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Neglect after section of a left telencephalotectal tract in pigeons
1
Behavioural Brain Research, 18 (1985) 1-9 Elsevier BBR00504
Research Papers NEGLECT AFTER SECTION OF A LEFT TELENCEPHALOTECTAL TRACT IN PIGEONS
O N U R G ~ N T ( ) R K O N and H A N S - H O R S T H O F E R I C H T E R
Ruhr-Universitiit Bochum, Experimentelle Tierpsychologie, Psychologisches Institut, Bochum (F.R.G.) (Received February 1st, 1985) (Revised version received August 27th, 1985) (Accepted August 28th, 1985)
Key words: visual discrimination - lesion - lateralization - optic tectum - neglect - pigeon
The effects of unilateral and bilateral lesions of the telencephalotectal fibres of the tractus occipitomesencephalicus (OM) were studied in pigeons in a successive visual pattern discrimination. On alternate sessions the animals performed the task with both eyes open or sight restricted to one or the other eye. Unilateral lesions of the left OM led to severe deficits in the total number of pecking responses emitted under both monocular and binocular conditions. Pigeons with lesions of the right OM showed no deficits and the animals with bilateral lesions had an impaired performance only in the binocular condition. The percent correct discrimination performance of all experimental pigeons were at the same level as that of the control group. The results are discussed in the context of visual lateralization in birds. It is suggested that the deficits reflect a sensory neglect through deactivation of neurons in the deep tectal laminae which are known to have projections to reticular nuclei of the brainstem.
INTRODUCTION
Previous studies on the behavioural effects of lesions of the avian visual system have primarily concentrated on the two pathways which convey optic information to the telencephalon of birds 1~. One of these pathways, the tectofugal route, begins with optic nerve axons which decussate completely in the chiasma opticum and terminate in the optic tectum. This structure in turn projects on the nucleus rotundus in the thalamus, which itself sends fibres to the ipsilateral ectostriatum, a core area of the telencephalon 5. The other visual pathway, the thalamofugal route, consists of retinal fibres which also decussate completely in the chiasma opticum and proceed to a nuclear complex in the contralateral thalamus. These nuclei in turn project mainly to the ipsilateral wulst, a structure in the frontodorsal telencephalon 28. Lesions of the ectostriatum yield severe deficits in
visual pattern and brightness discrimination tasks (ref. 20, but see ref. 8). Bilateral lesions of the wulst lead only to minor impairments in simple visual colour, brightness and pattern discriminations 31"33. Paradoxical results were reported by Nau and Delius 29 who found marked deficits in simple pattern discriminations when pigeons with unilateral wulst ablations used the eye contralateral to the lesioned hemisphere, while bilaterally lesioned animals showed no deficits. When using the ipsilateral eye the discrimination performance of the unilaterally lesioned animals was at the level of the control birds. Nau and Delius 29 ascribed these results to the modulatory effect which is exerted by the wulst via its efferent pathway, the tractus septomesencephalicus (TSM), on intertectal inhibition which is conveyed by the commissura tectalis and the commissura posterior. Assuming that the partly excitatory effect of the TSM at the tectal level compensates the inhibitory
Correspondence: 0. Glintiirkiin, Ruhr-Universit~it Bochum, Experimentelle Tierpsychologie, Psychologisches Institut, D 4630 Bochum, F.R.G.
