Visual Neuroscience (1992), 9, 225-233. Printed in the USA. Copyright © 1992 Cambridge University Press 0952-5238/92 $5.00 + .00

Visual-discrimination deficits after lesions of the centrifugal visual system in pigeons {Columba livia)

UWE HAHMANN AND ONUR GUNTURKUN Allgemeine Psychologie, Universitat Konstanz, Konstanz, Germany (RECEIVED September 30, 1991; ACCEPTED January 6, 1992)

Abstract The effects of bilateral lesions of the centrifugal visual system (CVS) on the visual-discrimination capacity were studied in pigeons. Three different behavioral experiments, each testing different aspects of visual analysis, were performed. In the first two experiments, a grain-grit discrimination task and a visual-acuity determination, stimuli were presented in the frontal binocular visual field. A third experiment investigated the early detection of slow moving objects, introduced into the monocular lateral visual field. After bilateral lesions in the nucleus isthmo-opticus (ION) and in the ectopic nucleus isthmo-opticus (EION), a multiple linear regression analysis was employed to correlate the postoperative performance in all three tasks with the amount of structure loss within ION and EION. Deficits in the grain-grit discrimination procedure were a function of the ION lesion extent and did not depend on EION damage. Thus, these two structures could be functionally differentiated for the first time. Neither the ION nor the EION seems to be involved in visualacuity performance or the early detection of large shadows moving forward through the visual field. Our data support the hypothesis that the CVS is involved in pecking and food selection among static stimuli at a short viewing distance in ground-feeding birds such as pigeons and chickens. Keywords: Isthmo-optic nucleus, Ectopic neurons, Retina, Visual acuity, Grain-grit discrimination, Stimulus detection latency

Introduction Centrifugal visual systems (CVS) have been described in all classes of vertebrates (Reperant et al., 1989), but most studies on the efferent innervation of the retina were performed in just two ground-feeding species, the pigeon and the chick. The CVS of these birds originate in two different mesencephalic cell groups. One of them is the isthmo-optic nucleus (ION), a folded bilaminate structure in the dorsolateral part of the midbrain tegmentum (Clarke & Cowan, 1976; Weidner et al., 1987; Giinturkiin, 1987; Woodson et al., 1991). The other is the nucleus of the ectopic isthmo-optic neurons (EION), a loosely scattered array of cells with reticular appearance surrounding the ION (Hayes & Webster, 1981; O'Leary & Cowan, 1982; WolfOberhollenzer, 1987). Both structures are part of a closed loop consisting of a projection from the retinal ganglion cells to the contralateral tectum, the efferents of which in turn project both to the ipsilateral ION and EION, whence back projections lead to the contralateral retina (McGill et al., 1966a,b; Holden & Powell, 1972; Crossland & Hughes, 1978). These projections are topographically organized with respect to the ION and probably also the EION (Catsicas et al., 1987a). However, both seem to innervate only the horizontal and ventral retina representing the upper half of the visual field (Hayes & Holden, 1983; CatReprint requests to: Uwe Hahmann, Allgemeine Psychologie, Universitat Konstanz, 7750-Konstanz, Germany. 225

sicas et al., 1987a). Recent experiments suggest that the ectopic cells are not the result of a misguidance of centrifugal neurons during ontogeny of the alar plate (Clarke & Cowan, 1976), but represent an independent neuronal cell group with regard to their resistance to intraocular kainic-acid injections and the morphology of their retinal endings (Catsicas & Clarke, 1987; Fritzsch et al., 1990). Electrophysiological data are only available for the ION. Miles (1972a) and Holden and Powell (1972) demonstrated that a large number of ION units show a preference for target movements in the anterior visual field and habituate rapidly to repetitive stimulation, indicating a role in the analysis of transient and dynamic features of the visual environment. Miles (19726) additionally demonstrated an effect of ION stimulation on the disinhibition of retinal ganglion cell surrounds and activation of ganglion cell centers. This would indicate a role in the modulation of local contrast and luminance sensitivities. Most ION cells have their receptive fields in the inferior anterior visual field and are thus related to the upper posterior parts of the retina, where paradoxically ION terminals are virtually absent (Holden & Powell, 1972; Hayes & Holden, 1983; Catsicas et al., 1987a). Authors have until now been unable to differentiate between lesions of the ION and EION in their behavioral studies. Hodos and Karten (1974), Jarvis (1974), Shortess and Klose (1977), and Knipling (1978) observed only mild or no deficits in visual intensity and pattern-discrimination experiments after bilateral

