Beha vioural Brahl Research, 51 (1992) 211-215 9 1992 Elsevier Science Publishers B.V. All rights reserved. 0166-4328/92/$05.00

21 1

BBR01359

Short Communications

Visual discrimination performance after lesions of the ventral lateral geniculate nucleus in pigeons (Columba livia) M a s u m i W a k i t a ~, S h i g e r u W a t a n a b e ~, T o r u S h i m i z u b'* a n d L u i z R . G . B r i t t o ~ ~Department of Psychology, Keio University, Tokyo (JapalO, hDepartment of Neurosciences, School of Medichze, University of California at San Diego. La Jolla, CA 92903 (USA) and *Department of Physiology and Biophysics, bzstitute for Biomedical Sciences, S~o Paulo, SP (Brazil) (Received 25 February 1992) (Revised version received 20 July 1992) (Accepted 21 July 1992)

Key words: Ventral lateral gcniculate nucleus; Pigeon; Color discrimination; Pattern discrimination; Subcortical visual pathway; Thalanms

Pigeons were trained to perform simultaneous pattern and color discrimination tasks. After their training was completed, bilateral electrolytic lesions were made in the ventral lateral geniculate nucleus (GLv). Following the surgery, they were retrained to their preoperative performance levels. Lesions of GLv caused no deficits in pattern discrimination performance. The birds which had been trained for discrimination of red vs. magenta showed a slight decline in their performance. This impaired performance on color discrimination was not, however, as severe as that of a bird with lesions in the nucleus rotundus. These results suggest that GLv plays some role in the detection of short wavelengths of light.

The avian ventral lateral geniculate nucleus (GLv) is a retinorecipient thalamic nucleus located immediately dorsal to the optic tract. At least some of the retinal afferents to GLv are collateral branches of axons which project to other retinal targets, including the optic teet u m 2'5'6'9"1~ In addition to the retinal input, GLv receives projections from the visual telencephaIon I~ and pretectai nuclei 7, and has reciprocal connections with tile optic tectum s'6"9. The role of the avian GLv in visual processing is still unknown. In a previous study of behavioral effects after lesions in the GLv of pigeons, no significant deficits were found in either pattern or light intensity visual discrimination t2"~3"22. Some units in the avian GLv are, however, sensitive to particular wavelengths of light z~ These data suggest that the avian GLv may play a role in color detection. A similar role has also been suggested for the GLv in mammals ~5't6. Tile purpose of the present study was to

* Present address: Department of Psychology, BEH 339, College of Art and Sciences, University of SouthFlorida, 4202 E. Fowler Avenue, Tampa, FL 33620-8200, USA. Correspondence: S. Watanabe, Department of Psychology, Kcio University, 2-15-45 Mira Minato-ku, Tokyo 108, Japan.

investigate the behavioral effects of bilateral lesions in GLv on the color discrimination by pigeons. A discrimination task of pattern stimuli was also used as a control test. As mentioned elsewhere t2't3"2z, if GLv lesion is combined with rotundal lesion, the performance in the visual discrimination task is better than the bird with damage confined to either GLv or Rt. Thus, specific effect of GLv lesion on the visual performance can be supported theoretically not only from the results of GLv-lesioned birds but also from those of birds with rotundal lesion or with combined lesion of GLv and Rt, considering the differential effects of these lesions. Four naive pigeons (Cohmlba livia) of either sex younger than 2 years old were used in the experiments. They were maintained at about 75 70 oftheir free-feeding weight. The experimental chamber was a 2-key operant chamber which was modified so that stimuli could be projected on the rear surface of the keys by an externally located slide projector. A shutter was mounted in the path of the light beam so that projection of stimuli could be blocked during the inter-trial interval (ITI). Tile keys made of opaque glass were located horizontally and their centers were at the height of 22 cm above the floor. The experiment was controlled by MSX corn-