2 effect of the contralateral tectum, unilateral lesions of the wulst could create an inhibitory intertectal imbalance which can be corrected by an additional ablation of the intact Wulst, or else of the intact TSM. According to this suggestion it is not the lesion of the Wulst, or else of the T S M as such but the asymmetrical inhibitory interaction between the tecta that would account for the observed deficits. There are indeed electrophysiological 2'38, as well as behavioural results 32 which support this hypothesis. The only other telencephalotectal pathway of birds is the tractus occipitomesencephalicus (OM) which originates in the archistriatum and projects to lamina III of the ipsilateral tectum where fibres of the T S M also synapse 3,9,48,49. Ritchie 37 suggested that the O M arises from a subdivision of the archistriatum that receives visual input from telencephalic components of the tectofugal pathway. According to a more recent study ~6 the archistriatum also receives a more direct paucisynaptic visual input. It is therefore likely that at least parts of the archistriatum are involved in visual information processing. The OM as the main efferent pathway of the archistriatum would then also convey visual information and could modulate the intertectal inhibition in a way similar the TSM. If this assumption is correct, unilateral lesions of the O M would by analogy be expected to produce more profound deficits on a visual discrimination task than bilateral ones. METHOD
Sixteen experimentally naive adult homing pigeons (Columba livia) were used. They were maintained at 80~o of their normal body weight throughout the experiments. A conventional Skinner box with a single response key on which the visual stimuli were back-projected with a multi-channel microprojector was used. Rewards were delivered with a solenoid activated foodhopper, situated below the response key. A reinforcement light accompanied food reward. The box, which was located in a sound-attenuated chamber, was illuminated by a houselight. All relevant events were programmed with a digital
microprocessor, which also counted the keypecking responses. Pecking on the white-light illuminated key was shaped using an autoshaping procedure. When the animals had learned to associate key pecking with food reward, the discrimination program began. Two stimuli, shown in Fig. 1, were successively projected onto the response key in a quasi-random sequencelL For half of the pigeons one of the two stimuli was deemed to be correct and for the other half the other. Pecks to the correct stimulus yielded 4 s of food access. Each peck on the incorrect stimulus extended the projection time for 2 s, thus ensuring eventual extinction of pecking to the incorrect pattern. Without such extension each trial lasted 20 s. Trials with the correct pattern lasted also 20 s including the 4 s for eventual food delivery. To assess the frequency of pecking to the correct and the incorrect stimuli only the responses during the standard first 20 s were considered. Each session consisted of 40 trials. At the beginning of the discrimination the pigeons were reinforced on a VR 4 schedule. After reaching 85 ~o of correct responses in one session the ratio was increased to VR 8, then to VR 16 and finally to VR 32. Due to the lean reinforcement schedule the pigeons did not receive food on every positive trial. Since there was no apparent difference between positive trials with or without reinforcement the separate calculation of response rates preceding or following food delivery seemed not to be necessary. After reaching 85 ~o of correct responses in 3 consecutive sessions with a VR 32 schedule the acquisition phase was completed and the pigeons underwent surgery. While the animals were anaesthetized with a pentobarbital - chloral hydrate mixture (for details see ref. 27) the scalp was incised at the midline and retracted sideways. The skull was trephined using a dental drill over the appropriate locations. For radiofrequency electrocoagulation a 0.25 mm thick insect needle, insulated except for 0.50 mm at the tip, was used. The electrode was introduced under stereotaxic guidance. At the coordinates A 7, L 5, D 7 and A 8, L 5, D 6.75 of the pigeon brain atlas 25 where the O M courses at the most ventral border of the telencephalon the tissue was coagulated for 20 s with 15 mA. Preliminary data
had shown that a coagulation with these parameters resulted in a lesion-size of about 1 mm 3. In 4 animals only the left and in 4 other animals only the right OM was coagulated. Four pigeons received bilateral lesions, and 4 control pigeons were only sham-operated. The 16 animals were randomly distributed over these 4 groups. At the end of the operation a small metal head block with a tapped hole was fixed to the skull of each animal with dental cement. The animals were allowed to recover from the operation for 4 days before the discrimination procedure continued. The pigeons pecked on alternate sessions with both eyes open or with sight restricted to one eye by means of eyecaps which were screwed onto the metal headblock. The hemispherical opaque eye caps were constructed of gauze and acetone cement. The sequence of the right and left monocular and binocular conditions was balanced amongst animals. Each pigeon completed 18 sessions, that is 6 sessions under each condition. Then the pigeons were perfused intracardially with saline and 4~o formaline and the location of the lesions was ascertained in Olivecrona-stained brain sections 3°.
RESULTS
In all animals the lesions were restricted to the expected extent and location (Fig. 1). In the first postoperative days 3 of the 4 pigeons with lesions of the left OM showed a marked inattention of the right side. They did not respond to the experimenter's hand touching the right side of their body, nor to approach of this hand from the right. None of the other pigeons with bilateral or right-sided lesions showed a similar defect. The performance of the animals in the discrimination task was assessed in two ways: (a) by the total number of responses, that is the sum of the correct and incorrect responses issued in each session and (b) by the percent correct responses, that is the ratio of the number of correct to the total number of responses per session. An overall ANOVA demonstrated that the lesions had a significant effect on the behavioral results of the animals (F3,1o65 = 2.89, P < 0.05).
