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Lateralization reversal after intertectal commissurotomy in the pigeon
Brain Research, 408 (1987) 1-5 Elsevier
1
BRE 12466
Research Reports
Lateralization reversal after intertectal commissurotomy in the pigeon Onur Gtintiirktin and Paul G. BOhringer Experimentelle Tierpsychologie, Psychologisches lnstitut, Ruhr-Universitdt Bochum, Bochum, (F. R. G.)
(Accepted 19 August 1986) Key words: Late ralization; Visual system; Tectal commissure; Commissurotomy; Pigeon
After transection of the intertectal commissures, the lateralization of a visually controlled behaviour of pigeons was reversed to a degree proportional to the extent of the commissurotomy. Preoperatively, the pigeons produced higher pecking rates in a successive pattern discrimination task when seeing with the right eye. Postoperatively, this lateralization reversed to show a superiority with the left eye. Visual lateralization may depend on an asymmetrical intertectal interaction. INTRODUCTION Cerebral lateralization as a functional or anatomical left-right-asymmetry of the brain was once thought to be an exclusively human attribute 3.. This opinion changed after Nottebohm demonstrated that there is a dominance of the left hemispheric structures for vocalization in canaries that resembled the lateralization of speech areas in the human brain 23. Since these first studies, many experiments have demonstrated that the left brain hemisphere in birds is not only dominant for vocalization but also for a variety of visual tasks 2'3"9'12"13'15"3°.Through the virtually complete decussation of the optic nerves of birds, the avian visual system is particularly suited for research on lateralization 26'31. Temporary occlusion of one eye entails that most information entering through the unobstructed eye is processed by the contralateral hemisphere. Pigeons performing a pattern discrimination task under these conditions generally show higher response rates and a superior discrimination capacity when seeing with the right eye, which projects to the dominant left hemisphere 12'13. Until now the organizational principles underlying functional asymmetries in birds and mammals are
generally obscure. In different models (for an excellent review see ref. 1) it is assumed that the lateralization of, for example, language or handedness in humans depends on functionally specialized subunits in the brain which are genetically determined to be localized mainly in one hemisphere 1°'22. Other authors discuss the possibility that lateralization may depend on an asymmetrical activatory or inhibitory interaction between the hemispheres 8'2°. This assumption suggests that the asymmetry may be altered by unilateral lesions or by commissure transections thereby leading to changes in iateralization. We now report that the performance superiority observed under right-eye seeing conditions in pigeons can be reversed after transecting the midbrain cornmissures that connect the optic tecta of the two hemispheres. This result provides a dramatic demonstration that visual lateralization of pigeons may depend, at least at midbrain level, on an asymmetrical interaction between the tecta, MATERIALS AND METHODS Sixteen adult homing pigeons were maintained at 80% of their normal weight throughout the experi-
Correspondence: 0. GiJnttirkiin, Experimentelle Tierpsychologie, Psychologisches Institut, Ruhr-Universit~it Bochum, D-4630 Bochum, F.R.G.
0006-8993/87/$03.50 © 1987 Elsevier Science Publishers B.V. (Biomedical Division)
ment. A Skinner-box with a single response key o n which stimuli were back-projected with a multi-chartnel microprojector was used. A digital microprocessor controlled events within the experimental sessions and recorded the key pecking responses. Pecking on the white light illuminated key was conditioned using an autoshaping procedure 5. When the animals had learned to associate key pecking with food reward, a small metal block with a tapped hole was cemented to each animal's skull while under ~fnaesthesia s. Discrimination training began after 4 days of postoperative recovery. On alternate sessions the subjects' sight was restricted to either the left or the right eye with the aid of an opaque cap attached to the metal block (Fig. 1E). The sequence of right/left monocular seeing conditions was balanced
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Fig. 1. Mean pecking responses of (A) commissurotomized and (B) control pigeons before and after the operation (op). C: preand postoperative mean percent correct responses with stundard errors of control and experimental pigeons during either the left or the right eye seeing conditions. D: stimuli used in the experiment. E: pigeon with eye cap.
