73
Behavioural Brain Research, 40 (1990) 73-80 Elsevier BBR01094
Visuomotor feeding perturbations after lateral telencephalic lesions in pigeons Ralf J~ger Experimentelle Tierpsychologie, Psychologisches Institut, Ruhr-Universitiit Bochum, D-4630 Bochum (F.R.G.) (Received 18 January 1990) (Revised version received 5 March 1990) (Accepted 31 May 1990)
Key words: Grasping; Lesion; Pecking; Telencephalon; Visual discrimination; Pigeon
Pigeons with lesions of the lateral part of the telencephalon, visual Wulst, and fronto-archistriatal tract were compared with sham-operated controls in 2 procedures. In one of them the time it took the pigeons to grasp and eat a certain number of grains was recorded. In the other experiment the number of grains was counted that the pigeons consumed out of a mixture of grains and pebbles within a fixed time interval. Only the pigeons with lateral telencephalic lesions were impaired. While in the first experiment the lateral ablated birds improved with time there was no recovery of performance in the second experiment.
INTRODUCTION
While it has long been accepted that normal eating in the pigeon is permanently abolished by decerebration or telencephalic ablation ~'2°the critical regions involved have not yet been identified. Salzen et al.18 found that lateral telencephalic lesions decreased the accuracy of peck localization and disrupted grasping and mandibulation in chicks feeding from a mixture of pebbles and grains. They suggested that the lateral telencephaIon might play some role in the coordination of inputs involved in eating. Eating in the pigeon involves a sequence of pecking, grasping and mandibulation that requires the precise coordination of neck, head and jaw movements. Behavioral a n a l y s e s 5"24'25 suggest that this behavior is under the sequential control of 2 different sensory systems -vision and
oral somatosensation. Pecking is elicited and guided by visual inputs and involves both the identification and localization of the food object 7. Grasping is characterized by an adjustment of gape size to object size 4'12A3 and may thus require inputs from both vision and jaw proprioception. Mandibulation, i.e. intraoral manipulation of the food object, is dependent upon somatosensory (trigeminal) feedback from the beak 22. Lesions of the lateral telencephalon in adult pigeons have been shown to produce deficits in color, intensity and pattern discrimination tasks utilizing an operant, key-pecking paradigm 6 but eating was not examined. The lesions in these studies included the lateral neostriatum (N), the lateral edge of the ventral hyperstriatum (HV), the lateral corticoid area (CDL) and the area temporo-parieto-occipitalis (TPO). This area is in receipt of inputs from both the visual and the
Correspondence: R. J~ger, Universit~it Konstanz, Sozialwissenschaftliche Fakult~it, Allgemeine Psychologie, Postfach 5560, D-7750 Konstanz, F.R.G. 0166-4328/90/$03.50 © 1990 Elsevier Science Publishers B.V. (Biomedical Division)
74 trigeminal system. The lateral part of the caudal neostriatum (NC) receives intratelencephalic visual afferents from the ectostriatal belt 17. Trigeminal inputs are relayed from the basofrontal telencephalon via the fronto-archistriate tract (FA) which terminates within a region of the caudal neostriatum (NCT). This region is a component of a trigeminal sensorimotor circuit, originating in the principal sensory trigeminal nucleus (PrV), including the nucleus basalis (N. bas), neostriatum caudale, pars trigeminale (NCT) and archistriatum (A) and terminating in jaw premotor and motor neurons 3"~9"21. Lesions of various structures in this circuit have been shown to disrupt peck localization, grasping, and food manipulation 14-22. Given this pattern of visual and trigeminal inputs, the lateral telence-
L 10
I
5
0
5
10
I
t
I
I
A4
phalon seemed an appropriate starting point tot studies designed to clarify the role oftelencephalic structures in the control of eating in the pigeon. The present study was designed to examine the effects of lateral telencephalic lesions upon the identification, localization and grasping of the food object. The deficits seen after such lesions were compared with those seen after control lesions of the Wulst and of the fronto-archistriate tract, which convey visual and trigeminal afterents, respectively. MATERIALS A N D M E T H O D S
Subjects Twenty adult pigeons (Columba livia) of unknown sex and age were housed in individual
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) Fig. 1. Lesions of the lateral telencephalon (abbreviations, see text).
75 cages in a colony room with a 12/12-h light/dark cycle. Throughout the experiment, they were maintained at 80 ~ of their free-feeding weight by food deprivation.
Behavioral procedures (1) Ingestive efficiency. The food trough normally attached to the home cage was replaced by a transparent trough (width: 9 cm, depth: 5 cm, height: 6 cm). Ten safflower seeds (Carthamus tinctorius, average length 4 mm) were presented in the trough and pecking behavior was timed from the first peck until all grains were consumed.