In Fig. 2 the means of the total number of pecking responses for the binocular and both monocular conditions are shown for all groups. In the control group the number of pecking responses was lower in each monocular condition as compared with the binocular one (each F1,33 > 13.57, P < 0.01). There was also a clear difference between the two monocular conditions of the control birds. The quantity of pecking responses emitted in the right eye seeing condition was significantly larger than in the left eye seeing one (F 1,33 = 6.36, P < 0.05). In the unilaterally lesioned animals there were clear differences between the behavioural results of left- and right-sided lesions of the OM. While pigeons with lesions of the right OM showed no deficits in any of the eye cap conditions as compared with the control group (each F1, 6 < 3.23, P > 0.1) the performance of the animals with coagulations of the left OM was clearly impaired. Both in the binocular and in the right eye seeing performance the animals with left OM lesions showed significantly lower numbers of pecking responses than the control birds (each F~,6 > 6.45, P < 0.05). Compared with the control group, the performance of the left OM lesioned birds in the left eye seeing condition was also deficient, but this effect did not reach statistical significance (F~.6 = 2.11, P > 0.05). The animals with bilateral lesions of the OM showed a deficit in terms of the numbers of pecking responses only in the binocular condition (F~.6 = 10.41, P < 0.05). In both monocular seeing conditions there were no significant differences between control and bilaterally lesioned pigeons (each F I , 6 < 1.48, P > 0.1). The animals with left OM lesions had significant deficits in both monocular conditions in comparison with the pigeons in the two other experimental groups. In the right eye seeing condition the left OM lesioned group showed significantly fewer pecking responses than both other experimental groups (each F~.6 > 7.99, P < 0.05). The amount of pecks during the left eye seeing condition was also reduced, but this deficit was significant only in the comparison with the right OM lesioned group (F~,6 = 6.21, P < 0.05), while the difference in comparison with the bilaterally OM lesioned animals just failed to reach statisti-
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cal significance ( E l , 6 = 5.29, P > 0.05). There were no significant differences in any monocular or binocular seeing conditions between the performances of the bilateral O M and right side O M lesioned groups. In Fig. 3 the means of the percent correct discrimination scores for the 3 eye cap conditions of all groups are shown. The results obtained in the left eye seeing condition were in all groups lower than in both the right eye and the binocular seeing condition. These differences were significant in the control animals (each F1,33 > 7.97, P < 0.01) and in the pigeons with lesions of the right O M (each F1.33 > 7.02, P < 0.05). As is obvious from Fig. 3, there were virtually no differences among the performances of the four groups in the percent correct discrimination scores (each F1,6 < 4.79, P > 0.1).
DISCUSSION The control pigeons showed a right eye superiority in the number of pecking responses as well as in the percent correct responses of the discrimination task. From the virtually complete decussation of the optic nerves it follows that most of the information coming from one eye is mainly processed in the contralateral hemisphere 35'46. Thus the superiority in the right eye seeing condition implies a superiority of the left brain hemisphere. This agrees with previous studies in birds demonstrating a dominance of the left hemisphere in a variety of visual tasksl,~3"14'lT'21'23'39"4°. A dominance of the left hemisphere for visually guided behaviour can also be inferred from the differential effects of the unilateral coagulations in
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Fig. 3. Means and standard errors of the percent correct responses per session under the binocular and the two monocular seeing conditions. Significant P values are indicated at the bottom of the figure (two dots: P < 0.01, one dot: P < 0.05).
