- Email: [email protected]
Monocular visual discrimination in the goldfish after unilateral ablation of the optic tectum
EXPERIMENTAL
NEUROLOGY
98,659-663 (1987)
RESEARCH
NOTE
Monocular Visual Discrimination in the Goldfish after Unilateral Ablation of the Optic Tectum J.PAULHEMSLEYANDGEORGEE.
SAVAGE
School of Biological Sciences, Queen Mary College, University of London, Mile End Road, London El 4NS, United Kingdom Received September 5, 1986; revision received May 18, 1987 Goldfish with unilateral ablation of the optic tectum and trained to the ablated side failed to learn or to transfer interocularly a differential classically conditioned color discrimination. The direct ipsilateral retinal projection to the intact/naive side is therefore shown to contribute little to engram formation. Evidence is also presented demonstrating that the absence of one tectum does not atfect the learning of a differential bar discrimination task when trained via the intact brain side. o 1987 Academic Press. Inc.
Each hemisphere of the mammalian brain receives retinal fibers from both eyes, hence the interocular transfer of visual discriminations becomes dependent on interhemispheric connections only in the split-chiasm animal. In fish it has been generally assumed that the retinofugal pathways undergo a complete decussation at the chiasm and synapse in the optic tectum contralateral to the eye of origin; therefore information transfer necessarily implicates commissural systems. However, in addition to the contralateral optic input, a number of workers have reported direct ipsilateral projections to the diencephalon and preoptic regions ( lo- 12). In Carassius, Springer and Landreth (11) describe three ipsilateral pathways, a rostral, nondecussating fascicle entering the medial portion of the ipsilateral optic tract and two groups of fibers which recross the midline above the chiasm. The first of these Abbreviation: DQ-discrimination
quotient.
659 0014-4886/87 $3.00 Copyright 8 1987 by Academic Press, Inc. All rights of reproduction in any form reserved.
660
HEMSLEY
AND
SAVAGE
traverses the posterior commissure and distributes to dorsal thalamic as well as pretectal nuclei. A second group of redecussating axons courses through the minor commissure and terminates in preoptic regions. There is no evidence that either of these ipsilateral projections is effective in engram forrnation and fish are able to learn conflicting discriminations of pattern or color with opposite eyes (7). Information arriving via these pathways does not interfere with the discrimination learning based on the direct contralateral input. This assumption is central to previous studies of interocular transfer in fish (3-9,13- 15) and is verified in the experiments reported here. The left optic tectum was removed in five goldfish (Curussius auratus) using techniques detailed elsewhere (1, 2). Five fish also received a sham operation. Comparison of monocular training in these animals provides an opportunity to assess the relative roles of the ipsilateral and contralateral projections in memory formation. Each fish was trained, to the right eye on a red/green color discrimination ( 17” X lo” visual angle) using a differential cardiac conditioning procedure standardized in our laboratory (3). Testing for discrimination via the left eye (intact brain half) indicates the capacity of the ipsilateral projection to contribute to memory formation. Within 1 h after completion of color discrimination testing the intact brain half of shamand tectal-operated animals received training on a differential bar orientation task (lo” X 2” visual angle). The discrimination performance for a block of 10 training trials (5 reinforced, 5 nonreinforced) and the 10 unreinforced transfer trials to the opposite eye for each task is shown by the discrimination quotient (DQ) DQ=
Mean cardiac deceleration to reinforced stimulus Mean cardiac deceleration to nonreinforced stimulus .
Therefore, a DQ < 1 indicates an incorrect/reverse discrimination and a DQ > 1 a correct discrimination (14, 15). Results for all fish are presented in Fig. 1 and Table 1. The data show that the rate of learning on the color task differed considerably between shamand tectal-operated groups. Animals with tectal ablation and trained to the same side failed to acquire the discrimination and more significantly also failed to discriminate the stimuli when presented to the intact side even though the ipsilateral input was functional. A comparison of DQ values for the final 30 training trials and 10 transfer trials (intact side) for the two groups showed a significant difference (Table 1). The deficits in discrimination performance by the intact side were not due to any inteference effects caused by absence of the contralateral tectum as direct training of the intact side (bar task) led to good acquisition. DQ values and trials to criterion for the two groups were not significantly different (Table 1).
