodal transfer training is as effective and as robust as previously assumed, then visual intensity training will enhance recovery of an auditory intensity discrimination more than comparable auditory training. But, if the temporal cortex must be intact for visual crossmodal transfer to occur, then crossmodal transfer training will not aid postoperative performance of the auditory discrimination. METHOD

Suhjects The subjects were 140 male albino rats between 90-120 days old when the experiment began. Each rat was housed singly in the home colony with unlimited food and water. All rats were tested in the light portion of the 12:12 h light:dark cycle (lights on 0800 h).

Apparatus The test apparatus was a four-way shuttle (60 cm 2 × 57 cm high) which was painted uniformly white and was divided into quadrants by 5 cm high partitions. Each quadrant and the partitions could be electrified separately with 0.2-0.3 mA scrambled shock (6). When training with visual stimuli, a 100 W and a 15 W white incandescent light were activated. These lights were located side by side 67 cm above the center of the shuttle and covered with translucent glass. A room ventilation fan generated 48 +_ 2 dB background noise (re: 20 # N / m 2, A scale). When training with auditory stimuli, the fan was turned off and pseudorandom white noise, generated by an SN76477 (Texas Instruments) coupled to an amplifying circuit (10), was presented through two speakers mounted in opposite walls of the shuttle.

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produced 5 Ix background light, l h c rise and [all times of light and noise cues followed a negatively accelerating function in which each conditioned stimulus (CS) reached gS~ of full intensity change within 100 ms and full changc within the next 50 ms.

/>rOL'Udlll'U Because the sensory conditions used in this experiment can alter arousal levels (7) and the rate of learning of the avoidance response (1), steps were taken to minimize the impact of the test environment. Each rat was handled for 5 min and then habituated to the shuttle tbr a m i n i m u m of 10 min on 6 consecutive days before the first training session. During these habituation periods, the sensory conditions in the shuttle were alternated between 53 Ix white light and the room fan one day and the red light and 60 dB the next day. Midway through each habituation period, the rat was given two noncued escape trials to expose the rat to shock before any training. To minimize the arousal effects of the CS and background stimuli during a training session, relatively low intensity values were chosen tbr noise (60 and 72 dB) and light (53 and 270 lx) stimuli (7). In addition, each rat was habituated to the background conditions and the shuttle apparatus for 20 rain before each training session. During a trial, shock followed CS onset by 5 s. Any response that moved the rat from one quadrant to another after CS onset terminated the CS and allowed the rat to either avoid or escape shock, lntertrial intervals were random and ranged from 40 to 80 s (mean 60 s). After each session, the shuttle was cleaned with a weak ammonia-based cleaner, rinsed, and then dried. During the single preoperative training session, half of the rats were trained to emit an avoidance response when light was mcreased from 53 to 270 lx until they emitted nine avoidance responses in 10 trials (9/10). Then the rats were divided into 10 groups of seven rats each with the number of slow and last learning rats matched across groups. The rest of the rats were trained to emit avoidance responses when white noise was increased from 60 to 72 dB until they reached the 9/10 criterion. Then an equivalent number of slow- and fast-learning rats were divided among 10 groups of seven rats each. Henceforth, rats preoperatively trained with the visual CS will be identified as visual rats and those trained with the noise CS will be identified as auditory rats.

Twenty-four hours later, rats assigned to five of the visual groups received bilateral visual cortex ablations by suction under sodium pentobarbital anesthesia (50 mg/kg, IP). Each rat was given atropine sulfate (0.15 cc, 10 mg/cc, IP) to minimize salivation during surgeD' and Durapen (0.08 cc, 300,000 units/ml, 1M) to prevent infection. Similarly, five of the auditory groups received bilateral ablations of the auditory cortex. Six days after surgery, one lesion group and one control group from each CS modality were given additional training to a 5/10 criterion in one of four experimental conditions. One experimental training condition was a within-modality direct (WMD) condition in which rats received more training with their respective preoperative CS. A second condition was within-modality reversal (WMR) training in which the CS was the same modality as preoperative training but with the CS-background intensities reversed. Visual rats were given training in which CS intensity was 53 lx with 270 Ix between trials and, similarly, auditory rats were given training in which CS intensity was 60 dB with 72 dB between trials. A third experimental condition was crossmodal direct (CMD) training in which the stimuli from the opposite modality were used and, like the preoperative train-