across animals. Two stimuli, shown in Fig. 1D, were successively projected onto the response key in a quasi-random sequence. For half of the pigeons one, for the other half the other stimulus was deemed to be correct. Pecks to the correct stimulus yielded 4 s food access according to a variable ratio schedule. Each peck on the incorrect stimulus extended the projection time for 2 s, thus ensuring eventual respouse extinction. Without extension a trial lasted 20 s;each session consistedof40trials. To assess the percent correct and incorrect respouses, only the pecks during the initial 20 s of stimulus presentation were considered. At the beginning of acquisition, the pigeons were reinforced on a VR 2 schedule. After reaching 85% of correct responses in one session, this ratio was increased on reaching or maintaining 85% correct responses to VR (variable ratio) 4, to V R 8, then to VR 16 and finally to VR 32. After reaching a criterion of 85% correct responses in 3 consecutive sessions with a VR 32 reinforcement schedule in operation, 20 further sessions were run in which the animals were seeing with either the left or the right eye on alternate sessions. Then each pigeon was anaesthetized, its head was held in a stereotaxic apparatus and the skull was trephined with a dental burr. In 8 of the animals a surgical microknife was inserted under stereotaxic guidance between the forebrain hemispheres and the two intertectal commissures, commissura tectalis and commissura posterior, were transected. The knife was constructed according to specifications of Cudnod and Zeier 6 and consisted of a 0.8-mm diameter syringe needle with an axle across the tip on which was hinged a 3-mm long stainless steel blade. The blade could be closed or extended by retracting or pushing a stiff stainless steel wire running through the needle. After trephining the skull, the sinus sagittalis along the midline of the brain was pulled gently sidewards. The knife was in-
troduced with the blade extended at the coordinate A7 L0 according to the pigeon brain atlas is and at an angle of 71 ° with reference to the brain's surface for a distance of 8.5 ram. Then the blade was swung over an angle of 35 ° by retracting the steel wire in the needle for 8 mm and extending it again. Then the knife was withdrawn (Fig. 2C). The remaining 8 pigeons were sham-operated by incising the scalp and trephining the skull at the same coordinates as in the experimental pigeons. After 5 days' recovery, 20 fur-
A
B 30-
index for the reversal of lateralization of this animal. The latter was the preoperative right-left response difference, minus the postoperative right-left re-
' " •
c_
sponse difference, divided by the sum of the pre- and postoperative responses. The result was multiplied by 100 to give an integer index.
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_5 0
RESULTS
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, , ~o 60 eommissurotomy
, 80
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Fig. 2. A: correlation between the extent of commissurotomy and the lateralization reversal. B: photomicrograph of a frontal section of the pigeon brain which corresponds to the A 3.75 plane of the pigeon brain atlas. Arrow indicates the commissurotomy. C: diagram of the sagittal plane L 0.50 of the pigeon brain atlas in which the path of the knife is shown. Anterior is to the right. Cb, cerebellum, CA, commissura anterior; CO, chiasma opticum; CP, commissura posterior; CT, commissura tectalis; DSD + DSV, decussatio supraoptica dorsalis et ventralis; HA, hyperstriatum accessorium; RP, n. reticularis porttis caudalis,
ther sessions were run under the same conditions as before. Then the animals were anaesthetized and perfused intracardially with saline followed by 4% formalin. The brains were embedded in paraffin, cut into frontal 26-/zm sections and stained with Luxol fast blue and Cresyl violet for demonstration of fibres and cell bodies. The histological sections of the experimental animais were compared at 250-/~m intervals with corresponding sections of control pigeon brains processed with the same histological procedure. One of the authors (O.G.), who made the histological analysis, was not informed about the behavioral results of the pigeons under microscopical examination. A cornplete lack of commissural fibres was considered as a 100% commissurotomy (Fig. 2B). If the commissure was only partly sectioned, the diameter of the remaining fibre bundle was measured microscopically with an ocular micrometer-grid. The percent extent of the commissurotomy for that section was then calculated by comparing this diameter with that of the commissures in corresponding sections of control pigeons. From these comparisons an average extent of commissurotomy was determined for every pigeon, This commissurotomy score was correlated with an