INTEROCULAR
TRANSFER
661
IN GOLDFISH
TRIALS
FIG. 1. Learning curves for the tectal-ablated and sham-operated fish. Closed circles represent the results for animals trained on the red/green color discrimination via the ablated tectum, open circles for sham-operated fish trained on the same task. The discrimination performance ofthe untrained side was tested (TR) and after a break of60 mitt tectal-operated fish were trained to the intact tectum (closed triangles) and sham-operated to the previously untrained side (open triangles) with a horizontal vs. vertical bar discrimination task.
The untrained brain side received only a direct ipsilateral projection because the tectum was absent from the contralateral (trained) side. This ipsilateral projection is unlikely to contribute to engram formation since fish
TABLE 1 Mean Results + Standard Error for Fish with Unilateral Ablation of Left Optic Tectum Color discrimination Train to Trials to criterion“
Ablated side (N= 5)
Sham (N= 5)
Not reached 56 + 2.5 (U = 0, P = 0.004)
Bar discrimination Intact tectum (N=5)
Sham (N=5)
60 f 6.3 56 rk 5.0 (U = 10, P = 0.345)
Wb
Last 30 trials
0.36 -t 0.2
3.5k2.1
(II = 0, P = 0.004)
Transfer
0.6 t- 0.29 (u=o,P=o.oo4)
3.2 + 0.9
2.7 * 0.2 3.1 -to.3 (U=8,P=O.21) 0.29 f 0.1 2.9 I!I0.3 (cl= 10, P= 0.345)
LICriterion was attained when three successiveDQ values z 2 were recorded. Figures in parentheses are probability values obtained using the Mann-Whitney rank order test to compare tectal and sham-operated fish. b Discrimination quotient.
662
HEMSLEY
AND SAVAGE
tested via this side but trained to the opposite tectal ablated side showed poor discrimination. Therefore, following monocular acquisition the demonstration of a trained response when testing the naive eye correctly implicates commissural systems in cross-brain transfer. Moreover, there is no evidence that the rate nor asymptote of learning is affected by unilateral tectal ablation when the subject is trained to the intact side. This argues against a bilateral participation in memory formation but not necessarily against bilateral engram deposition. The naive side may simply receive an engram when acquisition is complete rather than participating actively in its formation. This distinction is upheld by previous results showing that (i) there is no difference in the rate of learning between control goldfish and those trained following transection of the commissure subserving transfer of either color (3) or shape (3, 4, 13, 14) information, and (ii) memory is present in both naive and trained sides when monocular conditioning is followed by commissurotomy (5, 13). In contrast, Dunn-Meynell (1) argued that fish with half tectal ablation were slower in learning than control subjects. This was interpreted as evidence for bilateral learning mechanisms but may in fact be due to interference effects caused by reorganisation of tectum on the ablated side. REFERENCES 1. DUNN-MEYNELL, A. A. 1982. Learning and Interocular Transfer of Classically Conditioned Visual Discrimination by Goldfish with Retinotectal Compression, Ph.D. thesis, Univ. of London. 2. DUNN-MEYNELL, A. A., AND G. E. SAVAGE. 1985. Learning and interocular transfer of visual discriminations by goldfish with retinotectal compression. Exp. Neural. 88: 696713.