CROSSMODEL TRANSFER AND CORTICAL LESIONS

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FIG. 1. The extent of the largest (crosshatched area) and smallest (slanted rule area) lesions of the auditory and visual cortices. ing, the CS began when the stimulus changed from low to high intensity. For example, rats initially trained with the visual CS were now trained with the 72 dB noise CS (intertrial interval intensity = 60 dB). The fourth condition was crossmodal reversal (CMR) training in which the stimuli were of the opposite modality and intensity values as preoperative training. For instance, rats with preoperative visual training now were trained with a 60 dB noise CS (intertrial interval intensity = 72 dB). The 5/10 criterion was selected rather than 9/10 to prevent the WMD groups from being completely retrained on the discrimination before the other lesion rats were given the same opportunity. Two additional groups, one lesion and one control, from each modality were assigned to a no training (NT) condition in which rats remained in the home colony. One day later (7th day postop), all rats were retrained to the 9/10 criterion on their respective preoperative task. After this session, lesion rats were sacrificed by drug overdose and perfused with formalin. A map was drawn of each lesion, frozen sections were cut at 20 um thickness, and every 10th section was stained with cresyl violet and Luxol fast blue.

RESULTS

Histological Results Figure 1 illustrates the largest and smallest lesion of each cortical area. Each rat with auditory neocortical lesions sustained damage throughout the primary and secondary auditory cortex, Tel, Te2, and Te3 (33). The lesion generally involved a small portion of the lateral occipital neocortex (Oc2L), the posterior borders of the parietal cortex (Parl), and varying amounts of the anterior areas of the perirhinal cortex (PRh). In a number of rats, some damage also was observed in the posterior portion of the agranular insular cortex (ALP) and the lateral entorhinal cortex (Ent). Degeneration was found in the medial geniculate, the dorsal lateral geniculate, and the lateral posterior nuclei. In all rats with visual cortex lesions, damage was seen throughout visual areas Oc 1, Oc2M, and most of Oc2L. Typically, the lesion extended into RSA, 29D, the posterior frontal and parietal (Parl) regions. Thalamic degeneration was evident in the dorsal lateral geniculate nucleus, nucleus lateralis posterior, and the nucleus lateralis thalami. Microscopic examination revealed that all cor-

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EXPERIMENTAL TRAINING CONDITIONS

FIG. 2. Mean trials to 9/10 criterion during preoperative learning and postoperative relearning of the control and lesion rats trained with either the auditory or visual avoidance task. Experimental training conditions: PRE = preoperative learning, NT = no training, WMD = within-modality direct, WMR = within-modality reversal, CMD = crossmodality direct, and CMR - crossmodality reversal.

tical layers a n d typically some o f the underlying radiations were damaged t h r o u g h o u t each lesion. No lesion extended into the hippocampus.

Behavioral Results Before any data were analyzed, the 10 criterion trials were subtracted from the preoperative a n d the relearning raw scores. First, the effects of lesions a n d experimental training on the prea n d postoperative raw scores as well as the trials to criterion during experimental training were analyzed separately for each modality. Then, to m a k e c o m p a r i s o n s between modalities, proportional scores derived by dividing relearning scores by preoperative scores were analyzed. Raw score analyses. A n analysis of variance o f the preoperative scores indicated that the rats learned the auditory discrimination in significantly fewer trials (mean = 20.90) than the visual discrimination (mean = 27.73), F(1, 120) = 20.06, p < 0.001 (Fig. 2), but no differences were detected a m o n g the groups within each CS morality. To assess the effects of each lesion, the preoperative a n d the relearning raw scores of the N T groups were analyzed independent of the other groups. This analysis revealed significant modality by session, F(I, 24) = 9.28, p < 0.01, a n d lesion by session, F( 1, 24) = 69.02, interactions. N e w m a n - K e u l s tests showed that the raw scores of all control rats in the second session were significantly lower t h a n the scores of the lesion rats, and the pre- a n d postoperative scores of the visual decorticate rats were equivalent, while the postoperative scores of the auditory decorticate rats were significantly higher t h a n their preoperative scores. To evaluate the effects of the experimental training conditions on postoperative performance, separate one-way between subject analyses of variance a n d post hoc tests were conducted on the raw scores for the relearning session of the control a n d the lesion groups within each modality (Fig. 2). For the visual control groups, the A N O V A procedures indicated significant training effects for the visual control groups, F(4, 30) = 5.54, p < 0.002, a n d the auditory control groups, F(3, 30) = 3.47, p < 0.02). The N e w m a n - K e u l s tests (p < 0.05) showed that within each CS sensory modality the W M R group required significantly more trials to relearn the intensity discrimination t h a n the other control groups. The analyses for the lesion groups revealed s o m e w h a t