The performance of the animals in the discrimination task was assessed by the total number of pecking responses, a measure of activity, and by the percent correct discrimination scores, an index of the discrimination accuracy. The response rate was the sum of the correct and incorrect responses emitted during each session. The percent correct discrimination score was calculated as the ratio of the number of correct to the total number of responses per session. Preoperatively, both control and experimental pigeons pecked significantly more per session when seeing with the right eye than with the left (each F 1/133 t> 20.94, P < 0.001, degrees of freedom of the A N O V A calculated for two conditions, 10 sessions and 8 animals, Fig. 1A, B). Postoperatively, this right eye superiority remained unchanged in the control pigeons (F 1/133 = 32.09, P < 0.001), while there was a complete reversal of the right-left difference in the commissurotomized animals. These now emitted more pecks when seeing with the left eye (F 1/133 = 19.59, P < 0.001, Fig. 1A). The extent of the reversal of eye-dominance correlated significantly with the extent of the commissurotomy as established histoiogically (r = 0.88, P < 0.01, Fig. 2A). A comparison of the pre- and the post-operative pecking frequencies of the experimental pigeons shows that the reversal of lateralization resulted from a marked decrease with the right eye seeing (F 1/133 = 54.96, P < 0.001) and a mild increase with the left (F 1/133 = 6.29, P < 0.05). This increase is probably due to the influence of continued training, since the control pigeons also pecked postoperatively more in both monocular conditions (each F 1/133 t> 8.28, P < 0.01) and there was no significant difference between control and experimental birds in the postoperative response rates with the left eye (F 1/14 = 2.73, P > 0.05). No significant differences were found in the percent correct discrimination scores either pre- or postoperatively between the two monocular conditions
(each F 1/133 ~< 1.72, P > 0.05, Fig. 1C). There were also no significant differences between the two groups in any eye cap condition (each F 1/14 ~< 2.37, P > 0.05). DISCUSSION As in previous studies, all pigeons showed higher preoperative pecking rates when seeing with the right eye ~2'~3. Due to the virtually complete decussation of the optic nerves in birds, this asymmetry can be attributed to a superiority of the left hemisphere, This agrees with previous studies in birds which also demonstrate a dominance for the left hemisphere for visually guided behaviour 2'9'12'15. However, the percent correct scores with the right eye seeing were not superior to those with the left eye seeing. The absence or presence of a right-left discrimination advantage seems to depend on the kind of discriminative stimuli used. In another experiment j2 there was a consistent superiority in the response rates emitted under right eye seeing conditions but either a pronounced or only a marginal advantage with the right eye in the percent correct scores, depending on the pair of stimuli used. After commissurotomy the lateralization in the amount of response rates reversed mainly through decrease in the pecking responses when seeing with the right eye. This result makes it unlikely that visual lateralization of response rates in birds is due to specialized visual structures with gross morphological left/right asymmetries as demonstrated, for example, in the human speech areas 33. A commissurotomy would not in fact alter such pronounced asymmetries and could therefore not lead to changes in lateralization. It is more likely that the visual lateralization of normal pigeons depends, at least in part, on an asymmetric interaction between the tecta. Commissurotomy would lead to modifications of this asymmetry and thus to changes in the visual lateralization. Until now there was no evidence for an asymmetry in the tectal commissures, but this may be a result of the fact that as far as we know the tecto-tectal interactions have not yet been analyzed with such an asymmetry in mind. Prolonged monocular deprivation in optic chiasm-sectioned kittens results in functional and anatomical asymmetries of the corpus caliosum,
such that the influence of the non-deprived hemisphere on the deprived one is much greater than m the opposite direction 7. Thus, asymmetric visual experience during the period of brain maturation can alter the symmetry of interhemispheric connections. Rogers 29 demonstrated that lateralization of visually guided behavior in chicks correlates with the differential exposure to light of the two eyes during a critical embryonic period in which the embryo is asymmetrically oriented in the egg. Thus, it seems reasonable to suppose that an asymmetry of the intertectal commissures could have been developed through asymmetric pre-hatching visual stimulations. At present, it cannot be excluded that other commissures, like the commissura anterior or the dorsal supraoptic decussation, also participate in the maintenance of visual lateralization in birds. The axons of the two intertectal pathways, the commissura tectalis and the commissura posterior, synapse mainly inhibitorily on the neurones of the tectal layers I I I - V 14"Z6"2~'32. Previous studies demonstrate that the neurones of these laminae receive afferences from the Wulst and the archistriatum 4'w'~5, two telencephalic structures which receive visual afferences and participate, at least in part, in the control of visually guided behaviour ~1"j3"17"24"27.The neurones of the tectal laminae I I - V send ascending efferences to the visual thalamic nuclei, n. rotundus and n. dorsolateralis anterior thalami pars lateralis ~'. Descending efferences lead to reticular and motor nuclei of the mid- and hindbrain ~5. An asymmetrical tecto-tectal interaction could provide for a lateralized activation of sensory, attentional and motor structures in a context of visually guided behaviour. This could account for the differences in the pecking rates under right or left eye control. Modifying this asymmetrical interaction by commissurotomy leads to concomitant changes in lateralized control.
