Lateral forebrain lesions affect pecking accuracy in the pigeon

Behavioural Processes, 28 (1993) 0 1993

181-I

181

88

ElsevierScience Publishers B.V. All rights reserved 0376-6357/93/$06.00

BEPROC 00453

Lateral forebrain

lesions affect pecking accuracy in the pigeon Ralf Jiger

Allgemeine

Psychologie,

UniversitSt

Konstanz,

Konstanz,

FRG

(Accepted 28 September 1992)

Abstract

Pigeons were trained to preferentially

peck the centermost element of a concentric key

array. When they had learned the task to a lateral telencephalon. The ablation caused proportionally more pecks being directed at analysis this result was interpreted as being

criterion the subjects received lesions of the an unexpected performance improvement, the central key element. However, on closer the effect of a mandibular gape control loss

rather than being due to an actual peck localization enhancement.

Key words:

Pigeon; Telencephalic

lesion; Pecking; Response localization;

Gape control

Introduction

The organization and control of pecking of birds has lately attracted increasing attention as a simple motor act controlled by neuronal structures that might be accessible to a thorough analysis (Delius, 1985; Siemann, 1992; Zeigler et al., 1980; Zweers, 1982). One of the brain regions involved in the control of pecking behavior is the lateral pole of the telencephalon, which is known to receive visual and trigeminal input (Ritchie, 1979; Wild et al., 1985). Older experiments performed with chickens indicated visual impairments after lesions of this area and showed a marked deficit in grain uptake (Salzen et al., 1975). Visual impairments

Correspondence

were confirmed

in a better-controlled

to: R. Jkiger, Allgemeine Psychologie, UniversiGt

study on pigeons demonstrating

Konstanz,

D 7750

Konstanz,

FRC.

182

the incidence of intensity, hue and shape discrimination deficits after ablations of the said forebrain region (Delius et al., 1984). Furthermore, in a recent study, it was shown that after equivalent ablations, pigeons need significantly longer than control birds to find and eat a given number of grains dispersed within a defined quantity of grit. The same birds, however, also revealed difficulties in simply grasping and eating a fixed number of easily visible grains. There was no postoperative recovery with the grain/grit discrimination but the performance on the grain-alone task improved somewhat with experience and time, though never to preoperative levels (Jager, 1991). Based on these differing recovery courses it was suggested that the lesions had separately produced both a visual and a visuomotor impairment of feeding behaviour. The first effect could be easily linked with the findings of the earlier mentioned visual deficit studies. On the other hand the precise nature of the pecking accuracy impairment was less certain. Some incidental observations, however, supported the hypothesis that it entailed a diminished ability to direct pecks at targets. The experiment we now report was thus designed to directly measure the peck location accuracy of pigeons before and after lateral forebrain lesions.

Materials

and Methods

Subjects Ten adult pigeons (Columba /ivia) of local homing stock participated in this experiment. Birds were deprived to 80% of their normal body weight and housed individually under an alternating 12-h light/dark schedule. All animals were trained to peck a horizontally mounted piezoelement for the delivery of a few grains in a trough next to it.

Apparatus The experimental chamber (34 x 34 X 34 cm) was illuminated by a shaded house light and incorporated a specially designed panel bearing a horizontally mounted compound key (Fig. 1). The key (24 mm overall diameter) consisted of four independent concentric annuli (each 2 mm wide) separated by 0.5 mm gaps and surrounding a circular center element (4 mm diameter). Each element was mounted on a spring leaf and could be activated separately. Depression of an element closed an individual electric contact. A light bulb above the key signalled the enabling of the contacts. Whenever the contact of one element was closed it caused the disabling of all key contacts and the extinction of the signal light. Mixed grain could be offered with a solenoid-operated hopper. Event sequencing and data recording was controlled by modular digital equipment.

Behavioral

procedures

Trials within the peck localization training began with the signalled enabling of the key

183

signal light for ksy

--

-

Fig. 1. Experimental chamber with food hopper, signal light, and horizontally

elements.