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different findings. For the visual lesion groups, the training c~mdition effect, 1,'(4, 30) = 20.85, p < 0.001, was due lo the postoperative raw scores of the W M R lesion group that were significantly greater than all other groups and to the scores of the N I group which, in turn, were significantly higher than the scores of the W M D , C M D , and C M R groups. The training variable also altered the postoperative raw scores of the auditory lesion groups, F(4, 30) --- 20.82, p < 0.001. The raw scores of the W M R lesion group were significantly higher than the other rats and the scores of the N T group were higher than the C M D and CMR, but not the W M D lesion groups. E.vperimenlal training. The n u m b e r of trials to the 5/10 criterion for experimental training were analyzed in a similar manner but without subtracting the criterion trials, because this would have resulted in a score of zero tbr many of the rats. The threeway A N O V A indicated that effects of lesion conditions, F(1.96) - 90.66, p < 0.001, training conditions, F(3, 96) 143.45,/) < 0.001, a n d their interaction, F(3, 96) 69.27, p < ().001, were significant (Fig. 3). Lesion rats given crossmodal training required a b o u t the same n u m b e r of trials to reach criterion as their respective control groups, but lesion rats given within-modality training required more trials to reach criterion than their control groups. To study the interaction more closeb, these data were partitioned to examine the effects of experimental training on each lesion condition within the two modalities. The training conditions significantly affected the control groups lbr the auditory modality, F(3, 24) - 7.91, p < 0.01. The W M D group reached the 5/10 criterion in significantly fewer trials than the other control groups and the C M D group required fewer trials than the C M R and W M R groups. The analysis of the visual control groups indicated similar significant effects due to training, F(3, 24) = 12.06, p < 0.01. The scores tbr the W M D and the C M D control groups, while similar to each other, were significantly lower than the two reversal groups. The training conditions also significantly affected the n u m b e r of trials to criterion for the auditory lesion group, F(3, 24) - 33.52, p < 0.01, and the visual lesion groups, F(3, 24) 156.76, p < 0.01. Within both sets of lesion groups, the scores for the W M D and the C M D groups were equivalent, but significantly less than the C M R and W M R groups. In addition, the C M R groups required fewer trials to criterion than the W M R groups.

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EXPERIMENTAL TRAINING CONDITIONS

FIG. 3. Mean trials to 5/10 criterion during experimental training 6 days after surgery of the control and lesion rats trained with either the auditory or visual avoidance task. Experimental training conditions: WMD = within-modality direct, WMR = within-modality reversal, CMD = crossmodality direct, and CMR = crossmodality reversal.