ACKNOWLEDGEMENTS Supported by the Deutsche Forschungsgemeinschaft through its Sonderforschungsbereich 114. We thank J.D. Delius and J. Emmerton for critically reading the manuscript and U. Schall and H, Rohmann for essential assistance.
REFERENCES 1 Allan, M.. Models of hemispheric specialization, Psychol. Bull., 93 (1983) 73-104. 2 Andrew, R.J.. Lateralization of emotional and cognitive function in higher vertebrates with special reference to the domestic chick. In J.P. Ewert, R. Capranica and D.J. Ingle (Eds.), Advances in Vertebrate Neuroethology, Plenum Press, New York, 1983, pp. 477-510. 3 Andrew, R.J., Mench, J. and Rainey, C., Right-left asymmerry of response to visual stimuli in the domestic chick. In D.J. Ingle, M.A. Goodale and I. Mansfield (Eds.), Advances in the Analysis of Visual Behavior. MIT Press, 1982, 197- 209. 4 Bagnoli, P., Grassi, S. and Magni, F., A direct connection between visual Wulst and tectum opticum in the pigeon (Columba livia) demonstrated by horseradish peroxidase, Arch. ltal. Biol., 118 (1980) 72-88. 5 Brown, P.L. and Jenkins, H.M., Auto-shaping of the pigeon's key-peck. J. Exp. Anal. Behav., 11 (1968) 1-8. 6 Cu6nod, M. and Zeier, H., Transfert visuelinterh6misph6rique et commissurotomie chez le pigeon, Schweizer Arch. Neurol. Psychiatry, 100 (1967)365-380. 7 Cynader, M., Lepore, F. and Guillemont. J., lnter-hemispheric competition during postnatal development, Nature (London), 290 (1981) 139-140. 8 Denenberg, V.H., Hemispheric laterality in animals and the effects of early experience, Behav. Brain Sci., 4 (1981) 1-49.
9 Gaston. K.E.. Interocular transfer of pattern discrimination learning in chicks, Brain Research, 310 (1984) 213-221. 10 Gazzaniga. M.S. and Le Doux, J.E., The Integrated Mind, Plenum Press, New York. 1978. 11 GiJntiirkiJn. O.. Evidence for a third primary visual area in the telencephalon of the pigeon, Brain Research, 294 (1984) 247-254. 12 Gi.inttirkfin, O., Lateralization of visually controlled behavior in pigeons. Physiol. Behav.. 34 (1985) 575-577. 13 Gi~ntiirki.in. O. and Hoferichter, H.H., Neglect after section of a left telencephalotectal tract in pigeons, Behav. Brain Res., 18 (t985) 1-9. 14 Hardy, O., Leresche. N. and Jassik-Gerschenfeld, D., Postsynaptic potentials in neurons of the pigeon's optic tectum in response to afferent stimulation from the retina and other visual structures: an intracellular study, Brain Research, 311 (1984) 65-74. 15 Howard, K.J., Rogers, L.J. and Bourda, A.L.A., Functional lateralization of the chicken forebrain revealed by use of intracranial glutamate, Brain Research, 188 (1980) 369-382. 16 Hunt, S.P. and K/inzle, H., Observations on the projections and intrinsic organisation of the pigeon optic tectum: an autoradiographic study based on anterograde and retrograde, axonal and dendritic flow, J. Comp. Neurol., 170 (1976) 153-172. 17 Hunt, S.P. and Webster, K.E., Thalamo-hyperstriateinterrelations in the pigeon, Brain Research, 44 (1972) 647-651. 18 Karten, H.J. and Hodos, W., A Stereotaxic Atlas of the