226 CVS lesions. Thus, it was suggested that the centrifugal visual system only plays a minor, supplementary role in visual analysis. However, using a different approach Rogers and Miles (1972) demonstrated profound deficits in the detection of suddenly occurring moving stimuli and the perception of grain on the black squares of a checkerboard. These authors suggested that the centrifugal system may play a role in detecting moving objects and in enhancing contrast under dim light conditions through a mechanism of dynamic adaption at the retinal level. This hypothesis largely coincides with the suggestion of Weidner et al. (1987) that the CVS is involved in pecking and visual food selection among static stimuli at a short viewing distance. Their conclusion was based on a comparative neuroanatomical study in different species of birds which evinced important differences between raptors and ground-feeding birds. In galliformes, passeriformes, and columbiformes, which are mostly seed or fruit-eating, the ION was always very well differentiated and laminated, containing 7000-12,000 neurons. In all raptors examined, the ION was poorly differentiated and reticular in appearance, with only 900-1400 cells. Holden (1990) extends the interpretation of Weidner et al. (1987) and assumes that the hypertrophy of CVS in ground-feeding birds is a result of its importance in predator detection (by its terminals in the horizontal and ventral retina) while playing a role in food selection (by its receptive fields in the lower visual field). This short overview demonstrates that the functional analysis of CVS in birds is only beginning. Any additional behavioral study has to deal with three major concerns. First, postoperative deficits of visual performance have to be assessed differently with respect to ION and EION. Second, all experiments performed have to separately test both the lateral horizontal and the frontal lower visual fields. Third, to cope with the multitude of functions attributed to the CVS, different behavioral experiments, each testing a different aspect of visual analysis, have to be performed with each animal. Within this approach negative findings can be as important as positive ones. The present study is an attempt to specify the possibly different behavioral functions of ION and EION by correlating preoperative vs. postoperative visual-performance attenuations in three different tasks with the amount of structure loss in both midbrain structures of pigeons.

Methods

Subjects Seven naive adult homing pigeons (Columba livia) of local origin and unknown sex were used. The birds were maintained at 80% of their free-feeding weights during the experiments, with water always available in the home cages. One week before the start of the behavioral experiments the birds were anesthetized (Giinturkun & Remy, 1990), and shock electrodes were implanted under both scapulae and connected to a miniature socket on the back of the animals. These electrodes were used when the conditioned suppression technique (Smith, 1970) was employed during a stimulus-detection experiment (see below). Additionally the scalp was incised along the midline, and a small metal head block with a tapped hole was glued to the skull with dental cement. Opaque hemispherical eye caps could be fixed to these blocks during monocular discrimination sessions.

U. Hahmann and O. Giintiirkun Abbreviations B CVS DIV EDI

EION FLM GGI ION L L% LoC nIV R /?% VAI Wla

binocular seeing condition centrifugal visual system decussatio nervi trochlearis early detection index ectopic isthmo-optic nucleus fasciculus longitudinalis medialis grain-grit index isthmo-optic nucleus left-eye seeing condition percentages of tissue destroyed in the left hemisphere locus cerulus nucleus nervi trochlearis right-eye seeing condition percentages of tissue destroyed in the right hemisphere visual acuity index weighted index of the combined damage in the left and right hemispheres