CROSSMODEL TRANSFER AND CORTICAL LESIONS

Proportional score analyses. A comparison of the effects of the experimental training conditions between the two modalities could not be made directly with raw scores because there were significant differences in the rate of preoperative learning of the two tasks. Consequently, a ratio or proportional score which had been used previously (8,9) was generated for each rat by dividing the relearning score by the preoperative learning score. Thus, any score less than 1.0 would indicate savings from preoperative learning. Also, using the preoperative score as a baseline reduced between-subject variability from fast- and slow-learning rats and helped the analyses reveal some additional experimental effects. An analysis of variance examining the effects of modality, lesions, and experimental training conditions on proportional scores found all main effects and interactions significant, including the three-way interaction, F(4, 120) = 9.29, p < 0.001 (Fig. 4). To study the effects of the experimental training variable more closely, one-way analyses of variance and Newman-Keuls tests were performed on the data of each lesion condition within each modality. The experimental training condition had a significant effect on the scores of the visual control groups, F(4, 30) = 6.76, p < 0.001, and the post hoc test indicated that the WMR group had larger proportional scores than the other four control groups. A significant training condition effect, F(4, 30) = 3.69, p < 0.025, also was found for the auditory control groups, but only the WMD group had lower proportional scores than the WMR control group. The proportional scores of the auditory lesion groups also were significantly affected by training conditions, F(4, 30) = 44.33, p < 0.001, and further testing indicated that the scores for each group differed significantly (p < 0.05) from every other group in the following order, from smallest to largest: CMD, CMR, WMD, NT, and WMR. The results for the rats with visual cortex lesions showed similar group differences, F(4, 30) = 33.19, p < 0.001, except that the scores for the CMR and the WMD groups did not differ. These data were also partitioned by the experimental training variable to examine group differences within each training condition. Each of the ANOVAs for the NT, WMD, and WMR conditions found a significant interaction between modality and lesion variables: F(1, 24) = 13.50, p < 0.005; F(1, 24) = 48.72, p < 0.001; and F(1, 24) = 13.58, p < 0.005, respectively. In each of these training conditions, the proportional scores of the control groups were significantly smaller than both lesion groups and the rats with the auditory lesions had significantly higher scores than rats with visual cortex lesions. However, only the lesion variable was significant for the CMD, F(1, 24) = 13.94, p < 0.005, and the CMR, F(1, 24) = 75.46, p < 0.001, training conditions. When comparing the effectiveness of WMD and CMD training on subsequent discrimination performance, one question that needed to be examined was whether the total amount of postoperative training was different for the two training conditions. That is, did one or both experimental training conditions actually reduce the total amount of postoperative training, or should the experimental training and the relearning be viewed simply as spaced discrimination learning rather than massed learning as experienced by the NT groups. To test this, a second proportional score was computed for the WMD and CMD lesion groups to compare the total amount of postoperative training obtained by these rats with the NT lesion group of each modality. This was done by adding the raw score for experimental training to that of the relearning session and then dividing this sum by the preoperative score. These proportional scores were then compared to the previous proportional scores of the corresponding NT lesion group. The analysis of the data for the visual lesion rats detected significant differences between these groups,

297

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EXPERIMENTAL TRAINING CONDITIONS

FIG. 4. Mean proportional scores (relearning/originallearning) for the control and lesion rats trained with either the auditory or visual discriminative avoidance task. Experimental training conditions: NT = no training, WMD = within-modalitydirect, WMR = within-modality reversal, CMD = crossmodalitydirect, and CMR = crossmodalityreversal.

F(2, 18) = 3.82, p < 0.05. The scores of the NT (mean = 0.954) and WMD (mean = 1.039) groups did not differ, while the scores for the CMD group (mean = 0.704) were significantly lower than the WMD group. Similar performance differences also were found for the auditory lesion rats, F(2, 18) = 9.17, p < 0.01. While the proportional scores for the WMD rats (mean = 2.100) did not differ from the NT lesion rats (mean = 1.700), the scores for the CMD lesion group (mean = 0.996) were significantly lower than the other two groups. In effect, both sets of analyses indicated that the total amount of postoperative training for the NT and the WMD groups, while equivalent within their respective modality, was greater than the total amount of postoperative training given to the corresponding CMD groups. In summary, relearning of either a brightness discrimination or a loudness discrimination was disrupted by ablation of the corresponding sensory neocortex, although the deficit after auditory decortication was greater than the deficit after visual decortication. Raw score analyses of the relearning data indicated that WMD training reduced the relearning deficit following visual cortex lesions but not after auditory lesions. However, analysis of proportional scores showed that when experimental training trials were added to the relearning scores, the scores of the WMD lesion rats for each ablation site did not differ from the respective NT lesion group. WMR training significantly increased the relearning deficit of each cortical lesion. On the other hand, proportional score analyses indicate that CMD training significantly reduced the relearning deficit more than all other forms of experimental training atter ablation of either cortical area. Although CMR training was not as effective as CMD training, CMR training reduced the relearning deficit as much as WMD training following visual cortex lesions and significantly more than WMD training following auditory cortex lesions. DISCUSSION

While all visual decorticate rats relearned the brightness discrimination, their performance was not as efficient as that of control rats and was affected by experimental training that appeared to influence associational rather than sensory functions. As expected, the NT-lesion rats required about the same number of trials to relearn the brightness task as they did to learn the discrimination before the lesion. Even though visual WMD