(2) Discriminationoffood from non-food objects. Thirty safflower seeds and pebbles of roughly similar sizes were mixed to produce a pebble/seed mixture (volume: 30 ml) and presented in the trough. Subjects were allowed to peck for 30 s, after which the trough was removed and the number of seeds consumed was recorded. Preoperatively, subjects were trained on both tasks for 15 consecutive daily sessions and the last 10 or 5 sessions (see below) provided baseline data. The pigeons were then matched according to their baseline performance and assigned to 5 different treatment conditions (n = 4) as follows:
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(1) ablation of the lateral telencephalon, (2) Wulst ablation, (3)transection of the tractus frontoarchistriatalis (FA), (4) control surgical procedure for the Wulst- and laterally lesioned birds, and (5) a second control surgical procedure for the FA-birds, which were tested some months later. Postoperative testing commenced after a 3-day recovery period and continued for 20 (treatment condition 1, 2, 4) or 10 (treatment condition 3, 5) consecutive daily sessions.
Surgical and h&tologicalprocedures Subjects were anesthetized with a barbiturate/chloral hydrate solution (0.5 ml/100 g body weight, i.m.15). After local applications of xylocaine they were placed in a stereotaxic apparatus, the scalp was incised along the midline and surgical procedures were carried out guided by coordinates drawn from a stereotaxic atlas 1°. All procedures were bilateral. For the lateral telencephalic ablation lines were drawn on both sides of the skull from coordinates A 6/L 7 - A 13/L 5.5. The bone was removed along that line with a dental drill, brain tissue to be removed separated with a vertical scalpel incision and aspirated through a pipette. The space was packed
AI4
A8 ~D
A9 HD
AIO HO
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Fig. 2. Lesions of the visual Wulst (abbreviations, see text).
76 with gelfoam and the wound sutured. For the Wulst ablation, a quadrangular plate of bone was defined by coordinates A 14/L 1-3 and A 9/L 1-3 and removed. Wulst tissue was removed by an aspiration procedure adjusted so as not to exceed the dorsal surface of the ventral hyperstriatum. FA was sectioned electrolytically using a stainless steel electrode insulated except for a 0.5-mm tip. The needle was inserted at each of 3 overlapping locations along a medio-lateral line (A 10.5/L 6.0, L 6.5 and L 7.0), advanced until it reached the skull floor and then retracted for 0.5 ram. A lesion was placed at each location (9 mA for 15 s). The surgical control birds sustained identical treatment, except for insertion of an electrode. At the conclusion of the experiment, the animals were anesthetized, perfused intracardially with a 0.9~o saline solution (40 °C) followed by 4% formalin. After fixation for a week in 4~o formalin brains were removed, embedded in egg-yolk, hardened in formalin vapors for a week and cut at 40/~m, with every 13th section stained with cresylviolet. With the aid of a microscope, the extent of the lesions was transferred to drawings of transverse brain sections taken from the Karten and Hodos 1° atlas. RESULTS
Anatomical The ablations in the lateral telencephalic group were generally symmetrical (Fig. 1). In all birds the dorsolateral part of the neostriatum and the area temporo-parieto-occipitalis (TPO) had been aspirated. In 2 birds parts of the lateral corticoid area (CDL) had been destroyed, 2 others had minor, unilateral damage to the outermost part of ectostriatum (E) while in 2 other subjects both the lateral pole of the archistriatum (A) and FA sustained bilateral damage. The Wulst lesions (Fig. 2) varied somewhat in extent and were slightly asymmetrical, but in all cases the anterior portion of the visual Wulst had been removed. One bird sustained almost complete unilateral removal of the hyperstriatum ventrale. In 3 of the FA birds, the tract was transected bilaterally; in the 4th the damage was unilateral and its data were therefore excluded from the analysis (Fig. 3).
One sham-operated FA control bird died under anesthesia.
Behavioral A measure of ingestive efficiency for each of the groups was obtained by calculating the mean time
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Fig. 3. Transsections of the frontoarchistriatal tract LPO, lobus parolfactorius; QF, tractus quintofrontalis; for further abbreviations, see text.
77 needed to ingest all ten of the seeds. Session-bysession data for this task under each of the treatment conditions are presented in Figs. 4 and 5. Analyses of variance ~l indicated no significant differences between the groups preoperatively. Postoperatively, there were no significant differences between the Wulst, sham-operated controls and FA birds. However, postoperative comparisons indicated that the lateral telencephalic group took significantly longer to ingest the seeds than the other treatment groups (lateral vs. control: FI,6 = 8.4, P < 0.05; lateral vs. Wulst: F 1 , 6 = 10.8, P < 0.05). After about 6days of testing the lateral subjects showed a highly significant recovery (first 10 sessions vs. last 10 sessions: F1.39 = 8.0, P < 0.01) and performance locked up slightly below their preoperative levels. Incidental observations of this temporary deficit of the lateral birds indicated that the birds were capable of peck localization, since many of their pecks made contact with the seeds. However, these subjects appeared to have considerable difficulties with mandibulation. Pecks result-
control o~O~-D O~ o/ ~
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Fig. 5, Pre- and postoperative means of time needed to grasp 10 grains ( 0 , I , ingestive efficiency) and of numbers of grains grasped ( 0 , V-l,discrimination of food from non-food objects) by pigeons with lesions in the frontoarchistriatal tract.
ing in contacts were not followed by grasping and the seeds were scattered within the trough. Birds frequently failed to ingest even those seeds which were successfully grasped. In other cases, the
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78 control
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Fig. 6. Pre- and postoperative means of numbers of grains grasped by Wulst- and lateral lesioned pigeons (discrimination of food from non-food objects).