19
20
21
22
23
24
25
Brain of the Pigeon, Johns Hopkins Press, Baltimore, MD, 1967. Karten, H.J., Hodos, W., Nauta, W.H.J. and Revzin, A.L., Neural connections of the 'visual Wulst' of the avian telencephalon. Experimental studies in the pigeon (Columba livia) and owl (Speotyto cunilaria), J. Comp. Neurol., 150 (1973) 253-277. Luria, A.R. and Simernitskaya, E.G., Interhemispheric relations and the function of the minor hemisphere, Neuropsychologia, 15 (1977) 175-178. Mailin, H.D. and Delius, J.D., Inter- and intraocular transfer of colour discriminations with mandibulation as an operant in the head-fixed pigeon, Behav. Anal. Lett., 3 (1983) 297-309. Marin, O.S.M., Schwartz, M.F. and Saffran, E.M., Origins and distribution of language. In M.S. Gazzaniga (Ed.), Handbook of Behavioral Neurobiology, Vol. 2, Plenum Press, New York, 1979. Nottebohm, F., Origins and mechanisms in the establishment of cerebral dominance. In M.S. Gazzaniga (Ed.), Handbook of Behavioral Neurobiology, Vol. 2, Plenum Press, New York, 1979, pp. 295-344. Pasternak, T. and Hodos, W., Intensity difference thresholders after lesions of the visual Wulst in pigeons, J. Comp. Physiol. Psychol., 91 (1977)485-497. Reiner, A. and Karten, H.J., Laminar distribution of the ceils of origin of the descending tectofugal pathways in the pigeon (Columba livia), J. Comp. Neurol., 204 (1982) 165-187.
26 Rep6rant, J., Nouvelles donn6es sur les projections visueUes chez le pigeon (Columba livia), J. Hirnforsch., 14 (1973) 151-187. 27 Ritchie, T.L.L. and Cohen, D.H., The avian tectofugal visual pathway: projections of its telencephalic target, the ectostriatal complex., Neurosci. Abstr., 3:94 (1977) 275. 28 Robert, F. and Cu6nod, M., Electrophysiology of the intertectal commissures in the pigeon. If. Inhibitory interaction, Exp. Brain Res., 9 (1969) 123-136. 29 Rogers, L.J., Light experience and asymmetry of brain function in chickens, Nature (London), 297 (1982) 223-225. 30 Rogers, L.J. and Anson, J.M., Lateralization of function in the chicken forebrain, Pharmacol. Biochem. Behav., 10 (1979) 679-686. 31 Takatsuji, K., Ito, H. and Masai, H., Ipsilateral retinal projections in Japanese quail, Coturnix coturnix japonica, Brain Res. Bull., 10 (1983) 53-56. 32 Voneida, T.J. and Mello, N.K., Interhemispheric projections of the optic rectum in the pigeon, Brain Behav. Evol.. 11 (1975)91-108. 33 Wada, J.A., Clarke, R. and Hamm, A., Cerebral hemispheric asymmetry in humans, Arch. Neurol., 32 (1975) 239-246. 34 Walker, S.F., Lateralization of functions in the vertebrate brain: a review, Br. J. Psychol., 71 (1980) 329-367. 35 Zeier, H. and Karten, H.J., The archistriatum of the pigeon: organization of afferent and efferent connections, Brain Research, 31 (1971) 313-326.
1
BRE 12466
Research Reports
Lateralization reversal after intertectal commissurotomy in the pigeon Onur Gtintiirktin and Paul G. BOhringer Experimentelle Tierpsychologie, Psychologisches lnstitut, Ruhr-Universitdt Bochum, Bochum, (F. R. G.)