212 puter system. The discrimination problems consisted of color and pattern discrimination tasks. There were three intensity conditions for each task which were conducted by using three N D filters (Kodak No. 96) differing by 1.00 log unit. Stimuli used in the color task were red ( F U J I CC-40R; broad-band red with peaks above ca. 620 nm) and magenta ( F U J I CC-40M; mixture of CC40R and broad band ofwavelength of light 360-500 nm with peak at 400 nm). The difference in the subjective brightness was less than 1 jnd (log 0.12) II. The N D filters paired in this task were N D 2, 3, and 4. Stimuli used in the pattern task were a vertical bar and a horizontal bar (2.0 by 0.2 mm). The pattern stimuli were black against a white field. The N D filters paired in this task were N D 1, 2, and 3. N D 4 filter was not used in this condition since it would have made the contrast between the figure and the ground severely reduced. Preoperative discrimination training was introduced after the preliminary training was completed. Seven pecks on the correct key were reinforced with access to food for 3-5 s. If the bird pecked an incorrect key four times, the trial shifted to ITI (25 s) during which the shutter was closed and the chamber was darkened. Following an incorrect response, a correction method was used to facilitate their learning. That is, the same stimulus pair was continuously presented until the bird made a correct response. Corrected responses were reinforced by the presentation of food only for 1 s. Each daily session began with a warm-up period of 12 trials. This was followed by an experimental session which consisted of 120 trials. The sequence of stimulus presentation was determined by the Gellermann sequence 8. Each of the 12 kinds of the stimulus pairs was presented once in the 12 trials. Stimulus pairs of either the same intensity-condition (ND filters), the same taskcondition (color or pattern) or the same location of correct key (left or right) were never presented successively in more than two trials. As for the location of correct side, for instance, it was determined as L (left), R (right), L, L, R, R, L, R, R, L and so forth. Response latency on each initial trial was recorded in the experimental session, in which the differential reinforcement of other-behavior (DRO) schedule followed ITI for 5 s. Thus, ITI was 30 s if the birds did not peck the key before the stimuli appeared. The criterion of discrimination was 9 0 ~ or better on the same six problems for three successive sessions. However, the criterion was 75~o on the N D 4 condition of the color task, because it seemed difficult for the birds to attain 9 0 ~ or better performance on this problem. Data from the warm-up period and the corrected trials were discarded. Within 24-48 h of achieving criterion performance,

the birds were anesthetized with ketamine injected intramuscularly. They were then placed in a stereotaxic instrument. Xylocaine was injected around the area of incision. A bilateral lesion was made in the G L v electrolytically, using coordinates obtained from an atlas of the pigeon brain xS. Bilateral lesions in the nucleus rotundus (Rt; the major thalamic nucleus of the tectofugal visual pathway) and sham lesion was conducted as controls. In the case of chemical lesions, 0.41ll of ibotenic acid in phosphate buffer (20 mg/ml) was pressure-injected bilaterally into Rt through a micropipette (0.5 mm tip diameter). Five days were allowed for a postoperative recovery period, after which the postoperative training began. In the postoperative sessions, the same procedure used in the preoperative sessions was employed until the birds again met each criterion on all conditions. When the postoperative training was completed, birds were sacrificed and their brains were histologically analyzed. Damaged volume of the structures in each brain was estimated with a weighted index: W~o x4, since unilateral lesions would have no measurable effect on the behavioral tests used as long as the subjects are permitted to view the stimuli bilaterally. Thus, volume of bilateral damage ( W ~ ) is represented as W ~ = ( L ~ x R~o) x 100, in which L~o and R ~ are the percentages of damage to the left and right sides, respectively. Saving scores were calculated on the basis of the number of sessions required to reach the criterion before and after surgery. Saving scores are defined as (Npr e -Npost)/Npre X 100, where Npr e and Npost a r e the numbers of sessions before reaching criterion sessions in the pre- and the postsurgery trainings. Thus, the saving score in N D 4 condition of color task in A-31, for instance, is calculated as {(12 - 3) - (3 - 3)}/ (12 - 3) • 100 = i00. The value of 3, which represents the number of the criterion sessions, was subtracted from the number of sessions needed to complete each task. If the number of the criterion sessions had not been subtracted, the saving score would have been calculated as ( 1 2 - 3 ) / 1 2 • 100 = 75 and the score of 100 could not have been attained even by this perfect learner. Table I presents the results of the quantitative analysis of the extent and the location of the lesion in all birds. Two pigeons (C-11, and E-13) had lesions in GLv (W~o's were 19.00~o and 59.65~o, respectively), but E-13 had lesions also in Rt ( W ~ = 7.94). One pigeon (A-31) had sham lesions and no damage in the brain. One pigeon (F-132) had lesions in Rt (W~o = 50.89~o), but only a small unilateral lesion into GLv. Table II summarizes the data of performance (number of sessions, saving score and percentage of correct

213 TABLE I

Analj'sis of the lesions, lesion o f vohtme Omn J) and percent damage to the smtcture The first column shows the total lesion volume, rcgardless of the anatomical boundaries. The remaining columns present lesions of the various thalamic regions and the optic tract. GLv, the ventral lateral geniculate nucleus; Rt, nucleus rotundus; OT, optic tract.