Initially

the

pigeons

were

hopper-rewarded

(3

s> for

key elements

mounted key elements.

pecking

any of the

key

elements. Later they were rewarded for pecks directed at the inner elements but punished with time out (house light off, 15 s> for pecks at the outermost ring element. Trials were separated by intervals (3 s) during which the house light was on but the signal light was off. As training proceeded, additional outer rings were programmed to yield punishment, the aim being to get subjects to peck the central element only. Whenever the pigeons had achieved 90% correct responses in two successive sessions they proceeded to the next constraint stage. Each of the daily sessions consisted of 50 trials. Ten final stage sessions served as a preoperative baseline and XI sessions served for postoperative assessment. Correct and incorrect responses to the various key components were counted separately. Latencies from trial onset to response were measured.

Surgery and histology On the basis of the performance during the final training stages the pigeons were divided into two matched groups, each containing five birds. The subjects of the lesion group sustained aspiration ablations of the lateral telencephalon and the control birds underwent sham surgery, all under anesthesia. The pigeons were allowed three days recovery before postoperative testing started. When testing was completed the birds were perfused intracardially, and the brains cut on a freezing microtome. The extent of the lesions was examined with a microscope and transferred onto drawings of a pigeon brain atlas (Karten and Hodos, 1967). The detailed surgical and histological procedure is described elsewhere (Delius et al., 1984).

sessions Fig.

2.

Mean

percent

pertorlndnc-e

of

and

experimentdl

dnd

postoperative

control

5e~sions

(C)p:

bircls

in

precJperdtive

bdseline

sesbions

Surgery).