In three cases the head blocks had to be replaced during the experiments by rings of velcro, fixed around the eyes with a nonirritating glue. Eye caps could be stuck onto these velcro rings. Grain-grit discrimination (experiment 1) The visual-discrimination procedure was similar to that used by Jager (1990) and Giinturkiin and Kesch (1987). The pigeons had to discriminate common vetch (Vicia sativa) grains of approximately 4 x 3-mm axial length from small grit particles of varying size. Thirty grains were mixed with 30 g of grit (about 1000 in number) in a wooden tray of 9.5 x 6.5 x 5.7 cm with a transparent observation window at the front. The pigeons remained in their home cages and could peck at the grain/grit mixture when the tray was inserted under an opening of 6 x 10 cm in the front panel of the cage. The tray was removed 30 s after the first peck, and, by counting the remaining grains, the number of grains swallowed was calculated. In addition, the number of pecks by the animals during the 30-s testing procedure was counted by the experimenter. The pigeons were familiarized with the procedure within ten training sessions before the experimental data were recorded for subsequent analysis. The animals were then tested under binocular or, by means of eye caps, left or right monocular conditions. Each pigeon completed 30 sessions; that is 10 sessions under each condition. Ordering of binocular and the two monocular conditions was balanced across animals in all experiments during the study. The data from the first 30 sessions served as a base line for each of the three conditions. On each day two sessions were conducted. For each session four measures of the pigeons' performance were assessed: (1) the number of grains eaten; (2) the quantity of swallowed grit measured by weighing the grit after each session; (3) the number of pecks, as an index of the activity level of the animal; and (4) the percentage of pecks leading to swallowing of grain, which gives a measure for the discrimination performance of the animal. This percentage was calculated as being the number of grains eaten multiplied by 100 and divided by the number of pecks. After bilateral coagulation lesions of ION and EION, the animals were allowed to recover for 1 week before they were tested postoperatively under the same conditions as described above. The data were compared with the base line results for each viewing condition and each pigeon individually.

A lesion study on the pigeon's centrifugal visual system Visual acuity (experiment 2) The pigeons were trained and tested in a two-key operantconditioning apparatus illuminated by a shielded houselight. The overall chamber illumination was 41.8 Ix. The ceiling luminance varied from 309.4 cd/m 2 directly below the lamp to 6.8 cd/m 2 in the darkest corner. Experimental events were controlled and registered by conventional solid-state control equipment (Coulbourn Instruments, Lehigh Valley, PA). One sidewall of the pigeon chamber was modified to permit back projection of stimuli onto the two circular 25-mm-diameter Plexiglas pecking keys with an external 35-mm slide projector (Kodak Modal Carousel S-AV 1000, Stuttgart, Germany). The positive stimuli were gratings ranging in spatial frequency on the keys from 1.6 to 25.9 lines/mm (1.6, 3.3, 8.3, 12.5, 18.7,20.8, and 25.9 lines/mm) made from photographic negatives of commercial grating patterns (Letraset, Frankfurt, Germany). Black and white line widths were equal. The contrast of the stimuli [calculated as (/ max - / m i n / / m a s + / min )] ranged from 75% for the 1.6 lines/mm stimuli to 35% for the 25.9 lines/mm stimuli. The negative stimulus was a uniform light grey surface produced by defocused photographs of the same grating patterns. Positive and negative stimuli were photographed on the same roll of film (Agfa-Ortho, 25 ASA, Leverkusen, Germany) and developed in the same bath to achieve identical black coloring. During the experiment, positive and negative patterns were projected onto the two pecking keys. Luminance of the stimulus ranged from 2.68 log cd/m 2 for the finest gratings to 3.29 log cd/m 2 for the coarsest gratings (Table 1). Microscope cover glasses were added to either one of the two stimuli to match the average luminance within each stimulus pair. Differences, as measured with a Labosix Model 2000 S photometer, within pairs, ranged from 0.004 to 0.034 log units (Table 1). The average luminance difference between stimulus pairs was 0.014 log units. The brighter stimulus was the blank or the grating stimulus in half of the pairings. After an autoshaping procedure that established key pecking, an instrumental simultaneous discrimination procedure with correction trials was performed. The acquisition phase started with 16 trials of the 1.6 lines/mm pattern paired with the matched negative stimulus. A single peck on the grating stimulus resulted in 2-s grain delivery and additionally illuminated the feeder light within the chamber. Then a new stimulus pair was presented. The left-right position of stimuli was changed pseudorandomly (Gellermann, 1933). A peck on the negative stimulus resulted in a 10-s time-out period, during which chamber and key lights were inoperative and after which the same

Table 1. Summary of stimulus luminances and within-pair luminance differences Luminance (log cd/m2)

Grating frequency (lines/mm) on pecking key

Grating stimuli

Blank stimuli

Within-pair luminance difference (log cd/m2)