seeds were turned around within the beak before being swallowed. While birds of the other treatment groups grasped several seeds consecutively, the lateral telencephalic subjects could grasp an additional grain only after the preceding one had been swallowed. Moreover, lateral subjects refused to eat large size seeds (maize and peas) when mixed with their normal diet. Finally, the lateral birds continued to peck at seeds they had missed, while the other subjects generally pecked at the next closest grain. An index of the birds' ability to discriminate food from non-food objects was obtained from measures of seeds and pebbles ingested in a 30-s test period and the data for each treatment group are presented in Figs. 5 and 6. While there were no preoperative differences between the groups, the lateral group ingested only about 8-10 seeds per session postoperatively, in contrast to 20-25 seeds per session for the Wulst and control groups. These differences were significant beyond the 0.01 level for both comparisons (lateral vs. Wulst: F I , 6 = 153.2, P < 0.01 ; lateral vs. control: F I , 6 = 674.2, P < 0.01). Although the number of pecks made by each group was not recorded,
incidental observations suggested that they did not differ sufficiently in this respect to account for the differences in the number of seeds ingested. Moreover, in contrast to the other subjects, the lateral telencephalic birds appeared to be ingesting an increased amount of pebbles. No improvement in the pebble-seed discrimination task was seen during the 20 postoperative sessions. DISCUSSION
Behavioral studies of the avian brain have suggested that the lateral telencephalon may play some role in the sensorimotor control of feeding TM. The area is known to receive inputs from both the visual 2'~7 and trigeminal systems 21 and there is evidence from a cyto- and myeloarchitectonic mapping s t u d y 16 that it may be involved in integrating afferents from several modalities with efferent systems. To test this hypothesis we examined the effects of lateral telencephalic ablations upon tasks designed to distinguish between different components of the pigeon's feeding response sequence. The first of these tasks required the visual localization and
79 subsequent ingestion of seeds; the second required, in addition, a discrimination between food and non-food objects (seeds vs. pebbles). None of the lesioned subjects had problems in maintaining weight or food uptake in the cage except for lateral lesioned birds, which left out larger size grains. For subjects with Wulst lesions or FA transections no significant deficit was seen in either task. However, subjects with lateral telencephalic lesions, showed significant reduction in performance on both tasks. In the first task, there was no obvious effect upon peck localization (i.e., most pecks terminated in contact with the seed), but the probability of grasping was reduced and the time taken for mandibulation was increased. Several days after surgery, however, the birds' performance rose to slightly below their preoperative level and that of the control group. These deficits are most parsimoniously interpreted as reflecting a deficit in the trigeminal sensorimotor control of ingestion though the participation of a minor localization deficit could not be excluded. Similar deficits are seen after trigeminal deafferentation23, or lesions of central trigeminal structures, including N. bas. and NCT 22. On the second task, lateral telencephalic subjects reduce their intake of seeds and increase their intake of pebbles postoperatively. In contrast to what happened with the former task the birds' performance did not recover. Although the increased intake of pebbles suggests a deficit in the oral somatosensory discrimination of food from non-food objects, this deficit only explains why an object cannot be identified as a seed or a pebble once it is grasped. It does not explain, however, the decrease in grasped (e.g. ingested) seeds, since pecking and grasping is under visual control 13. Furthermore, feeding behavior in the first task showed a significant recovery to almost preoperative level and thus one also should expect a recovery of performance in the discrimination of food from non-food objects. Therefore the permanently reduced intake of seeds in the second task reflects a visual discrimination deficit. Thus lateral telencephalic lesions produce deficits in both the manipulative and discriminative components of ingestive behavior and these deficits involve disruptions of both visual and trigeminal
processes. A remarkable recovery from the mandibulative deficit must be contrasted against the permanence of the discriminative deficit. Therefore these latter results confirm the persisting visual discrimination deficits of lateral telencephalon-ablated pigeons reported earlier6. The results of the present study thus support a role for the lateral telencephalon in the visuomotor and somatosensorimotor control of eating in the pigeon. The fact that recovery from the manipulation and visual discrimination deficits have different time-courses suggests that they have different though possibly overlapping neural substrates. It seems unlikely that the defect reflects damage to multimodal neurons. Moreover, the absence of deficits in the Wulst group suggests that pathways other than the thalamofugal system mediate the visual discrimination of food from non-food objects. The tectofugal-ectostriatal pathway seems a likely candidate. Our results also qualify earlier reports suggesting that the FA is important in transferring trigeminal information to the archistriatum 2~. FA transections in our hands failed to produce deficits in any of the tasks we used. A visual role for this tract is therefore negated. Finally, it is known that both visual and trigeminal inputs project upon the archistriatum in the pigeon 8"9'17'21. An analysis of its role in the visuomotor and somatosensorimotor control of feeding would be of considerable interest. ACKNOWLEDGEMENTS This research was supported by the Deutsche Forschungsgemeinschaft. While preparing the manuscript the author was supported by a D F G postdoctoral grant (II 0 2 - Ja 433/1-1). The assistance of Prof. J.D. Delius (Konstanz) and H.P. Zeigler (New York) who carefully revised the manuscript, and G. Keim (Bochum) and B. Bayless (New York) who did the photographic work is gratefully acknowledged. REFERENCES 1 Akerman, B., Fabricius, E., Larsson, B. and Steen, L., Observations on pigeonswithprethalamicradiolesionsin the nervous pathway from the telencephalon, Acta PhysioL Scand., 56 (1962) 286-298.