3. HEMSLEY, J. P., AND G. E. SAVAGE. 1987. Two distinct mechanisms mediating interocular transfer in the goldfish (Carassius auratus). Exp. Neural. 94: 324-332. 4. HEMSLEY, J. P., AND G. E. SAVAGE. 1987. Interocular transfer of shape discrimination in the goldfish-a reassessment of the role of the posterior commissure. Exp. Neurol. 98: 664-672. 5. HEMSLEY, J. P., AND G. E. SAVAGE. 1988. Interocular transfer of preopemtively trained visual discriminations in goldfish following selective commissure transection. Submitted for publication. 6. INGLE, D. J. 1965. The use of fish in neuropsychology. Perspect. Biol. Med. 8: 241-260. 7. iNCiLE, D. J. 1968. Interocular integration of visual learning in the goldfish. Brain Behav. Evol. 1: 58-85. 8. INGLE, D. J., AND A. CAMPBELL. 1977. Interocular transfer of visual discriminations by goldfish with selective commissure lesions. J. Camp. Physiol. Psychol. 91: 327-335. 9. MARK, R. F., 0. PEER, AND J. STEMER. 1973. Integrative functions in the midbrain commissures of fish. Exp. Neural. 39: 140- 156. 10. REPERANT, J., AND M. LEMIRE. 1976. Retinal projections in cyprinid fishes:a degeneration and radioautographic study. Brain Behav. Evol. 13: 34-57.
INTEROCULAR
TRANSFER
IN
GOLDFISH
663
A. D., ANDG. E. LANDRETH. 1977. Direct ipsilateral retinal projections in goldfish (Carassius auratus). Brain Res. 124: 533-537. 12. VONEIDA, T. J., AND C. M. SLIGAR. 1976. A comparative neuroanatomic study of retinal projections in two fishes:Astynax hubbsi and Astynax mexicanus. J. Comp. Neurol. 165:
11. SPRINGER,
89-106.
13. YEO, C. H. 1979. Interocular transfer in the goldfish. Pages 53-60 in I. S. RUSSELL, M. W. VAN HOF, AND G. BERLUCCHI, Ms., Structure and Function of Cerebral Commissures. Macmillan, London. 14. YEO, C. H., AND G. E. SAVAGE. 1976. Mesencephalic and diencephalic commissures and interocular transfer in the goldfish. Exp. Neural. 53: 5 l-63. 15. YEO, C. H., ANDG. E. SAVAGE. 1975. The tectai commissure and interocular transfer of a shape discrimination in the goldfish. Exp. Neural. 49: 29 I-298.
NEUROLOGY
98,659-663 (1987)
RESEARCH
NOTE
Monocular Visual Discrimination in the Goldfish after Unilateral Ablation of the Optic Tectum J.PAULHEMSLEYANDGEORGEE.
SAVAGE
School of Biological Sciences, Queen Mary College, University of London, Mile End Road, London El 4NS, United Kingdom Received September 5, 1986; revision received May 18, 1987 Goldfish with unilateral ablation of the optic tectum and trained to the ablated side failed to learn or to transfer interocularly a differential classically conditioned color discrimination. The direct ipsilateral retinal projection to the intact/naive side is therefore shown to contribute little to engram formation. Evidence is also presented demonstrating that the absence of one tectum does not atfect the learning of a differential bar discrimination task when trained via the intact brain side. o 1987 Academic Press. Inc.
Each hemisphere of the mammalian brain receives retinal fibers from both eyes, hence the interocular transfer of visual discriminations becomes dependent on interhemispheric connections only in the split-chiasm animal. In fish it has been generally assumed that the retinofugal pathways undergo a complete decussation at the chiasm and synapse in the optic tectum contralateral to the eye of origin; therefore information transfer necessarily implicates commissural systems. However, in addition to the contralateral optic input, a number of workers have reported direct ipsilateral projections to the diencephalon and preoptic regions ( lo- 12). In Carassius, Springer and Landreth (11) describe three ipsilateral pathways, a rostral, nondecussating fascicle entering the medial portion of the ipsilateral optic tract and two groups of fibers which recross the midline above the chiasm. The first of these Abbreviation: DQ-discrimination
quotient.
659 0014-4886/87 $3.00 Copyright 8 1987 by Academic Press, Inc. All rights of reproduction in any form reserved.