1.6 3.3 8.3

3.236-3.298 3.090-3.215 2.686-2.789

3.220-3.298 3.084-3.224 2.668-2.785

0.004-0.031 0.006-0.034 0.006-0.024

227 stimulus pair was presented again. Correction trials were repeated until a correct response was made. These additional correction trials were not counted. After reaching 85% correct responses in a single session, the next set with higher spatial frequencies was used. This procedure was continued until the performance of the animals dropped to chance level without improvement within 12 sessions. With our procedure, pigeons discriminated spatial frequencies of 12.5-25.9 lines/mm at chance level. We therefore only used the 1.6, 3.3, and 8.3 lines/mm gratings. During experimental tests 32 instead of 16 stimuli pairs were presented per session. Three sessions were performed daily. Animals were tested on alternate sessions seeing with both eyes or with sight restricted to the left or the right eye by means of eye caps. Four grating stimuli of each category (1.6, 3.3, and 8.3 lines/mm) matched with the negative stimuli were presented in the following order: 1.6, 3.3, 8.3, 1.6, 3.3, 8.3, 1.6, and 1.6 lines/mm. This arrangement was necessary because the preliminary visual-acuity task had shown that the motivation of the birds attenuated during discrimination of the high-frequency gratings. The last eight stimuli pairs with 1.6 lines/mm each were not taken into account. A psychometric function was calculated for each session and each bird. The spatial frequency at which performance was at 75% correct was regarded as threshold. Testing was continued until the daily visual-acuity thresholds of 12 consecutive sessions did not exceed ±15% of the mean threshold of these sessions. To estimate the final visual acuity of the pigeons, two birds were videotaped during the discrimination procedure and the distance from the surface of gratings to the pupil nodal point was measured from the monitor screen. For this operation the standard chamber door was substituted by a clear sheet of Plexiglas. The mean target viewing distance was estimated to be 58.0 mm. Early detection of moving objects in the lateral visual field (experiment 3) The pigeons were trained and tested in an experimental chamber with a single pecking key. This key was transilluminated by white light behind the pecking key. The key luminance was 128.4 cd/m 2 . One sidewall of the chamber was replaced by transparent acrylic covered with waxed tissue paper. A black cardboard square (30 x 30 mm) circling around an axle with a constant velocity of 14 cm/s served as a moving shape. A bulb at the center of this arrangement caused the cardboard to cast a moving shadow of 35 x 35 mm on the translucent sidewall of the box. The average luminance of that wall varied from 41.1 cd/m 2 along the upper edge to 3.4 cd/m 2 in the darkest corner. The square could either move horizontally along the upper edge of that wall, so that a shadow was visible from inside, or along an oblique orbit so that it was invisible to the pigeon inside the box. The density of the shadow; i.e. its average contrast with the surround [calculated as (/max - Imin/Imax + / min )] was 90.3%. The rotation axle was usually in its oblique position, but regularly (on average once every 20 min) it was tilted to the horizontal position by a solenoid so that the shadow was cast onto the sidewall of the chamber. Stimulus onsets and offsets were registered by two small photoelectric cells fixed on the two side edges of the sidewall and recorded with a penrecorder (Watanabe, Ettlinger, Germany), which also registered all pecking re-

U. Hahmann and O. Gunturkun

228 sponses. Shadow projection was always from posterior to anterior with regard to the animal, assuming that it faced the key, and could either be presented to the left or the right eye by simply relocating the translucent sidewall of the chamber. A loudspeaker producing 70 dB white noise was installed in the other sidewall of the chamber to mask acoustic signals from the solid-state equipment. The size of the stimulus was adjusted to the ecological conditions of pigeons of central European breeds. According to Gensbol (1986) 14 species of birds of prey hunt for pigeons in this area. Ten of them usually attack their prey from close by using bushes and small trees as hideouts. These animals are often visible when less than 10 m away and would thus create on the pigeon's retina an image of about the size of the stimulus used. Only the remaining four species, most of them endangered, circle in large distances above ground and are thus only visible as small spots on the sky. The animals were conditioned to peck at a variable ratio of 50:1 for 3-s food access. This resulted in a high and stable response rate of 2-3 pecks/s. Then, the early detection acquisition phase started. While the pigeons pecked onto the illuminated key, the shadow suddenly appeared on the translucent pane. The stimulus offset was followed immediately by a weak electric shock applied through the scapulae electrodes (1 mA, 100 ms). The concomitant interruption of the pecking responses generally lasted for only a few seconds. After a few pairings of shadow and shock, the pigeons interrupted pecking responses as soon as they saw the shadow. The time difference between stimulus onset and the interruption of pecking responses was measured using the traces of the penrecorder and was defined as the early-detection latency. After initial acquisition, only every second shadow projection was accompanied by shock. One session was performed daily alternating between left and right monocular viewing tests. The data without electric shock trial of eight consecutive sessions were used to calculate the preoperative performance of each animal and each eye.