80 2 Belekhova, M.G., Subcortico-cortical relationships in birds, Neurosci. Transl., 2 (1968) 195-203. 3 Berkhoudt, H., Klein, B.G. and Zeigler, H.P., Afferents to the trigeminal and facial motor nuclei in the pigeon (Columba livia L.): central connections of jaw motoneurons, J. Comp. Neurol., 209 (1982) 301-312. 4 Deich, J., Klein, B.G. and Zeigler, H.P., Grasping in the pigeon: mechanisms of motor control, Brain Res., 337 (1985) 362-367. 5 Delius, J.D., The peck of the pigeon: free for all. In: C.F. Lowe, M. Richelle, D.E. Blackman, C.M. Bradshaw (Eds.), Behaviour Analysis and Contemporary Psychology, Erlbaum, London, 1985. 6 Delius, J.D., J~.ger, R. and Friesel, M., Lateral telencephalic lesions affect visual discriminations in pigeons, Behav. Brain Res., 11 (1984) 249-258. 7 Goodale, M.A., Visually guided pecking in the pigeon (Columba livia), Brain Behav. Evol., 22 (1983) 22-41. 8 Gfintfirkfin, O., Evidence for a third primary visual area in the telencephalon of the pigeon, Brain Res., 294 (1984) 247-254. 9 Gfintfirkfin, O., Verhaltensphysiologisehe Untersuchungen
zur funktionellen Organisation des visuellen Systems der Taube, Unpublished Dissertation, Psyehologisehes Institut der Ruhr-Universit~t Bochum, Bochum, 1984. 10 Karten, H.J. and Hodos, W., A Stereotaxic Atlas of the Brain of the Pigeon, Johns Hopkins Press, Baltimore, MD, 1967. 11 Kirk, R., Experimental Design: Procedures for the Behavioural Sciences, Brooks/Cole, Belmont, CA, 1968. 12 Klein, B.G., Deich, J.D. and Zeigler, H.P., Grasping in the pigeon (Columba livia): final common path mechanisms, Behav. Brain Res., 18 (1985) 201-213. 13 LaMon, B. and Zeigler, H.P., Grasping in the pigeon (Columba livia): stimulus control during conditioned and consumatory responses, Anim. Learn. Behav., 12 (1984) 223-231. 14 Levine, R.R. and Zeigler, H.P., Extratelencephalic pathways and feeding behavior in the pigeon (Columba livia), Brain Behav. Evol., 19 (1983) 56-92.
15 Mallin, 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. 16 Rehk~mper, G., Zilles, K. and Schleicher, A., A quantitative approach to cytoarchitectonics, X. The areal pattern of the neostriatum in the domestic pigeon (Columba #via f.d.). A cyto- and myeloarchitectonical study, Anat. Embryol., 171 (1985) 345-355. 17 Ritchie, T.L.C., lntratelencephalic Connections and their Relationship to the Archistriatum in the Pigeon (Columba livia), Thesis Ph.D., University of Virginia, Charlottesville, VA, 1979. 18 Salzen, E.A., Parker, D.M. and Williamson, A.J., A forebrain lesion preventing imprintingin domestic chicks, Exp. Brain Res., 24 (1975) 145-157. 19 Schall, U., Gfintfirkfin, O. and Delius, J.D., Sensory projections to the nucleus basalis prosencephali in the pigeon, Cell Tissue Res., 245 (1986) 539-546. 20 Thauer, R. and Peters, G., Sensibilit~it und Motorik bei lange fiberlebendenZwischen-Mittelhirntauben,Pfliiger's Arch. Ges. Physiol., 240 (1938) 503-526. 21 Wild, J.M., Arends, J.J.A. and Zeigler, H.P., Telencephalic connections of the trigeminal system in the pigeon (Columbia livia): a trigeminal sensory motor circuit, J. Comp. Neurol., 234 (1985) 441-464. 22 Zeigler, H.P. and Karten, H.J., Brain mechanisms and feeding behavior in the pigeon (Columba livia), |I. Analysis of feeding behavior deficits following lesions of quintofrontal structures, J. Comp. Neurol., 152 (1973) 83-102. 23 Zeigler, H.P., Miller, M. and Levine, R.R., Trigeminal nerve and eating in the pigeon (Columba livia): neurosensory control of the consumatory responses, J. Comp. Physiol. Psychol., 89 (1975) 854-858. 24 Zeigler, H.P., Levitt, P.W. and Levine, R.R., Eating in the pigeon (Columba livia): movement patterns, stereotypy, and stimulus control,J. Comp. Physiol. Psychol., 94 (1980) 783-794. 25 Zweers, G.A., Pecking of the pigeon (Columba livia L.), Behaviour, 81 (1982) 175-230.