298 training improved pertbrmance of lesion rats during the relearning session, proportional scores indicated that the total number of trials over the 2 days of training were similar to their preoperative score and to the performance of the NT-lesion rats. This suggests that visual WMD training was essentially the space practice equivalent to the NT condition. Earlier studies have shown that visual decorticate rats suffer decreased luminance discriminability that forces them to utilize flux cues when confronted with a brightness discrimination (30). However, in this study visual decorticate rats given the brightness reversal training not only required more trials to reach the 5/10 criterion than other groups during experimental training, but the raw scores and proportional scores of the WMR lesion group showed that they also required more training to reach criterion on the task after the lesion than before the lesion. These findings indicate that, while these rats may have suffered a loss of capacity for utilizing luminance cues (30), they also had difficulties reversing the relationship between discriminative stimuli and response outcome during visual reversal learning and, as reported by others (5,29), the reversal learning contributed interference effects detrimental to subsequent performance of the preoperatively acquired brightness discrimination. Disturbances in associational functions atier this lesion are well documented, and several theories regarding these effects have been advanced. For example, Braun (2,3) has proposed that the associative salience of a visual cue is disturbed by the lesion: that is, visual agnosia occurs when the learned significance of a visual cue (e.g., luminance) is lost after injury, and the lesion rat must relearn the discrimination with another sensory, feature (e.g., flux). Another theory, proposed by LeVere (20,21), states that cortical injury upsets the balance between neural systems and shifts functional control of behavior from the damaged system to intact systems. Thus, a visual decorticate rat will first attempt to solve a visual problem with modalities other than vision before finally returning to the less efficient, damaged visual system. In contrast to the effects of experimental training with visual cues, auditory CMD training significantly reduced the brightness discrimination deficit more than all other forms of experimental training, even though the number of intervention trials was similar to WMD training. Moreover, the relearning scores of the lesion rats given auditory CMR training were comparable to the relearning scores of the rats given visual WMD training in spite of the dimensional reversal that produced adverse effects after visual WMR training. These results are particularly important because, in contrast to a previous report (9), they were observed when the level of learning for all experimental conditions was the same. Both crossmodal training conditions produced positive, although nonequivalent, transfer effects on brightness discrimination performance. This suggests that specific as well as nonspecific transfer, characteristic of crossmodal transfer effects in intact rats (4,8,11), occurred after experimental training. Nonspecific transfer often involves a learning-to-learn response set (11,13) that generalizes from one learning situation to another similar situation. Developed from auditory intensity discrimination training, this type of learning set could help the visual decorticate rat identify new visual cues (e.g.. flux) to use in place of cues no longer available (e.g., luminance) as a result of visual agnosia (2,3), or help other visual structures such as the superior colliculus reestablish functional control over visual behavior learned prior to the injury, if a neurological imbalance exists (20,21). If only nonspecific transfer effects occurred, then CMD and CMR training should have had equivalent effects on behavior. However, crossmodal transfer also can include information about specific stimulus relationships, such as the relative intensity of discriminative cues (4,11). Typically, in specific