(Accepted 19 August 1986) Key words: Late ralization; Visual system; Tectal commissure; Commissurotomy; Pigeon
After transection of the intertectal commissures, the lateralization of a visually controlled behaviour of pigeons was reversed to a degree proportional to the extent of the commissurotomy. Preoperatively, the pigeons produced higher pecking rates in a successive pattern discrimination task when seeing with the right eye. Postoperatively, this lateralization reversed to show a superiority with the left eye. Visual lateralization may depend on an asymmetrical intertectal interaction. INTRODUCTION Cerebral lateralization as a functional or anatomical left-right-asymmetry of the brain was once thought to be an exclusively human attribute 3.. This opinion changed after Nottebohm demonstrated that there is a dominance of the left hemispheric structures for vocalization in canaries that resembled the lateralization of speech areas in the human brain 23. Since these first studies, many experiments have demonstrated that the left brain hemisphere in birds is not only dominant for vocalization but also for a variety of visual tasks 2'3"9'12"13'15"3°.Through the virtually complete decussation of the optic nerves of birds, the avian visual system is particularly suited for research on lateralization 26'31. Temporary occlusion of one eye entails that most information entering through the unobstructed eye is processed by the contralateral hemisphere. Pigeons performing a pattern discrimination task under these conditions generally show higher response rates and a superior discrimination capacity when seeing with the right eye, which projects to the dominant left hemisphere 12'13. Until now the organizational principles underlying functional asymmetries in birds and mammals are
generally obscure. In different models (for an excellent review see ref. 1) it is assumed that the lateralization of, for example, language or handedness in humans depends on functionally specialized subunits in the brain which are genetically determined to be localized mainly in one hemisphere 1°'22. Other authors discuss the possibility that lateralization may depend on an asymmetrical activatory or inhibitory interaction between the hemispheres 8'2°. This assumption suggests that the asymmetry may be altered by unilateral lesions or by commissure transections thereby leading to changes in iateralization. We now report that the performance superiority observed under right-eye seeing conditions in pigeons can be reversed after transecting the midbrain cornmissures that connect the optic tecta of the two hemispheres. This result provides a dramatic demonstration that visual lateralization of pigeons may depend, at least at midbrain level, on an asymmetrical interaction between the tecta, MATERIALS AND METHODS Sixteen adult homing pigeons were maintained at 80% of their normal weight throughout the experi-
Correspondence: 0. GiJnttirkiin, Experimentelle Tierpsychologie, Psychologisches Institut, Ruhr-Universit~it Bochum, D-4630 Bochum, F.R.G.
0006-8993/87/$03.50 © 1987 Elsevier Science Publishers B.V. (Biomedical Division)
ment. A Skinner-box with a single response key o n which stimuli were back-projected with a multi-chartnel microprojector was used. A digital microprocessor controlled events within the experimental sessions and recorded the key pecking responses. Pecking on the white light illuminated key was conditioned using an autoshaping procedure 5. When the animals had learned to associate key pecking with food reward, a small metal block with a tapped hole was cemented to each animal's skull while under ~fnaesthesia s. Discrimination training began after 4 days of postoperative recovery. On alternate sessions the subjects' sight was restricted to either the left or the right eye with the aid of an opaque cap attached to the metal block (Fig. 1E). The sequence of right/left monocular seeing conditions was balanced
A
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~ 800
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i
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.
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Fig. 1. Mean pecking responses of (A) commissurotomized and (B) control pigeons before and after the operation (op). C: preand postoperative mean percent correct responses with stundard errors of control and experimental pigeons during either the left or the right eye seeing conditions. D: stimuli used in the experiment. E: pigeon with eye cap.