the left or the right hemisphere. While lesions of the right O M did not affect the results in the discrimination task, coagulations of the left O M impeded the performance of the animals in terms of the numbers of responses emitted. Comparable results were obtained in the study of Howard et al. 21 where chicks were unable to learn a discrimination task with either the left or the fight eye after injection of glutamate into the left telencephalon. Injections of the same transmitter into the right telencephalon did not affect the performance of the animals. The differential effects of left- and right-sided OM transactions are understandable in terms of the lateralization of the visual system in birds. However, the coagulation of the left O M as such cannot be the reason for the deficits observed since bilaterally lesioned pigeons showed no deft-
cits in either monocular conditions as compared with controls. This result confirms at least partly the previously mentioned hypothesis that unilateral lesions of the O M would cause stronger deficits than bilateral OM lesions. Assuming that the archistriatum modulates the intertectal inhibition which is exerted by the inhibitory tectal commissures 3s, unilateral lesions of the efferent pathway of the archistriatum would produce an inhibitory intertectal imbalance which leads to the observed deficits. Symmetrical coagulations of the O M would cause no such inhibitory imbalance at tectal level so that the deficits would be minimal. This interpretation is in accordance with the observations of Nau and Delius 29 that pigeons with bilateral lesions in the wulst show smaller deficits than unilaterally lesioned animals. Nau and Delius 29 postulated that the loss of the excita-
tory effect of the wulst on ipsilateral tectal neurons leads to an undercompensation of the inhibitory afferences from the contralateral tectum. This hypothesis is supported by electrophysiological experiments which demonstrate that the intertectal interaction is mainly inhibitory38, that an important component of the Wulst effects on the tectal units is e x c i t a t o r y 2,6 and that half of the visual tectal units receive afferents from the ipsilateral Wulst and the contralateral tectum ~8. Unfortunately, there are no electrophysiological investigations on the effect of archistriatal stimulation on tectal neurons. However, from the fact that both the OM and the TSM synapse on neurons essentially belonging to the same tectal l a m i n a e 3"48"49 and the observation that unilateral left OM lesions lead to stronger deficits than bilateral lesions, it can be concluded that the OM modulates the intertectal inhibition in a way similar to the TSM. There are comparable results in studies with mammals which demonstrate also more profound deficits after unilateral than after bilateral lesions. Sprague 45 observed deficits in cats in the contralateral visual hemifield after unilateral lesions of the visual cortex. Destruction of the superior colliculus contraiateral to the cortical lesion site or a collicular commissurotomy restored the animals' visual performance. Sprague 45 also explained his results with an inhibitory intercollicular imbalance after a unilateral visual cortex lesion, which was eliminated a f t e r t h e ablation of the contralateral superior colliculus. This hypothesis was supported in a series of b e h a v i o u r a l 43,47 and electrophysiological s t u d i e s 15,41,44. The left OM lesioned pigeons showed a significantly reduced number of pecking responses while the percent correct responses was at the level of the control birds. This means that the experimental animals discriminated very well between the two stimuli so that a pure visual sensory deficit can be excluded as a reason for their impeded performance. Furthermore, no postoperative motor deficits could be observed. The visual attention deficit without concomitant losses in discrimination ability of the left OM lesioned birds resemble a neglect in mammals 34. A key aspect of neglect is its multimodal nature
and the absence of any basic sensory or motor impairments ~9. In the present study only the visual aspect of the neglect was systematically tested, but at least during the first postoperative days a somatosensory neglect for the right side of the body was also present in most of the left OM lesioned birds. Neglect in mammals can be produced with lesions in a variety of cortical areas with efferents to the deep collicular layers 4"10'26 or with lesions of collicular efferents34. The neurons of the deep collicular layers project to different reticular nuclei of the brainstem 7'24,42. A neglect after lesions of these structures is therefore generally ascribed to arousal deficits caused by a reticular deactivation 19. The neurons of the tectal laminae in which the axons of the OM synapse project to the midbrain and pontine reticular formation 22'35 so that similar mechanisms may have produced the neglect observed in the present study. Lesions of the left TSM, the second tract which connects visual telencephalic areas with the tectum, produce deficits strikingly similar to those following lesions of the left OM (Gtlnttlrktln, in prep.). These results suggest that visual telencephalic areas of the left hemisphere modulate in a context of visually guided behaviour attentional mechanisms by interaction with tectal neurons which project to reticular nuclei of the avian brainstem. ACKNOWLEDGEMENTS