Behavioural Brain Research, 40 (1990) 73-80 Elsevier BBR01094
Visuomotor feeding perturbations after lateral telencephalic lesions in pigeons Ralf J~ger Experimentelle Tierpsychologie, Psychologisches Institut, Ruhr-Universitiit Bochum, D-4630 Bochum (F.R.G.) (Received 18 January 1990) (Revised version received 5 March 1990) (Accepted 31 May 1990)
Key words: Grasping; Lesion; Pecking; Telencephalon; Visual discrimination; Pigeon
Pigeons with lesions of the lateral part of the telencephalon, visual Wulst, and fronto-archistriatal tract were compared with sham-operated controls in 2 procedures. In one of them the time it took the pigeons to grasp and eat a certain number of grains was recorded. In the other experiment the number of grains was counted that the pigeons consumed out of a mixture of grains and pebbles within a fixed time interval. Only the pigeons with lateral telencephalic lesions were impaired. While in the first experiment the lateral ablated birds improved with time there was no recovery of performance in the second experiment.
INTRODUCTION
While it has long been accepted that normal eating in the pigeon is permanently abolished by decerebration or telencephalic ablation ~'2°the critical regions involved have not yet been identified. Salzen et al.18 found that lateral telencephalic lesions decreased the accuracy of peck localization and disrupted grasping and mandibulation in chicks feeding from a mixture of pebbles and grains. They suggested that the lateral telencephaIon might play some role in the coordination of inputs involved in eating. Eating in the pigeon involves a sequence of pecking, grasping and mandibulation that requires the precise coordination of neck, head and jaw movements. Behavioral a n a l y s e s 5"24'25 suggest that this behavior is under the sequential control of 2 different sensory systems -vision and
oral somatosensation. Pecking is elicited and guided by visual inputs and involves both the identification and localization of the food object 7. Grasping is characterized by an adjustment of gape size to object size 4'12A3 and may thus require inputs from both vision and jaw proprioception. Mandibulation, i.e. intraoral manipulation of the food object, is dependent upon somatosensory (trigeminal) feedback from the beak 22. Lesions of the lateral telencephalon in adult pigeons have been shown to produce deficits in color, intensity and pattern discrimination tasks utilizing an operant, key-pecking paradigm 6 but eating was not examined. The lesions in these studies included the lateral neostriatum (N), the lateral edge of the ventral hyperstriatum (HV), the lateral corticoid area (CDL) and the area temporo-parieto-occipitalis (TPO). This area is in receipt of inputs from both the visual and the
Correspondence: R. J~ger, Universit~it Konstanz, Sozialwissenschaftliche Fakult~it, Allgemeine Psychologie, Postfach 5560, D-7750 Konstanz, F.R.G. 0166-4328/90/$03.50 © 1990 Elsevier Science Publishers B.V. (Biomedical Division)
74 trigeminal system. The lateral part of the caudal neostriatum (NC) receives intratelencephalic visual afferents from the ectostriatal belt 17. Trigeminal inputs are relayed from the basofrontal telencephalon via the fronto-archistriate tract (FA) which terminates within a region of the caudal neostriatum (NCT). This region is a component of a trigeminal sensorimotor circuit, originating in the principal sensory trigeminal nucleus (PrV), including the nucleus basalis (N. bas), neostriatum caudale, pars trigeminale (NCT) and archistriatum (A) and terminating in jaw premotor and motor neurons 3"~9"21. Lesions of various structures in this circuit have been shown to disrupt peck localization, grasping, and food manipulation 14-22. Given this pattern of visual and trigeminal inputs, the lateral telence-
L 10
I
5
0
5
10
I
t
I
I
A4
phalon seemed an appropriate starting point tot studies designed to clarify the role oftelencephalic structures in the control of eating in the pigeon. The present study was designed to examine the effects of lateral telencephalic lesions upon the identification, localization and grasping of the food object. The deficits seen after such lesions were compared with those seen after control lesions of the Wulst and of the fronto-archistriate tract, which convey visual and trigeminal afterents, respectively. MATERIALS A N D M E T H O D S
Subjects Twenty adult pigeons (Columba livia) of unknown sex and age were housed in individual
A14
A4
CO A5
L"DI A6
Cl)t A7
1PC A8
b
A9
AIO
A11
A12 A13 AI4
q
)
) Fig. 1. Lesions of the lateral telencephalon (abbreviations, see text).
75 cages in a colony room with a 12/12-h light/dark cycle. Throughout the experiment, they were maintained at 80 ~ of their free-feeding weight by food deprivation.
Behavioral procedures (1) Ingestive efficiency. The food trough normally attached to the home cage was replaced by a transparent trough (width: 9 cm, depth: 5 cm, height: 6 cm). Ten safflower seeds (Carthamus tinctorius, average length 4 mm) were presented in the trough and pecking behavior was timed from the first peck until all grains were consumed.
(2) Discriminationoffood from non-food objects. Thirty safflower seeds and pebbles of roughly similar sizes were mixed to produce a pebble/seed mixture (volume: 30 ml) and presented in the trough. Subjects were allowed to peck for 30 s, after which the trough was removed and the number of seeds consumed was recorded. Preoperatively, subjects were trained on both tasks for 15 consecutive daily sessions and the last 10 or 5 sessions (see below) provided baseline data. The pigeons were then matched according to their baseline performance and assigned to 5 different treatment conditions (n = 4) as follows:
L
10
5
0
~
$0
I
i
I
I
f
xe
(1) ablation of the lateral telencephalon, (2) Wulst ablation, (3)transection of the tractus frontoarchistriatalis (FA), (4) control surgical procedure for the Wulst- and laterally lesioned birds, and (5) a second control surgical procedure for the FA-birds, which were tested some months later. Postoperative testing commenced after a 3-day recovery period and continued for 20 (treatment condition 1, 2, 4) or 10 (treatment condition 3, 5) consecutive daily sessions.