Birds

C-I i E-13 A-31 F-132

Target ~f lesion

GLv GLv + Rt Sham Rt

Total lesion rolume

GLr

Rt

OT other region

Volume

L%

R%

II'%

Volume

L%

R%

I 1'%

Vohm~e

Volume

4.29 5.34 0.00 15.54

0.72 1.24 0.00 0.20

34.21 72.13 0.00 19.05

55.53 82.70 0.00 0.00

19.00 59.65 0.00 0.00

0.36 1.29 0.00 4.96

15.82 27.71 0.00 56.21

0.00 28.66 0.00 90.53

0.00 7.94 0.00 50.89

2.27 0.97 0.00 0.11

0.94 1.84 0.00 10.27

TABLE 11

Summary of the trahtbtg data The first two left columns of each task indicate the numbcr of sessions nccdcd to complete the criterion sessions for the first time in the preand postoperative phases. The middle column of each task indicates saving scores based on the number of sessions required to reach the criterion before and after the surgery. The two right columns of each task indicate the mean percentage of corrcct responses of the preoperative final and the postoperative first three sessions of each task. The asterisks in F132 (Rt lesion) indicate that postoperative retraining on the color task was discontinued x~hen the number of sessions reached twice the number of sessions in the preoperative phase. Therefore corresponding saving scores could not be calculated. A double asterisk in the same bird indicates that the saving score could not bc obtained theoretically since the preoperative value in this case is thrce (although the same is true in the N D3 condition of the pattern task of A-31, we considered the saving score as 100.00 because the postoperative value was three). Bir~h

Color discrimination task Condition

Pattern discrimination task

N. of sessions

Saving

Mean % correct

Condition

N. of sessions

score

Pre-Op.

Post-Op.

Saffng

Mean % correct

score

Pre-Op.

Post-Op.

Pre-Op.

Post-Op.

Pre-Op.

Post-Op.

C-II

ND2 ND3 ND4

10 18 27

5 7 13

71.43 73.33 58.33

98.33 100.00 83.33

91.67 78.33 71.67

NDI ND2 ND3

5 9 6

3 3 6

100.00 100.00 0.00

100.00 100.00 96.67

96.67 96.67 86.67

E-13

ND2 ND3 ND4

6 9 9

3 3 6

100.00 100.00 50.00

98.33 96.67 76.67

98.33 96.67 73.33

NDI ND2 ND3

7 5 5

3 3 6

100.00 100.00 - 50.00

98.33 100.00 100.00

96.67 95.00 95.00

A-31

ND2 ND3 ND4

4 6 12

3 3 3

100.00 100.00 100.00

100.00 100.00 93.33

100.00 98.33 85.00

NDI ND2 ND3

12 5 3

3 3 3

100.00 100.00 100.00

100.00 96.67 96.67

98.33 100.00 96.67

F-132

ND2 ND3 ND4

8 12 16

20 * *

- 240.00 -

93.33 93.33 95.00

58.33 58.33 46.67

NDI ND2 ND3

7 4 3

27 21 13

- 200.00 - 170.00 **

100.00 98.33 100.00

71.67 65.00 75.00

responscs) in the preoperative last and the postoperative first three sessions. The pigeon with a sham lesion (A-31) showed no change in the saving score in both color and pattern discrimination tasks. Comparison of post-operative percentage response shows that C-I l, containing lesions in both GLv, showed a clear impaired performance compared with A-31 in color task (t2=4.108, P=0.0545) but not in pattern task (t2" 1.961, P = 0.1889). E-13, bearing large lesions of GLv but also lesions of both Rt, however, showed no

impairment in both color and pattern tasks (t2 = 1.499, P = 0.2726 and t2 = 2.498, P = 0.1298, respectively). Furthermore, the pigeon with rotundal lesions (F-132) showed severe deficits in both color and pattern tasks (t2=41.486, P=0.0006 and t,=7.144, P=0.019, respectively). This bird did not reach the criterion even after 42 sessions in the color task, when the number of sessions reached twice the number of sessions in the preoperative phase. Comparisons of saving scores with the control bird indicated that F-132 had large impair-

214 TABLE 111 Median and semi-blterquartile of response latency (s)

Medians and semi-interquartiles (enclosed value) of response latencies were represented. Difference between the postoperative median latency and the preoperative latency is also shown. Only data within the 3 S.D. range were analyzed. Birds

Color discrimination task

Pattern discrimhtation task

Condition

Pre-Op.

Post-Op.

C-11

ND2 ND3 ND4

0.766 (0.321) 0.833 (0.415) 0.866 (0.315)

1.140 (0.279) 1.408 (0.338) 1.150 (0.415)

E-13

ND2 ND3 ND4

0.950 (0.196 1.016 (0.310) 1.150 (0.300)

A-31

ND2 ND3 ND4

F-132

ND2 ND3 ND4

Difference

Condition

Pre-Op.

Post-Op.