This study was supported by the Deutsche Forschungsgemeinschaft through its Sonderforschungsbereich 114. We thank Prof. J.D. Delius and Dr. J. Emmerton for critically reading the manuscript, D. Hagenk0tter for typing it, A. Lohmann for making the drawings and U. Schall for his help in the statistical calculations. REFERENCES 1 Andrew, R.J., Mench, J. and Rainey, C. Right-left asymmetry of response to visual stimuli in the domestic chick. In D.I. Ingle, M.A. Goodale and I. Mansfield (Eds'.), Advances in the Analysis of Visual Behavior, MIT Press, Cambridge, MA, 1982, pp. 197-209. 2 Bagnoli, P., Francesconi, W. and Magni, F., Interaction of optic tract and visual wulst impulses on single units of
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Behavioural Brain Research, 18 (1985) 1-9 Elsevier BBR00504
Research Papers NEGLECT AFTER SECTION OF A LEFT TELENCEPHALOTECTAL TRACT IN PIGEONS
O N U R G ~ N T ( ) R K O N and H A N S - H O R S T H O F E R I C H T E R
Ruhr-Universitiit Bochum, Experimentelle Tierpsychologie, Psychologisches Institut, Bochum (F.R.G.) (Received February 1st, 1985) (Revised version received August 27th, 1985) (Accepted August 28th, 1985)
Key words: visual discrimination - lesion - lateralization - optic tectum - neglect - pigeon
The effects of unilateral and bilateral lesions of the telencephalotectal fibres of the tractus occipitomesencephalicus (OM) were studied in pigeons in a successive visual pattern discrimination. On alternate sessions the animals performed the task with both eyes open or sight restricted to one or the other eye. Unilateral lesions of the left OM led to severe deficits in the total number of pecking responses emitted under both monocular and binocular conditions. Pigeons with lesions of the right OM showed no deficits and the animals with bilateral lesions had an impaired performance only in the binocular condition. The percent correct discrimination performance of all experimental pigeons were at the same level as that of the control group. The results are discussed in the context of visual lateralization in birds. It is suggested that the deficits reflect a sensory neglect through deactivation of neurons in the deep tectal laminae which are known to have projections to reticular nuclei of the brainstem.
INTRODUCTION
Previous studies on the behavioural effects of lesions of the avian visual system have primarily concentrated on the two pathways which convey optic information to the telencephalon of birds 1~. One of these pathways, the tectofugal route, begins with optic nerve axons which decussate completely in the chiasma opticum and terminate in the optic tectum. This structure in turn projects on the nucleus rotundus in the thalamus, which itself sends fibres to the ipsilateral ectostriatum, a core area of the telencephalon 5. The other visual pathway, the thalamofugal route, consists of retinal fibres which also decussate completely in the chiasma opticum and proceed to a nuclear complex in the contralateral thalamus. These nuclei in turn project mainly to the ipsilateral wulst, a structure in the frontodorsal telencephalon 28. Lesions of the ectostriatum yield severe deficits in
visual pattern and brightness discrimination tasks (ref. 20, but see ref. 8). Bilateral lesions of the wulst lead only to minor impairments in simple visual colour, brightness and pattern discriminations 31"33. Paradoxical results were reported by Nau and Delius 29 who found marked deficits in simple pattern discriminations when pigeons with unilateral wulst ablations used the eye contralateral to the lesioned hemisphere, while bilaterally lesioned animals showed no deficits. When using the ipsilateral eye the discrimination performance of the unilaterally lesioned animals was at the level of the control birds. Nau and Delius 29 ascribed these results to the modulatory effect which is exerted by the wulst via its efferent pathway, the tractus septomesencephalicus (TSM), on intertectal inhibition which is conveyed by the commissura tectalis and the commissura posterior. Assuming that the partly excitatory effect of the TSM at the tectal level compensates the inhibitory
Correspondence: 0. Glintiirkiin, Ruhr-Universit~it Bochum, Experimentelle Tierpsychologie, Psychologisches Institut, D 4630 Bochum, F.R.G.