Surgery and histology After reaching criterion in all experiments, the pigeons were anesthetized, their heads were placed in a stereotaxic holder, the skin over the skull was incised, and a small portion of the skull was removed with a dental burr. Bilateral electrocoagulation lesions were made with an insulated insect pin electrode of 0.3mm diameter at the coordinates A 1.50 to A 2.00 (Karten & Hodos, 1967) with a current of 25 mA and duration of 10 s. According to pilot experiments, this procedure minimized damage to surrounding tissue while completely lesioning the ION and EION area. Then, the skin was pulled back and the wound was closed with a few stitches. One week of postoperative recovery was allowed before the experiments were continued. After postoperative testing was completed, the pigeons were anesthetized and perfused through the left ventricle with 0.9% NaCl (40°C) followed by 4% formaldehyde (4°C). The brains were removed from the skulls, postfixed in a mixture of 6% formaldehyde and 30% sucrose dissolved in 1.2 M phosphate buffer for 48 h, and cut at 40 nm in a frontal plane on a cryotome. Every second section was counterstained with cresyl violet. The sections were dehydrated and coverslipped. The location and extent of the lesion were reconstructed from these sections. Lesion studies generally correlate postlesional structure volume losses of all structures involved with an index for preop-

erative to postoperative performance decrement (e.g. Hodos et al., 1984). A significant correlation between lesion extent of a given brain structure and a performance attenuation thus indicates a relationship which is independent of unspecific surgery effects. For this procedure, it is assumed that the cell density of a given structure is roughly even within its volume. Although this was possible for ION, it could not be applied to EION, whose caudal and frontal poles occupy large volumes with very low cell densities. Therefore the retrograde fluorescent tracer Fast Blue (25 jtl, 2% in distilled water) was injected into the vitreous humor of two pigeons not used during the behavioral study. From histological sections the backlabeled EION neurons were counted for each stereotaxic frontal plane at 0.25-mm intervals from A 1.25 to A 2.50. These counts were corrected according to the correction formula of Floderus (1944). These corrected numbers were used to calculate the density of EION neurons per plane, giving a weighting factor for each of these stereotaxic planes. The lesion-dependent volume loss for each plane could now be multiplied with its particular factor giving an estimate of the actual number of EION cells destroyed by the lesion. Thus, the percentage of damage to ION and to EION could be obtained for each animal and each hemisphere. These numbers could be correlated with the performance deficit with the contralateral eye. Results from the binocular condition were correlated with a weighted bilateral damage index (Hodos & Bobko, 1984). Left- and right-sided lesions had on the average the same size.

Results Anatomical

results

In most of the seven animals used in the present study, the lesions were restricted to the expected location and extent (Fig. 1). One pigeon (No. 4) evinced slightly dorsally displaced coagulations so that latero-ventral cerebellar areas were also involved. In four animals (Nos. 1, 2, 5, and 7), the trochlear nucleus medial to EION was partly damaged; on average, 18% on the left and 11% on the right. There was no relation of trochlear lesion size to postoperative performance. This is illustrated by animal No. 1 which had the largest trochlear lesion of all subjects (55%, right side) but had only very mild postoperative impairments with the contralateral eye. Lesion extents ranged from 38.3 to 100% for the ION and 15.2 to 9 1 % for EION. Table 2 indicates for each animal the percentage of tissue destroyed in the left (Z.%) and right (/?%) side as well as a weighted index for the bilateral damage (W°to), which is the product of Z.% and R% divided by 100 (Hodos & Bobko, 1984). W% ranges from 3.6 to 100%. Since ION is completely surrounded by EION, lesion volumes of both structures correlated significantly with r = 0.84 (F 1/12 = 28.487, P < 0.001). Thus, it was not possible to statistically analyze effects of lesions in each of these structures independently. We therefore had to perform a multiple linear-regression analysis for each task. Grain-grit discrimination (experiment 1) None of the animals exhibited obvious postoperative motor disturbances that could have affected grain-grit discrimination performance. Nevertheless, discrimination accuracies (DA), calculated as outlined in the Methods section, were considerably