660
HEMSLEY
AND
SAVAGE
traverses the posterior commissure and distributes to dorsal thalamic as well as pretectal nuclei. A second group of redecussating axons courses through the minor commissure and terminates in preoptic regions. There is no evidence that either of these ipsilateral projections is effective in engram forrnation and fish are able to learn conflicting discriminations of pattern or color with opposite eyes (7). Information arriving via these pathways does not interfere with the discrimination learning based on the direct contralateral input. This assumption is central to previous studies of interocular transfer in fish (3-9,13- 15) and is verified in the experiments reported here. The left optic tectum was removed in five goldfish (Curussius auratus) using techniques detailed elsewhere (1, 2). Five fish also received a sham operation. Comparison of monocular training in these animals provides an opportunity to assess the relative roles of the ipsilateral and contralateral projections in memory formation. Each fish was trained, to the right eye on a red/green color discrimination ( 17” X lo” visual angle) using a differential cardiac conditioning procedure standardized in our laboratory (3). Testing for discrimination via the left eye (intact brain half) indicates the capacity of the ipsilateral projection to contribute to memory formation. Within 1 h after completion of color discrimination testing the intact brain half of shamand tectal-operated animals received training on a differential bar orientation task (lo” X 2” visual angle). The discrimination performance for a block of 10 training trials (5 reinforced, 5 nonreinforced) and the 10 unreinforced transfer trials to the opposite eye for each task is shown by the discrimination quotient (DQ) DQ=
Mean cardiac deceleration to reinforced stimulus Mean cardiac deceleration to nonreinforced stimulus .
Therefore, a DQ < 1 indicates an incorrect/reverse discrimination and a DQ > 1 a correct discrimination (14, 15). Results for all fish are presented in Fig. 1 and Table 1. The data show that the rate of learning on the color task differed considerably between shamand tectal-operated groups. Animals with tectal ablation and trained to the same side failed to acquire the discrimination and more significantly also failed to discriminate the stimuli when presented to the intact side even though the ipsilateral input was functional. A comparison of DQ values for the final 30 training trials and 10 transfer trials (intact side) for the two groups showed a significant difference (Table 1). The deficits in discrimination performance by the intact side were not due to any inteference effects caused by absence of the contralateral tectum as direct training of the intact side (bar task) led to good acquisition. DQ values and trials to criterion for the two groups were not significantly different (Table 1).
INTEROCULAR
TRANSFER
661
IN GOLDFISH
TRIALS
FIG. 1. Learning curves for the tectal-ablated and sham-operated fish. Closed circles represent the results for animals trained on the red/green color discrimination via the ablated tectum, open circles for sham-operated fish trained on the same task. The discrimination performance ofthe untrained side was tested (TR) and after a break of60 mitt tectal-operated fish were trained to the intact tectum (closed triangles) and sham-operated to the previously untrained side (open triangles) with a horizontal vs. vertical bar discrimination task.
The untrained brain side received only a direct ipsilateral projection because the tectum was absent from the contralateral (trained) side. This ipsilateral projection is unlikely to contribute to engram formation since fish
TABLE 1 Mean Results + Standard Error for Fish with Unilateral Ablation of Left Optic Tectum Color discrimination Train to Trials to criterion“
Ablated side (N= 5)
Sham (N= 5)
Not reached 56 + 2.5 (U = 0, P = 0.004)
Bar discrimination Intact tectum (N=5)
Sham (N=5)
60 f 6.3 56 rk 5.0 (U = 10, P = 0.345)
Wb
Last 30 trials
0.36 -t 0.2
3.5k2.1
(II = 0, P = 0.004)
Transfer
0.6 t- 0.29 (u=o,P=o.oo4)
3.2 + 0.9
2.7 * 0.2 3.1 -to.3 (U=8,P=O.21) 0.29 f 0.1 2.9 I!I0.3 (cl= 10, P= 0.345)
LICriterion was attained when three successiveDQ values z 2 were recorded. Figures in parentheses are probability values obtained using the Mann-Whitney rank order test to compare tectal and sham-operated fish. b Discrimination quotient.