2 effect of the contralateral tectum, unilateral lesions of the wulst could create an inhibitory intertectal imbalance which can be corrected by an additional ablation of the intact Wulst, or else of the intact TSM. According to this suggestion it is not the lesion of the Wulst, or else of the T S M as such but the asymmetrical inhibitory interaction between the tecta that would account for the observed deficits. There are indeed electrophysiological 2'38, as well as behavioural results 32 which support this hypothesis. The only other telencephalotectal pathway of birds is the tractus occipitomesencephalicus (OM) which originates in the archistriatum and projects to lamina III of the ipsilateral tectum where fibres of the T S M also synapse 3,9,48,49. Ritchie 37 suggested that the O M arises from a subdivision of the archistriatum that receives visual input from telencephalic components of the tectofugal pathway. According to a more recent study ~6 the archistriatum also receives a more direct paucisynaptic visual input. It is therefore likely that at least parts of the archistriatum are involved in visual information processing. The OM as the main efferent pathway of the archistriatum would then also convey visual information and could modulate the intertectal inhibition in a way similar the TSM. If this assumption is correct, unilateral lesions of the O M would by analogy be expected to produce more profound deficits on a visual discrimination task than bilateral ones. METHOD
Sixteen experimentally naive adult homing pigeons (Columba livia) were used. They were maintained at 80~o of their normal body weight throughout the experiments. A conventional Skinner box with a single response key on which the visual stimuli were back-projected with a multi-channel microprojector was used. Rewards were delivered with a solenoid activated foodhopper, situated below the response key. A reinforcement light accompanied food reward. The box, which was located in a sound-attenuated chamber, was illuminated by a houselight. All relevant events were programmed with a digital
microprocessor, which also counted the keypecking responses. Pecking on the white-light illuminated key was shaped using an autoshaping procedure. When the animals had learned to associate key pecking with food reward, the discrimination program began. Two stimuli, shown in Fig. 1, were successively projected onto the response key in a quasi-random sequencelL For half of the pigeons one of the two stimuli was deemed to be correct and for the other half the other. Pecks to the correct stimulus yielded 4 s of food access. Each peck on the incorrect stimulus extended the projection time for 2 s, thus ensuring eventual extinction of pecking to the incorrect pattern. Without such extension each trial lasted 20 s. Trials with the correct pattern lasted also 20 s including the 4 s for eventual food delivery. To assess the frequency of pecking to the correct and the incorrect stimuli only the responses during the standard first 20 s were considered. Each session consisted of 40 trials. At the beginning of the discrimination the pigeons were reinforced on a VR 4 schedule. After reaching 85 ~o of correct responses in one session the ratio was increased to VR 8, then to VR 16 and finally to VR 32. Due to the lean reinforcement schedule the pigeons did not receive food on every positive trial. Since there was no apparent difference between positive trials with or without reinforcement the separate calculation of response rates preceding or following food delivery seemed not to be necessary. After reaching 85 ~o of correct responses in 3 consecutive sessions with a VR 32 schedule the acquisition phase was completed and the pigeons underwent surgery. While the animals were anaesthetized with a pentobarbital - chloral hydrate mixture (for details see ref. 27) the scalp was incised at the midline and retracted sideways. The skull was trephined using a dental drill over the appropriate locations. For radiofrequency electrocoagulation a 0.25 mm thick insect needle, insulated except for 0.50 mm at the tip, was used. The electrode was introduced under stereotaxic guidance. At the coordinates A 7, L 5, D 7 and A 8, L 5, D 6.75 of the pigeon brain atlas 25 where the O M courses at the most ventral border of the telencephalon the tissue was coagulated for 20 s with 15 mA. Preliminary data
had shown that a coagulation with these parameters resulted in a lesion-size of about 1 mm 3. In 4 animals only the left and in 4 other animals only the right OM was coagulated. Four pigeons received bilateral lesions, and 4 control pigeons were only sham-operated. The 16 animals were randomly distributed over these 4 groups. At the end of the operation a small metal head block with a tapped hole was fixed to the skull of each animal with dental cement. The animals were allowed to recover from the operation for 4 days before the discrimination procedure continued. The pigeons pecked on alternate sessions with both eyes open or with sight restricted to one eye by means of eyecaps which were screwed onto the metal headblock. The hemispherical opaque eye caps were constructed of gauze and acetone cement. The sequence of the right and left monocular and binocular conditions was balanced amongst animals. Each pigeon completed 18 sessions, that is 6 sessions under each condition. Then the pigeons were perfused intracardially with saline and 4~o formaline and the location of the lesions was ascertained in Olivecrona-stained brain sections 3°.
RESULTS
In all animals the lesions were restricted to the expected extent and location (Fig. 1). In the first postoperative days 3 of the 4 pigeons with lesions of the left OM showed a marked inattention of the right side. They did not respond to the experimenter's hand touching the right side of their body, nor to approach of this hand from the right. None of the other pigeons with bilateral or right-sided lesions showed a similar defect. The performance of the animals in the discrimination task was assessed in two ways: (a) by the total number of responses, that is the sum of the correct and incorrect responses issued in each session and (b) by the percent correct responses, that is the ratio of the number of correct to the total number of responses per session. An overall ANOVA demonstrated that the lesions had a significant effect on the behavioral results of the animals (F3,1o65 = 2.89, P < 0.05).