Surgical and h&tologicalprocedures Subjects were anesthetized with a barbiturate/chloral hydrate solution (0.5 ml/100 g body weight, i.m.15). After local applications of xylocaine they were placed in a stereotaxic apparatus, the scalp was incised along the midline and surgical procedures were carried out guided by coordinates drawn from a stereotaxic atlas 1°. All procedures were bilateral. For the lateral telencephalic ablation lines were drawn on both sides of the skull from coordinates A 6/L 7 - A 13/L 5.5. The bone was removed along that line with a dental drill, brain tissue to be removed separated with a vertical scalpel incision and aspirated through a pipette. The space was packed
AI4
A8 ~D
A9 HD
AIO HO
A11
Ha
A12 HD
A14
Fig. 2. Lesions of the visual Wulst (abbreviations, see text).
76 with gelfoam and the wound sutured. For the Wulst ablation, a quadrangular plate of bone was defined by coordinates A 14/L 1-3 and A 9/L 1-3 and removed. Wulst tissue was removed by an aspiration procedure adjusted so as not to exceed the dorsal surface of the ventral hyperstriatum. FA was sectioned electrolytically using a stainless steel electrode insulated except for a 0.5-mm tip. The needle was inserted at each of 3 overlapping locations along a medio-lateral line (A 10.5/L 6.0, L 6.5 and L 7.0), advanced until it reached the skull floor and then retracted for 0.5 ram. A lesion was placed at each location (9 mA for 15 s). The surgical control birds sustained identical treatment, except for insertion of an electrode. At the conclusion of the experiment, the animals were anesthetized, perfused intracardially with a 0.9~o saline solution (40 °C) followed by 4% formalin. After fixation for a week in 4~o formalin brains were removed, embedded in egg-yolk, hardened in formalin vapors for a week and cut at 40/~m, with every 13th section stained with cresylviolet. With the aid of a microscope, the extent of the lesions was transferred to drawings of transverse brain sections taken from the Karten and Hodos 1° atlas. RESULTS
Anatomical The ablations in the lateral telencephalic group were generally symmetrical (Fig. 1). In all birds the dorsolateral part of the neostriatum and the area temporo-parieto-occipitalis (TPO) had been aspirated. In 2 birds parts of the lateral corticoid area (CDL) had been destroyed, 2 others had minor, unilateral damage to the outermost part of ectostriatum (E) while in 2 other subjects both the lateral pole of the archistriatum (A) and FA sustained bilateral damage. The Wulst lesions (Fig. 2) varied somewhat in extent and were slightly asymmetrical, but in all cases the anterior portion of the visual Wulst had been removed. One bird sustained almost complete unilateral removal of the hyperstriatum ventrale. In 3 of the FA birds, the tract was transected bilaterally; in the 4th the damage was unilateral and its data were therefore excluded from the analysis (Fig. 3).
One sham-operated FA control bird died under anesthesia.
Behavioral A measure of ingestive efficiency for each of the groups was obtained by calculating the mean time
k 76
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67
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Fig. 3. Transsections of the frontoarchistriatal tract LPO, lobus parolfactorius; QF, tractus quintofrontalis; for further abbreviations, see text.
77 needed to ingest all ten of the seeds. Session-bysession data for this task under each of the treatment conditions are presented in Figs. 4 and 5. Analyses of variance ~l indicated no significant differences between the groups preoperatively. Postoperatively, there were no significant differences between the Wulst, sham-operated controls and FA birds. However, postoperative comparisons indicated that the lateral telencephalic group took significantly longer to ingest the seeds than the other treatment groups (lateral vs. control: FI,6 = 8.4, P < 0.05; lateral vs. Wulst: F 1 , 6 = 10.8, P < 0.05). After about 6days of testing the lateral subjects showed a highly significant recovery (first 10 sessions vs. last 10 sessions: F1.39 = 8.0, P < 0.01) and performance locked up slightly below their preoperative levels. Incidental observations of this temporary deficit of the lateral birds indicated that the birds were capable of peck localization, since many of their pecks made contact with the seeds. However, these subjects appeared to have considerable difficulties with mandibulation. Pecks result-
control o~O~-D O~ o/ ~
o
FA-lesion
0
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o
o/
control
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Fig. 5, Pre- and postoperative means of time needed to grasp 10 grains ( 0 , I , ingestive efficiency) and of numbers of grains grasped ( 0 , V-l,discrimination of food from non-food objects) by pigeons with lesions in the frontoarchistriatal tract.
ing in contacts were not followed by grasping and the seeds were scattered within the trough. Birds frequently failed to ingest even those seeds which were successfully grasped. In other cases, the
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Fig. 4. Pre- and postoperative means of time needed to grasp l0 grains by Wulst- and lateral-lesioned pigeons (ingestive efficiency).