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transfer, the greater the similarity between thc cues of the two modalities, the better the transfer effect. In this study, evidence of specific transfer can be seen when comparing the superior brightness discrimination scores of visual decorticate lesion rats given CMD training to the scores of the lesion rats given ('MR training. Collectively, the data of the CMD and the (7'MR groups clearly show that alter visual cortex lesions auditory training generalizes to and facilitates recovery of visual behavior more effectively than equivalent visual training. In this study, lesions of the auditory neocortex included the primary and surrounding secondary auditory cortex. Although behavioral deficits have often been reported atter ablation of these areas in other species, most lesion studies with rats have dealt with sound localization and have found only minor disturbances in the perceptual ability to localize sounds (14-17). However, auditory cortex lesions in rats have been reported to disturb retrieval of a sound localization task (28) and of a brightness discrimination (24). While the results of the present study do not provide insights into sensory deficits that might follow auditory cortex lesions, the behavioral deficits exhibited by auditory decorticate rats were altered by experimental training in a manner similar to the effects of postoperative experimental training on brightness discrimination behavior. For instance, although the lesion retarded performance, all rats were able to relearn the discrimination and, although postoperative WMD reduced the relearning deficit, the performance of the auditory WMD group was similar to the NT lesion group when the postoperative experimental training and relearning scores were combined. Like visual WMR training, auditory WMR training increased the relearning deficit substantially, but not permanently. The similarities in the postoperative performance of the NT, WMD, and WMR groups for both lesion sites suggest that the conclusions regarding effects of the lesions of the visual cortex may be extended, in large part, to the effects of auditory cortex lesions in this study. That is, while there may be sensory consequences of the lesion, associative functions essential tbr relearning the loudness discrimination were clearly disrupted by ablation of the auditory neocortex. Explanations previously advanced for the effects of visual cortex lesions, such as lose of associative salience of a cue (2,3) or injury-induced shifts in functional control (20,21) from the auditory system to other intact systems, also appear to be potential explanations for the behavioral effects of auditory cortex lesions observed in this study. Importantly, lesions of the auditory cortex did not appear to adversely alter or block the effects of crossmodal transfer training. Earlier research found that naive rats with lesions of the auditory. cortex did not show evidence of transfer of learning from a brightness discrimination to an auditory intensity discrimination (32). More recent research reported that lesions of the auditory cortex or the fibers connecting the temporal cortex with the lateral entorhinal cortex (24,25) impaired retention of a visual discrimination learned before the injury. However, in this study auditory decorticate rats given visual CMD training reached the 5/10 criterion during experimental training at a rate equivalent to control groups and the 9/10 criterion in fewer trials when relearning the auditory discrimination than all other rats with auditory lesions. Moreover, although not as effective as visual CMD training, visual CMR training reduced the relearning deficit of auditory decorticate rats more than postoperative auditory WMD training. In general, visual crossmodal transfer training facilitated relearning after auditory lesions in a manner similar to the crossmodal transfer effects seen after visual cortex lesions, suggesting that visual crossmodal transfer training also produced nonspecific and specific transfer effects that enhanced perfor-

CROSSMODEL T R A N S F E R AND CORTICAL LESIONS

mance of auditory decorticate rats on the auditory intensity discrimination. Contrary to these findings, other investigators (12,17, 20,21,26) have reported that postoperative bimodal compound conditioning can produce an aberrant preference for the cues involving the noninjured sensory system that interferes with behavioral recovery. An obvious question then is why does postoperative crossmodal transfer training enhance recovery of function while postoperative bimodal c o m p o u n d conditioning does not. One major difference between crossmodal transfer and compound conditioning is the temporal relationship between stimuli. The temporal juxtaposition of compound stimuli may provide an optimum opportunity for polarizing an injury-induced response bias in a brain-injured rat which maximizes utilization of the intact modality and minimizes or blocks utilization of the injured system (20). On the other hand, crossmodal transfer training may reduce or prevent this response bias by temporally separating the stimuli and by providing successful postoperative responding with an intact system that serves as a template from which information can be derived for subsequent responding with the damaged system. Because recall of generalized skills and strategies is often less impaired by lesions than the ability to recall task-specific information (27,31), information acquired from crossmodal transfer training may be more readily available to the brain-damaged rat than within-modality information. Thus, whether postoperative multimodal training facilitates or interferes with subsequent recovery of a preoperatively

299 acquired behavior may depend upon the temporal relationship between the stimuli as well as the development of relational and nonspecific information that can be transferred between learning situations. A direct test of the importance of the temporal relationship between multimodal stimuli on recovery of function is needed, however, in view of the differences between the shuttle task used in this study and the methodologies used in compound conditioning studies. In conclusion, ablations of the visual and the auditory cortex in the rat disrupted relearning of visual and auditory intensity discriminations, respectively. In each case, the relearning deficit was essentially unaffected by postoperative training utilizing the damaged system (WMD) or was worsened (WMR). On the other hand, both forms of crossmodal transfer training reduced the deficit significantly more than the within-modality training counterpart. The similarity in the effects of CMD and CMR training on behavioral recovery after the two cortical lesions suggest that comparable nonspecific response sets and specific relational information were transferred from experimental training to subsequent discrimination behavior, and that this information may be accessible to several sensory modalities through c o m m o n processes. If this is correct, then crossmodal transfer training may be able to facilitate postoperative recovery of a broader range of behaviors than intensity discrimination. ACKNOWLEDGEMENT This research was supported by NSF Grant BNS-8909803 awarded to E. R. Delay.

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