In Fig. 2 the means of the total number of pecking responses for the binocular and both monocular conditions are shown for all groups. In the control group the number of pecking responses was lower in each monocular condition as compared with the binocular one (each F1,33 > 13.57, P < 0.01). There was also a clear difference between the two monocular conditions of the control birds. The quantity of pecking responses emitted in the right eye seeing condition was significantly larger than in the left eye seeing one (F 1,33 = 6.36, P < 0.05). In the unilaterally lesioned animals there were clear differences between the behavioural results of left- and right-sided lesions of the OM. While pigeons with lesions of the right OM showed no deficits in any of the eye cap conditions as compared with the control group (each F1, 6 < 3.23, P > 0.1) the performance of the animals with coagulations of the left OM was clearly impaired. Both in the binocular and in the right eye seeing performance the animals with left OM lesions showed significantly lower numbers of pecking responses than the control birds (each F~,6 > 6.45, P < 0.05). Compared with the control group, the performance of the left OM lesioned birds in the left eye seeing condition was also deficient, but this effect did not reach statistical significance (F~.6 = 2.11, P > 0.05). The animals with bilateral lesions of the OM showed a deficit in terms of the numbers of pecking responses only in the binocular condition (F~.6 = 10.41, P < 0.05). In both monocular seeing conditions there were no significant differences between control and bilaterally lesioned pigeons (each F I , 6 < 1.48, P > 0.1). The animals with left OM lesions had significant deficits in both monocular conditions in comparison with the pigeons in the two other experimental groups. In the right eye seeing condition the left OM lesioned group showed significantly fewer pecking responses than both other experimental groups (each F~.6 > 7.99, P < 0.05). The amount of pecks during the left eye seeing condition was also reduced, but this deficit was significant only in the comparison with the right OM lesioned group (F~,6 = 6.21, P < 0.05), while the difference in comparison with the bilaterally OM lesioned animals just failed to reach statisti-
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cal significance ( E l , 6 = 5.29, P > 0.05). There were no significant differences in any monocular or binocular seeing conditions between the performances of the bilateral O M and right side O M lesioned groups. In Fig. 3 the means of the percent correct discrimination scores for the 3 eye cap conditions of all groups are shown. The results obtained in the left eye seeing condition were in all groups lower than in both the right eye and the binocular seeing condition. These differences were significant in the control animals (each F1,33 > 7.97, P < 0.01) and in the pigeons with lesions of the right O M (each F1.33 > 7.02, P < 0.05). As is obvious from Fig. 3, there were virtually no differences among the performances of the four groups in the percent correct discrimination scores (each F1,6 < 4.79, P > 0.1).
DISCUSSION The control pigeons showed a right eye superiority in the number of pecking responses as well as in the percent correct responses of the discrimination task. From the virtually complete decussation of the optic nerves it follows that most of the information coming from one eye is mainly processed in the contralateral hemisphere 35'46. Thus the superiority in the right eye seeing condition implies a superiority of the left brain hemisphere. This agrees with previous studies in birds demonstrating a dominance of the left hemisphere in a variety of visual tasksl,~3"14'lT'21'23'39"4°. A dominance of the left hemisphere for visually guided behaviour can also be inferred from the differential effects of the unilateral coagulations in
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the left or the right hemisphere. While lesions of the right O M did not affect the results in the discrimination task, coagulations of the left O M impeded the performance of the animals in terms of the numbers of responses emitted. Comparable results were obtained in the study of Howard et al. 21 where chicks were unable to learn a discrimination task with either the left or the fight eye after injection of glutamate into the left telencephalon. Injections of the same transmitter into the right telencephalon did not affect the performance of the animals. The differential effects of left- and right-sided OM transactions are understandable in terms of the lateralization of the visual system in birds. However, the coagulation of the left O M as such cannot be the reason for the deficits observed since bilaterally lesioned pigeons showed no deft-