78 control
30-
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Fig. 6. Pre- and postoperative means of numbers of grains grasped by Wulst- and lateral lesioned pigeons (discrimination of food from non-food objects).
seeds were turned around within the beak before being swallowed. While birds of the other treatment groups grasped several seeds consecutively, the lateral telencephalic subjects could grasp an additional grain only after the preceding one had been swallowed. Moreover, lateral subjects refused to eat large size seeds (maize and peas) when mixed with their normal diet. Finally, the lateral birds continued to peck at seeds they had missed, while the other subjects generally pecked at the next closest grain. An index of the birds' ability to discriminate food from non-food objects was obtained from measures of seeds and pebbles ingested in a 30-s test period and the data for each treatment group are presented in Figs. 5 and 6. While there were no preoperative differences between the groups, the lateral group ingested only about 8-10 seeds per session postoperatively, in contrast to 20-25 seeds per session for the Wulst and control groups. These differences were significant beyond the 0.01 level for both comparisons (lateral vs. Wulst: F I , 6 = 153.2, P < 0.01 ; lateral vs. control: F I , 6 = 674.2, P < 0.01). Although the number of pecks made by each group was not recorded,
incidental observations suggested that they did not differ sufficiently in this respect to account for the differences in the number of seeds ingested. Moreover, in contrast to the other subjects, the lateral telencephalic birds appeared to be ingesting an increased amount of pebbles. No improvement in the pebble-seed discrimination task was seen during the 20 postoperative sessions. DISCUSSION
Behavioral studies of the avian brain have suggested that the lateral telencephalon may play some role in the sensorimotor control of feeding TM. The area is known to receive inputs from both the visual 2'~7 and trigeminal systems 21 and there is evidence from a cyto- and myeloarchitectonic mapping s t u d y 16 that it may be involved in integrating afferents from several modalities with efferent systems. To test this hypothesis we examined the effects of lateral telencephalic ablations upon tasks designed to distinguish between different components of the pigeon's feeding response sequence. The first of these tasks required the visual localization and
79 subsequent ingestion of seeds; the second required, in addition, a discrimination between food and non-food objects (seeds vs. pebbles). None of the lesioned subjects had problems in maintaining weight or food uptake in the cage except for lateral lesioned birds, which left out larger size grains. For subjects with Wulst lesions or FA transections no significant deficit was seen in either task. However, subjects with lateral telencephalic lesions, showed significant reduction in performance on both tasks. In the first task, there was no obvious effect upon peck localization (i.e., most pecks terminated in contact with the seed), but the probability of grasping was reduced and the time taken for mandibulation was increased. Several days after surgery, however, the birds' performance rose to slightly below their preoperative level and that of the control group. These deficits are most parsimoniously interpreted as reflecting a deficit in the trigeminal sensorimotor control of ingestion though the participation of a minor localization deficit could not be excluded. Similar deficits are seen after trigeminal deafferentation23, or lesions of central trigeminal structures, including N. bas. and NCT 22. On the second task, lateral telencephalic subjects reduce their intake of seeds and increase their intake of pebbles postoperatively. In contrast to what happened with the former task the birds' performance did not recover. Although the increased intake of pebbles suggests a deficit in the oral somatosensory discrimination of food from non-food objects, this deficit only explains why an object cannot be identified as a seed or a pebble once it is grasped. It does not explain, however, the decrease in grasped (e.g. ingested) seeds, since pecking and grasping is under visual control 13. Furthermore, feeding behavior in the first task showed a significant recovery to almost preoperative level and thus one also should expect a recovery of performance in the discrimination of food from non-food objects. Therefore the permanently reduced intake of seeds in the second task reflects a visual discrimination deficit. Thus lateral telencephalic lesions produce deficits in both the manipulative and discriminative components of ingestive behavior and these deficits involve disruptions of both visual and trigeminal
processes. A remarkable recovery from the mandibulative deficit must be contrasted against the permanence of the discriminative deficit. Therefore these latter results confirm the persisting visual discrimination deficits of lateral telencephalon-ablated pigeons reported earlier6. The results of the present study thus support a role for the lateral telencephalon in the visuomotor and somatosensorimotor control of eating in the pigeon. The fact that recovery from the manipulation and visual discrimination deficits have different time-courses suggests that they have different though possibly overlapping neural substrates. It seems unlikely that the defect reflects damage to multimodal neurons. Moreover, the absence of deficits in the Wulst group suggests that pathways other than the thalamofugal system mediate the visual discrimination of food from non-food objects. The tectofugal-ectostriatal pathway seems a likely candidate. Our results also qualify earlier reports suggesting that the FA is important in transferring trigeminal information to the archistriatum 2~. FA transections in our hands failed to produce deficits in any of the tasks we used. A visual role for this tract is therefore negated. Finally, it is known that both visual and trigeminal inputs project upon the archistriatum in the pigeon 8"9'17'21. An analysis of its role in the visuomotor and somatosensorimotor control of feeding would be of considerable interest. ACKNOWLEDGEMENTS This research was supported by the Deutsche Forschungsgemeinschaft. While preparing the manuscript the author was supported by a D F G postdoctoral grant (II 0 2 - Ja 433/1-1). The assistance of Prof. J.D. Delius (Konstanz) and H.P. Zeigler (New York) who carefully revised the manuscript, and G. Keim (Bochum) and B. Bayless (New York) who did the photographic work is gratefully acknowledged. REFERENCES 1 Akerman, B., Fabricius, E., Larsson, B. and Steen, L., Observations on pigeonswithprethalamicradiolesionsin the nervous pathway from the telencephalon, Acta PhysioL Scand., 56 (1962) 286-298.