0.347 0.575 0.284

ND1 ND2 ND3

0.933 (0.292) 0.808 (0.385) 0.833 (0.450)

0.992 (0.267) 0.883 (0.246) 1.100 (0.412)

0.059 0.075 0.267

1.033 (0.207) 1.000 (0.254) 1.283 (0.304)

0.083 - 0.016 0.133

NDI ND2 ND3

0.966 (0.181) 0.983 (0.242) 0.983 (0.229)

1.100 (0.173) 0.983 (0.104) 1.025 (0.283)

0.134 0.000 0.042

0.933 (0.109) 1.050 (0.246) 0.950 (0.204)

1.100 (0.173) 1.017 (0.198) 0.950 (0.142)

0.167 -0.033 0.000

ND1 ND2 ND3

1.183 (0.267) 0.883 (0.173) 1.090 (0.213)

1.050 (0.150) 1.017 (0.179) 1.092 (0.179)

-0.133 0.134 0.002

0.767 (0.151) 0.900 (0.208) 1.192(0.317)

1.183 (0.292) 1.100 (0.240) 1.500(0.517)

0.416 0.200 0.308

ND1 ND2 ND3

0.850 (0.127) 0.800 (0.142) 0.917(0.117)

1.150 (0.435) 1.100 (0.298) 1.150(0.404)

0.300 0.300 0.233

ments in both tasks and C-11 had an impairment only in color task ( P = 0.0206). E-13, however, had no impairment in both tasks. Table III presents medians and semi-interquartile of latencies before and after surgery. There was no difference between E-13 and A-31 in both tasks. F-132, which showed deficits in percentage correct response and saving score, also showed a deficit in the response latency in both color and pattern task (t2 = 11.547, P = 0.0074 and t2 = 3.442, P = 0.075, respectively) compared with those of the control bird. There was a slight change in color task between C-11 and A-31 (tz=2.773, P = 0.109),.whereas changes in pattern task were not significant (t2 = 1.352, P = 0.309). However, E-13 did not show any impairment in either task (t2=0.351, P = 0.7592 in color and t2 = 0.497, P = 0.6686 in pattern tasks). G L v lesions appear to affect performance only in color discrimination task, but not in pattern tasks. The deficits after the G L v lesions were not as severe as the deficit after lesions of Rt. These results are consistent with a previous study using pattern and brightness discrimination tasks by Hodos et al. ~2"~3 and Palacios et al. 22. They showed that lesions in GLv caused almost no effect in pattern and intensity discriminations while lesions in Rt caused severe deficits in the same tasks. In addition, Palacios et al. 22 recently showed that in pigeons discrimination threshold at 510 and 640 nm did not change after the bilateral lesions of GLv. Furthermore, both groups of researchers showed that com-

Difference

bined destruction of GLv and Rt produced less severe effects than those following lesions in Rt, as shown in the present study. Such results indicate a close relationship between Rt and GLv in the visual processing of birds. It was not possible to determine whether the magnitude of the deficit in the discrimination tasks was related to the size of the lesions since the number of subjects was small in the present study. Nevertheless, the present results suggest that a large lesion including the GLv did not cause severe deficits in visual discrimination performance. A small disturbance in the postoperative performance was found in our experiment of the color discrimination task, but not in the pattern discrimination tasks. The differences of the performances between our experiments and that of Paiacios et al. might be related to the different stimulus properties used in the experiments, rather than the difference in the procedure. In their experiment 510 nm (green) and 640 nm (red) of lights were used, whereas in our color discrimination task red and magenta were used. Considered with the spectral sensitivity of pigeons t, there was a discriminative range between red and magenta below 500 nm (as far as the filters used in our experiment were concerned). These facts may indicate that the detection of middle or longer wavelengths was essentially so easy for the birds that deficit in visual discrimination performance after the G L v lesion did not occur. Decrements in the percentage correct response or the saving score and longer latencies in the

215 postoperative phase would then represent a deficit in the analysis of shorter wavelengths of light. The present results are based on a single bird with lesion damage confined to the GLv. Therefore, other birds are necessary for further support of the effect of GLv lesion. Besides color detection, the GLv has been suggested for various roles in visual processing, including visuomotor integration 3'23'25, pupillary light reflex 17, and circadian rhythms4. The present results, however, may be consistent with a previous report 2~ which indicated that the avian GLv is a structure with a high percentage of color-opponent responses and that disproportionately, half of the chromatic preferences of its units are in the short wavelength end of the visible light spectrum. Therefore, there is a possibility that the avian GLv is indeed involved in the processing of the visual information related to shorter wavelengths of light. The authors thank Dr. Harvey J. Karten for his advice and support, and Ms. Cynthia K. Oldmen and Mr. Sesario V. Borlongan for editorial assistance. This work was supported by ONR Contract N00014-88-0504 and NINDS Grant NS24560 to Dr. H.J. Karten.

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