Results

Behavioral

d&a

PigecJib

birds Iwo

I.lt-&wwt

successive

key. The first

sessions

remaining

surrounding

that in several tJhe spring

st’SSi(Jns

demanding

eight birds

instances

90%

only

hut all

~~~cd~izd~iOl1trdiiling.

peck

but without

or more

managed withotut

the key elements,

baseline

birds.

matched

control

sessions

Perfot-mance

were

during

and experimental

I>aiiy pre- dnd postoperative

percentages The

Of

responses

/~iOWeVc’r,

ever meeting on the center

to reach the penultimate

ever achieving particularly

h\YJ

element

of

of Ihe

stage (center

the criterion.

the center

(mly

the criterion

and

It was remarkable

element,

wete

ripped

ofi

leabe mountings.

Preoperative

65%

60

the final stage of training

element)

ittdividual way.

dtJ()llt

tnanaged to enter

of the groups

preoperative

correct

(Fig.

of both groups the

dnd redched a level of 75-850/;,

In contrast,

the control subjects.

birds eventually Andlysis

stage reached

to divide sessions

POskJperdtiVe

of cWrect

provetnent

experimental

served responses

were

the subjects

were

run

by the into the

in the sdme

transformed

into mean

2).

Postoperatively

of dbout 7O’i/oc,orrec‘t responses,

run at the lerminal

sesGot)s

groups. scores

performance

responses.

necessarily these

but still (its

pige(JIX

c,orrect responses

showed

a delayed

exhibited

varidn(.e

cut pigeons

lesiotled

(Kit-k,

oscillated showed within

1’368)

45%

and

an immedidte

in)-

the first

improvement

a greater variability

between

three sessions.

to an dverage level in performance

of the lot-dlizdtitrn

scores

than

revedkd

185

Fig. 3. Diagrams of the lateral telencephalic lesions in the experimental group (for abbreviations

see

text).

no preoperative difference between experiments and controls (F(1/8) = 0.02; P > O.OS>, while postoperatively the differences were significant (F(1/8) = 6.22; P < 0.05). Analyses of variance of the latency data did not reveal any significant differences between the groups.

Anatomy The lateral parts of the neostriatum (N), the lateral corticoid area (CDL), the area temporo-parieto occipitalis (TPO), and the frontolateral edge of the ventral hyperstriatum (HV) were removed bilaterally in all birds (Fig. 3). In four birds, lesions of the left hemisphere were slightly larger than that of the right hemisphere including the outermost lateral pole of the ectostriatum (E). Four birds showed unilateral damage of the tractus dorsoarchistriatalis (DA). One bird had bilateral damage to this tract. In three birds, the outermost edge of the paleostriatum augmentatum (PA) was removed unilaterally. The tractus frontoarchistriatalis (FA) was damaged bilaterally in four pigeons and unilaterally in one pigeon.

Discussion Pecking for food requires accurate coordination of head, neck and beak movements in order to achieve a precise on-target peck localization (Zeigler et al., 1980; Zweers, 1982). Pigeons (and chickens: Salzen et al., 1975) with lateral telencephalic lesions show

186

decreased interpreted

efficiency in the ingestion as reflecting a visuomotor

of easily detectable grains. This has been tentatively deficit affecting peck localization (Jager, 1991). The

present experiment represented an attempt to verify this hypothesis. The expectation was that lateral forebrain lesioned birds would have more difficulties in exclusively directing pecks at a small operant target than control birds. However, the actual results were surprising. The first observation was that, although birds quickly learned to peck keys, generally they had considerable difficulties in concentrating their pecks exclusively on the central elements. Only two birds were partially successful in restricting their pecks to the middle 4 mm diameter disc element, the other eight only managing to partly focus them on a 6.5 mm diameter area. This relatively poor accuracy did not improve with extended training. Pigeons are known to be able to successfully target more than 90% of their pecks at seeds markedly smaller than 4 mm in normal foraging situations (Zeigler et al., 19X), but also when pecking small features displayed on operant targets they manage far better localization performances than those achieved in the present experiment (Jenkins and Sainsbury, 1970). Even more remarkable, however, was the finding that after surgery the lateral telencephalon lesioned subjects showed both a rapid and significant increase in the proportion of pecks exclusively localized on the center element as well as a less variable performance by the sham operated birds. Both the preoperative failure in acquiring the localization task and the apparent improvement shown by the lesioned subjects can be simply accounted for by considering certain features of the pecking response topography. Food-reinforced operant pecks are similar in their dynamic geometry to ingestive pecks (Jenkins and Moore, 1973). Both kinds of pecks include a grasping component involving the opening of the mandibles into a gape with approximately the size of food items serving as reinforcers (LaMon and Zeigler, 1984). Pigeons may, however, also adjust gape amplitude (Schall and Delius, 1991). The key elements used in partially smaller than the grains offered as reward. suggests that the pigeons were attempting to grasp

with respect to salient key features the present experiment were of sizes The key ripping that was observed the key components, including the

center disc. The resulting gape was presumably sufficiently large to cause frequent contact of one or the other mandible tip with key elements adjacent to the intended target and thus interfered with our requirements for peck localization, Attempts to condition animals to emit responses that interfere with their natural habits often result in learning failures (Breland and Breland, 1961). Our subjects were expected to learn to produce operant pecks with a necessarily almost closed beak, a response that can be assumed incompatible with the response normal for the context. This would explain the problems the birds had with fulfilling the criteria set by the experimenter. This account is completed by supposing that the enhancement after ablation does not reflect a genuine visuomotor improvement in peck targeting. Rather the lateral telencephalic lesions are assumed to cause a disturbance in the gape size adjustment mechanism. Indeed these lesions impinge upon a region in the caudal neostriatum which has been shown to be a component of a trigeminal sensorimotor circuit (Wild et al., 1985). Birds with lesions in the motoric end of this circuit have been reported to have gape adjustment problems (Levine and Zeigler, 1983). Pigeons with lateral telencephalic lesions have been found to often leave behind the larger sized grains of their normal forage mixture (lager, 1991). In concluding, the results are very clearly localization

accuracy

is disrupted

by lateral

in contradiction telencephalic

with the hypothesis lesions (JBger, 1991).

that peck Recent

187

evidence

indicates that this component

of the peck control mechanism

is not part of the

pigeon’s telencephalon C&iger et al., 1992). The most likely explanation for the deficits that these lesions cause with the uptake of easily visible large grains is that the preparation of grasping with an adequate gape adjustment is impaired by the disturbance of a component of the somatomotor control of pecking. Nevertheless the apparent improvement in the targeting of a motor act after a lesion is a remarkable finding.

Acknowledgments This research was supported by the Deutsche Forschungsgemeinschaft, including a postdoctoral grant to the author. I am grateful to Profs. J.D. Delius (Konstanz) and H.P. Zeigler (New York) for carefully revising the manuscript, S. Wagner (Bochum) for technical assistance, and G. Keim (Bochum)

and B. Bayless (New York) for photographic work.

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