80 2 Belekhova, M.G., Subcortico-cortical relationships in birds, Neurosci. Transl., 2 (1968) 195-203. 3 Berkhoudt, H., Klein, B.G. and Zeigler, H.P., Afferents to the trigeminal and facial motor nuclei in the pigeon (Columba livia L.): central connections of jaw motoneurons, J. Comp. Neurol., 209 (1982) 301-312. 4 Deich, J., Klein, B.G. and Zeigler, H.P., Grasping in the pigeon: mechanisms of motor control, Brain Res., 337 (1985) 362-367. 5 Delius, J.D., The peck of the pigeon: free for all. In: C.F. Lowe, M. Richelle, D.E. Blackman, C.M. Bradshaw (Eds.), Behaviour Analysis and Contemporary Psychology, Erlbaum, London, 1985. 6 Delius, J.D., J~.ger, R. and Friesel, M., Lateral telencephalic lesions affect visual discriminations in pigeons, Behav. Brain Res., 11 (1984) 249-258. 7 Goodale, M.A., Visually guided pecking in the pigeon (Columba livia), Brain Behav. Evol., 22 (1983) 22-41. 8 Gfintfirkfin, O., Evidence for a third primary visual area in the telencephalon of the pigeon, Brain Res., 294 (1984) 247-254. 9 Gfintfirkfin, O., Verhaltensphysiologisehe Untersuchungen
zur funktionellen Organisation des visuellen Systems der Taube, Unpublished Dissertation, Psyehologisehes Institut der Ruhr-Universit~t Bochum, Bochum, 1984. 10 Karten, H.J. and Hodos, W., A Stereotaxic Atlas of the Brain of the Pigeon, Johns Hopkins Press, Baltimore, MD, 1967. 11 Kirk, R., Experimental Design: Procedures for the Behavioural Sciences, Brooks/Cole, Belmont, CA, 1968. 12 Klein, B.G., Deich, J.D. and Zeigler, H.P., Grasping in the pigeon (Columba livia): final common path mechanisms, Behav. Brain Res., 18 (1985) 201-213. 13 LaMon, B. and Zeigler, H.P., Grasping in the pigeon (Columba livia): stimulus control during conditioned and consumatory responses, Anim. Learn. Behav., 12 (1984) 223-231. 14 Levine, R.R. and Zeigler, H.P., Extratelencephalic pathways and feeding behavior in the pigeon (Columba livia), Brain Behav. Evol., 19 (1983) 56-92.
15 Mallin, 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. 16 Rehk~mper, G., Zilles, K. and Schleicher, A., A quantitative approach to cytoarchitectonics, X. The areal pattern of the neostriatum in the domestic pigeon (Columba #via f.d.). A cyto- and myeloarchitectonical study, Anat. Embryol., 171 (1985) 345-355. 17 Ritchie, T.L.C., lntratelencephalic Connections and their Relationship to the Archistriatum in the Pigeon (Columba livia), Thesis Ph.D., University of Virginia, Charlottesville, VA, 1979. 18 Salzen, E.A., Parker, D.M. and Williamson, A.J., A forebrain lesion preventing imprintingin domestic chicks, Exp. Brain Res., 24 (1975) 145-157. 19 Schall, U., Gfintfirkfin, O. and Delius, J.D., Sensory projections to the nucleus basalis prosencephali in the pigeon, Cell Tissue Res., 245 (1986) 539-546. 20 Thauer, R. and Peters, G., Sensibilit~it und Motorik bei lange fiberlebendenZwischen-Mittelhirntauben,Pfliiger's Arch. Ges. Physiol., 240 (1938) 503-526. 21 Wild, J.M., Arends, J.J.A. and Zeigler, H.P., Telencephalic connections of the trigeminal system in the pigeon (Columbia livia): a trigeminal sensory motor circuit, J. Comp. Neurol., 234 (1985) 441-464. 22 Zeigler, H.P. and Karten, H.J., Brain mechanisms and feeding behavior in the pigeon (Columba livia), |I. Analysis of feeding behavior deficits following lesions of quintofrontal structures, J. Comp. Neurol., 152 (1973) 83-102. 23 Zeigler, H.P., Miller, M. and Levine, R.R., Trigeminal nerve and eating in the pigeon (Columba livia): neurosensory control of the consumatory responses, J. Comp. Physiol. Psychol., 89 (1975) 854-858. 24 Zeigler, H.P., Levitt, P.W. and Levine, R.R., Eating in the pigeon (Columba livia): movement patterns, stereotypy, and stimulus control,J. Comp. Physiol. Psychol., 94 (1980) 783-794. 25 Zweers, G.A., Pecking of the pigeon (Columba livia L.), Behaviour, 81 (1982) 175-230.