across animals. Two stimuli, shown in Fig. 1D, were successively projected onto the response key in a quasi-random sequence. For half of the pigeons one, for the other half the other stimulus was deemed to be correct. Pecks to the correct stimulus yielded 4 s food access according to a variable ratio schedule. Each peck on the incorrect stimulus extended the projection time for 2 s, thus ensuring eventual respouse extinction. Without extension a trial lasted 20 s;each session consistedof40trials. To assess the percent correct and incorrect respouses, only the pecks during the initial 20 s of stimulus presentation were considered. At the beginning of acquisition, the pigeons were reinforced on a VR 2 schedule. After reaching 85% of correct responses in one session, this ratio was increased on reaching or maintaining 85% correct responses to VR (variable ratio) 4, to V R 8, then to VR 16 and finally to VR 32. After reaching a criterion of 85% correct responses in 3 consecutive sessions with a VR 32 reinforcement schedule in operation, 20 further sessions were run in which the animals were seeing with either the left or the right eye on alternate sessions. Then each pigeon was anaesthetized, its head was held in a stereotaxic apparatus and the skull was trephined with a dental burr. In 8 of the animals a surgical microknife was inserted under stereotaxic guidance between the forebrain hemispheres and the two intertectal commissures, commissura tectalis and commissura posterior, were transected. The knife was constructed according to specifications of Cudnod and Zeier 6 and consisted of a 0.8-mm diameter syringe needle with an axle across the tip on which was hinged a 3-mm long stainless steel blade. The blade could be closed or extended by retracting or pushing a stiff stainless steel wire running through the needle. After trephining the skull, the sinus sagittalis along the midline of the brain was pulled gently sidewards. The knife was in-
troduced with the blade extended at the coordinate A7 L0 according to the pigeon brain atlas is and at an angle of 71 ° with reference to the brain's surface for a distance of 8.5 ram. Then the blade was swung over an angle of 35 ° by retracting the steel wire in the needle for 8 mm and extending it again. Then the knife was withdrawn (Fig. 2C). The remaining 8 pigeons were sham-operated by incising the scalp and trephining the skull at the same coordinates as in the experimental pigeons. After 5 days' recovery, 20 fur-
A
B 30-
index for the reversal of lateralization of this animal. The latter was the preoperative right-left response difference, minus the postoperative right-left re-
' " •
c_
sponse difference, divided by the sum of the pre- and postoperative responses. The result was multiplied by 100 to give an integer index.
2o>
[
o
= 10N °
_5 0
RESULTS
r:0.88
•
, 20
%
, , ~o 60 eommissurotomy
, 80
, loo
Fig. 2. A: correlation between the extent of commissurotomy and the lateralization reversal. B: photomicrograph of a frontal section of the pigeon brain which corresponds to the A 3.75 plane of the pigeon brain atlas. Arrow indicates the commissurotomy. C: diagram of the sagittal plane L 0.50 of the pigeon brain atlas in which the path of the knife is shown. Anterior is to the right. Cb, cerebellum, CA, commissura anterior; CO, chiasma opticum; CP, commissura posterior; CT, commissura tectalis; DSD + DSV, decussatio supraoptica dorsalis et ventralis; HA, hyperstriatum accessorium; RP, n. reticularis porttis caudalis,
ther sessions were run under the same conditions as before. Then the animals were anaesthetized and perfused intracardially with saline followed by 4% formalin. The brains were embedded in paraffin, cut into frontal 26-/zm sections and stained with Luxol fast blue and Cresyl violet for demonstration of fibres and cell bodies. The histological sections of the experimental animais were compared at 250-/~m intervals with corresponding sections of control pigeon brains processed with the same histological procedure. One of the authors (O.G.), who made the histological analysis, was not informed about the behavioral results of the pigeons under microscopical examination. A cornplete lack of commissural fibres was considered as a 100% commissurotomy (Fig. 2B). If the commissure was only partly sectioned, the diameter of the remaining fibre bundle was measured microscopically with an ocular micrometer-grid. The percent extent of the commissurotomy for that section was then calculated by comparing this diameter with that of the commissures in corresponding sections of control pigeons. From these comparisons an average extent of commissurotomy was determined for every pigeon, This commissurotomy score was correlated with an
The performance of the animals in the discrimination task was assessed by the total number of pecking responses, a measure of activity, and by the percent correct discrimination scores, an index of the discrimination accuracy. The response rate was the sum of the correct and incorrect responses emitted during each session. The percent correct discrimination score was calculated as the ratio of the number of correct to the total number of responses per session. Preoperatively, both control and experimental pigeons pecked significantly more per session when seeing with the right eye than with the left (each F 1/133 t> 20.94, P < 0.001, degrees of freedom of the A N O V A calculated for two conditions, 10 sessions and 8 animals, Fig. 1A, B). Postoperatively, this right eye superiority remained unchanged in the control pigeons (F 1/133 = 32.09, P < 0.001), while