cits in either monocular conditions as compared with controls. This result confirms at least partly the previously mentioned hypothesis that unilateral lesions of the O M would cause stronger deficits than bilateral OM lesions. Assuming that the archistriatum modulates the intertectal inhibition which is exerted by the inhibitory tectal commissures 3s, unilateral lesions of the efferent pathway of the archistriatum would produce an inhibitory intertectal imbalance which leads to the observed deficits. Symmetrical coagulations of the O M would cause no such inhibitory imbalance at tectal level so that the deficits would be minimal. This interpretation is in accordance with the observations of Nau and Delius 29 that pigeons with bilateral lesions in the wulst show smaller deficits than unilaterally lesioned animals. Nau and Delius 29 postulated that the loss of the excita-
tory effect of the wulst on ipsilateral tectal neurons leads to an undercompensation of the inhibitory afferences from the contralateral tectum. This hypothesis is supported by electrophysiological experiments which demonstrate that the intertectal interaction is mainly inhibitory38, that an important component of the Wulst effects on the tectal units is e x c i t a t o r y 2,6 and that half of the visual tectal units receive afferents from the ipsilateral Wulst and the contralateral tectum ~8. Unfortunately, there are no electrophysiological investigations on the effect of archistriatal stimulation on tectal neurons. However, from the fact that both the OM and the TSM synapse on neurons essentially belonging to the same tectal l a m i n a e 3"48"49 and the observation that unilateral left OM lesions lead to stronger deficits than bilateral lesions, it can be concluded that the OM modulates the intertectal inhibition in a way similar to the TSM. There are comparable results in studies with mammals which demonstrate also more profound deficits after unilateral than after bilateral lesions. Sprague 45 observed deficits in cats in the contralateral visual hemifield after unilateral lesions of the visual cortex. Destruction of the superior colliculus contraiateral to the cortical lesion site or a collicular commissurotomy restored the animals' visual performance. Sprague 45 also explained his results with an inhibitory intercollicular imbalance after a unilateral visual cortex lesion, which was eliminated a f t e r t h e ablation of the contralateral superior colliculus. This hypothesis was supported in a series of b e h a v i o u r a l 43,47 and electrophysiological s t u d i e s 15,41,44. The left OM lesioned pigeons showed a significantly reduced number of pecking responses while the percent correct responses was at the level of the control birds. This means that the experimental animals discriminated very well between the two stimuli so that a pure visual sensory deficit can be excluded as a reason for their impeded performance. Furthermore, no postoperative motor deficits could be observed. The visual attention deficit without concomitant losses in discrimination ability of the left OM lesioned birds resemble a neglect in mammals 34. A key aspect of neglect is its multimodal nature
and the absence of any basic sensory or motor impairments ~9. In the present study only the visual aspect of the neglect was systematically tested, but at least during the first postoperative days a somatosensory neglect for the right side of the body was also present in most of the left OM lesioned birds. Neglect in mammals can be produced with lesions in a variety of cortical areas with efferents to the deep collicular layers 4"10'26 or with lesions of collicular efferents34. The neurons of the deep collicular layers project to different reticular nuclei of the brainstem 7'24,42. A neglect after lesions of these structures is therefore generally ascribed to arousal deficits caused by a reticular deactivation 19. The neurons of the tectal laminae in which the axons of the OM synapse project to the midbrain and pontine reticular formation 22'35 so that similar mechanisms may have produced the neglect observed in the present study. Lesions of the left TSM, the second tract which connects visual telencephalic areas with the tectum, produce deficits strikingly similar to those following lesions of the left OM (Gtlnttlrktln, in prep.). These results suggest that visual telencephalic areas of the left hemisphere modulate in a context of visually guided behaviour attentional mechanisms by interaction with tectal neurons which project to reticular nuclei of the avian brainstem. ACKNOWLEDGEMENTS
This study was supported by the Deutsche Forschungsgemeinschaft through its Sonderforschungsbereich 114. We thank Prof. J.D. Delius and Dr. J. Emmerton for critically reading the manuscript, D. Hagenk0tter for typing it, A. Lohmann for making the drawings and U. Schall for his help in the statistical calculations. REFERENCES 1 Andrew, R.J., Mench, J. and Rainey, C. Right-left asymmetry of response to visual stimuli in the domestic chick. In D.I. Ingle, M.A. Goodale and I. Mansfield (Eds'.), Advances in the Analysis of Visual Behavior, MIT Press, Cambridge, MA, 1982, pp. 197-209. 2 Bagnoli, P., Francesconi, W. and Magni, F., Interaction of optic tract and visual wulst impulses on single units of
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