662
HEMSLEY
AND SAVAGE
tested via this side but trained to the opposite tectal ablated side showed poor discrimination. Therefore, following monocular acquisition the demonstration of a trained response when testing the naive eye correctly implicates commissural systems in cross-brain transfer. Moreover, there is no evidence that the rate nor asymptote of learning is affected by unilateral tectal ablation when the subject is trained to the intact side. This argues against a bilateral participation in memory formation but not necessarily against bilateral engram deposition. The naive side may simply receive an engram when acquisition is complete rather than participating actively in its formation. This distinction is upheld by previous results showing that (i) there is no difference in the rate of learning between control goldfish and those trained following transection of the commissure subserving transfer of either color (3) or shape (3, 4, 13, 14) information, and (ii) memory is present in both naive and trained sides when monocular conditioning is followed by commissurotomy (5, 13). In contrast, Dunn-Meynell (1) argued that fish with half tectal ablation were slower in learning than control subjects. This was interpreted as evidence for bilateral learning mechanisms but may in fact be due to interference effects caused by reorganisation of tectum on the ablated side. REFERENCES 1. DUNN-MEYNELL, A. A. 1982. Learning and Interocular Transfer of Classically Conditioned Visual Discrimination by Goldfish with Retinotectal Compression, Ph.D. thesis, Univ. of London. 2. DUNN-MEYNELL, A. A., AND G. E. SAVAGE. 1985. Learning and interocular transfer of visual discriminations by goldfish with retinotectal compression. Exp. Neural. 88: 696713.
3. HEMSLEY, J. P., AND G. E. SAVAGE. 1987. Two distinct mechanisms mediating interocular transfer in the goldfish (Carassius auratus). Exp. Neural. 94: 324-332. 4. HEMSLEY, J. P., AND G. E. SAVAGE. 1987. Interocular transfer of shape discrimination in the goldfish-a reassessment of the role of the posterior commissure. Exp. Neurol. 98: 664-672. 5. HEMSLEY, J. P., AND G. E. SAVAGE. 1988. Interocular transfer of preopemtively trained visual discriminations in goldfish following selective commissure transection. Submitted for publication. 6. INGLE, D. J. 1965. The use of fish in neuropsychology. Perspect. Biol. Med. 8: 241-260. 7. iNCiLE, D. J. 1968. Interocular integration of visual learning in the goldfish. Brain Behav. Evol. 1: 58-85. 8. INGLE, D. J., AND A. CAMPBELL. 1977. Interocular transfer of visual discriminations by goldfish with selective commissure lesions. J. Camp. Physiol. Psychol. 91: 327-335. 9. MARK, R. F., 0. PEER, AND J. STEMER. 1973. Integrative functions in the midbrain commissures of fish. Exp. Neural. 39: 140- 156. 10. REPERANT, J., AND M. LEMIRE. 1976. Retinal projections in cyprinid fishes:a degeneration and radioautographic study. Brain Behav. Evol. 13: 34-57.
INTEROCULAR
TRANSFER
IN
GOLDFISH
663
A. D., ANDG. E. LANDRETH. 1977. Direct ipsilateral retinal projections in goldfish (Carassius auratus). Brain Res. 124: 533-537. 12. VONEIDA, T. J., AND C. M. SLIGAR. 1976. A comparative neuroanatomic study of retinal projections in two fishes:Astynax hubbsi and Astynax mexicanus. J. Comp. Neurol. 165:
11. SPRINGER,
89-106.
13. YEO, C. H. 1979. Interocular transfer in the goldfish. Pages 53-60 in I. S. RUSSELL, M. W. VAN HOF, AND G. BERLUCCHI, Ms., Structure and Function of Cerebral Commissures. Macmillan, London. 14. YEO, C. H., AND G. E. SAVAGE. 1976. Mesencephalic and diencephalic commissures and interocular transfer in the goldfish. Exp. Neural. 53: 5 l-63. 15. YEO, C. H., ANDG. E. SAVAGE. 1975. The tectai commissure and interocular transfer of a shape discrimination in the goldfish. Exp. Neural. 49: 29 I-298.