there was a complete reversal of the right-left difference in the commissurotomized animals. These now emitted more pecks when seeing with the left eye (F 1/133 = 19.59, P < 0.001, Fig. 1A). The extent of the reversal of eye-dominance correlated significantly with the extent of the commissurotomy as established histoiogically (r = 0.88, P < 0.01, Fig. 2A). A comparison of the pre- and the post-operative pecking frequencies of the experimental pigeons shows that the reversal of lateralization resulted from a marked decrease with the right eye seeing (F 1/133 = 54.96, P < 0.001) and a mild increase with the left (F 1/133 = 6.29, P < 0.05). This increase is probably due to the influence of continued training, since the control pigeons also pecked postoperatively more in both monocular conditions (each F 1/133 t> 8.28, P < 0.01) and there was no significant difference between control and experimental birds in the postoperative response rates with the left eye (F 1/14 = 2.73, P > 0.05). No significant differences were found in the percent correct discrimination scores either pre- or postoperatively between the two monocular conditions
(each F 1/133 ~< 1.72, P > 0.05, Fig. 1C). There were also no significant differences between the two groups in any eye cap condition (each F 1/14 ~< 2.37, P > 0.05). DISCUSSION As in previous studies, all pigeons showed higher preoperative pecking rates when seeing with the right eye ~2'~3. Due to the virtually complete decussation of the optic nerves in birds, this asymmetry can be attributed to a superiority of the left hemisphere, This agrees with previous studies in birds which also demonstrate a dominance for the left hemisphere for visually guided behaviour 2'9'12'15. However, the percent correct scores with the right eye seeing were not superior to those with the left eye seeing. The absence or presence of a right-left discrimination advantage seems to depend on the kind of discriminative stimuli used. In another experiment j2 there was a consistent superiority in the response rates emitted under right eye seeing conditions but either a pronounced or only a marginal advantage with the right eye in the percent correct scores, depending on the pair of stimuli used. After commissurotomy the lateralization in the amount of response rates reversed mainly through decrease in the pecking responses when seeing with the right eye. This result makes it unlikely that visual lateralization of response rates in birds is due to specialized visual structures with gross morphological left/right asymmetries as demonstrated, for example, in the human speech areas 33. A commissurotomy would not in fact alter such pronounced asymmetries and could therefore not lead to changes in lateralization. It is more likely that the visual lateralization of normal pigeons depends, at least in part, on an asymmetric interaction between the tecta. Commissurotomy would lead to modifications of this asymmetry and thus to changes in the visual lateralization. Until now there was no evidence for an asymmetry in the tectal commissures, but this may be a result of the fact that as far as we know the tecto-tectal interactions have not yet been analyzed with such an asymmetry in mind. Prolonged monocular deprivation in optic chiasm-sectioned kittens results in functional and anatomical asymmetries of the corpus caliosum,
such that the influence of the non-deprived hemisphere on the deprived one is much greater than m the opposite direction 7. Thus, asymmetric visual experience during the period of brain maturation can alter the symmetry of interhemispheric connections. Rogers 29 demonstrated that lateralization of visually guided behavior in chicks correlates with the differential exposure to light of the two eyes during a critical embryonic period in which the embryo is asymmetrically oriented in the egg. Thus, it seems reasonable to suppose that an asymmetry of the intertectal commissures could have been developed through asymmetric pre-hatching visual stimulations. At present, it cannot be excluded that other commissures, like the commissura anterior or the dorsal supraoptic decussation, also participate in the maintenance of visual lateralization in birds. The axons of the two intertectal pathways, the commissura tectalis and the commissura posterior, synapse mainly inhibitorily on the neurones of the tectal layers I I I - V 14"Z6"2~'32. Previous studies demonstrate that the neurones of these laminae receive afferences from the Wulst and the archistriatum 4'w'~5, two telencephalic structures which receive visual afferences and participate, at least in part, in the control of visually guided behaviour ~1"j3"17"24"27.The neurones of the tectal laminae I I - V send ascending efferences to the visual thalamic nuclei, n. rotundus and n. dorsolateralis anterior thalami pars lateralis ~'. Descending efferences lead to reticular and motor nuclei of the mid- and hindbrain ~5. An asymmetrical tecto-tectal interaction could provide for a lateralized activation of sensory, attentional and motor structures in a context of visually guided behaviour. This could account for the differences in the pecking rates under right or left eye control. Modifying this asymmetrical interaction by commissurotomy leads to concomitant changes in lateralized control.
ACKNOWLEDGEMENTS Supported by the Deutsche Forschungsgemeinschaft through its Sonderforschungsbereich 114. We thank J.D. Delius and J. Emmerton for critically reading the manuscript and U. Schall and H, Rohmann for essential assistance.
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