A lesion study on the pigeon's centrifugal visual system

229

Fig. 1. Cresyl-violet-stained frontal sections which correspond to plane A 2.00 of the Karten and Hodos pigeon brain atlas (1967). The broken lines indicate the border of the smallest (A, animal No. 4) and the largest (B, animal No. 1) electrocoagulation lesions of ION and EION. The lesion in A is medial to ION and involves parts of EION. The lesion in B involves ION, EION, and the medially situated n IV. D IV: decussatio nervi trochlearis; FLM: fasciculus longitudinalis medialis; ION: nucleus isthmo-opticus; LoC: locus cerulus; and n IV: nucleus nervi trochlearis. Scale bars = 1 mm.

B

affected with the exception of one animal (No. 4). To correlate performance attenuation with structural damage, the grain-gritindex (GGI) was calculated as (DApostop

- DApreop/DAposU>?

+

DApreop). A negative index indicates that the discrimination performance had decreased postoperatively. Table 2 presents GGI values for each viewing condition and each pigeon. With the exception of pigeon No. 4, all subjects displayed significantly lower postoperative accuracy under each viewing condition. A multiple linear-regression analysis was performed with

GGI as the dependent variable and the volume losses of ION and EION, as well as their interactions, as predictive factors. The regression model fitted the grain-grit index data to a highly significant degree (F= 34.18, P < 0.0001, R2 = 0.851). That this deficit was due to an attenuation of discrimination capacity is also indicated by a 49% higher number of postoperatively consumed grit particles, while the number of postoperatively emitted pecks was virtually unchanged. ION lesion size was the only significant factor (F = 19.31, P< 0.001), whereas neither

U. Hahmann and O. Guntiirkun

230 Table 2. Summary of lesion reconstruction and efficiency indices of all experimental animals Lesion reconstructions

1 2 3 4 5 6 7

38.4 100.0 99.2 39.5 100.0 100.0 57.7

Total lesion volume (mm3)

EION

ION Subject no.

Efficiency indices

VAl

CGI

EDI

/?%

Win

L%

/?%

W%

Left

Right

L

R

B

L

R

B

L

R

38.4 100.0 100.0 38.3 91.0 69.1 46.6

14.7 100.0 99.2 15.1 91.0 69.1 26.9

37.9 76.8 78.9 15.2 90.8 53.5 35.1

48.2 69.1 90.1 23.5 56.4 27.0 31.5

18.3 53.0 71.1 3.6 51.2 14.5 11.1

0.73 1.07 1.17 0.36 0.99 0.55 0.42

0.56 1.24 1.16 0.25 1.34 0.89 0.46

-0.27 -0.88 -0.73 +0.06 -0.12 -0.56 -0.29

-0.31 -0.86 -0.60 +0.14 -0.81 -0.89 -0.22

-0.26 -0.85 -0.54 +0.16 -0.77 -0.85 -0.29

-0.06 -0.30

+0.24 -0.39 -0.47 -0.02 -0.49 +0.05 -0.20

+0.03 -0.06 -0.12 -0.18 -0.26 +0.15 -0.25

+0.15 +0.10 -0.17 +0.16 +0.71 +0.73 -0.28

-0.06 +0.63

a

-0.11 -0.21 +0.14 -0.03

a

-0.24 +0.67 -0.76 +0.24

"Data were not available; GGI: grain-grit index, VAI: visual-acuity index, EDI: early-detection index.

the EION lesions (F= 1.15, P = 0.30) nor the combination of both lesions (F = 0.00, P = 0.96) showed a significant influence. Fig. 2 is a summary illustration of the correlation between the individual GGI means and the amount of ION and EION structure loss for each pigeon. The figure indicates that the magnitude of the visual deficits was a function only of the ION lesion extent and did not depend on EION damage.

Visual acuity (experiment 2) Visual acuity (VA) decreased moderately after surgery. Table 3 presents the preoperative and postoperative visual-acuity performance at threshold for each subject and each viewing condition. To correlate this decline with structure damage, the visual acuity index (VAI) was calculated as (K4 p o s l o p — / + ^preop) f o r each bird and viewing condi-

ION

80

80

100%

EION

Table 3. Preoperative and postoperative visual-acuity threshold expressed in cycles per degree for each animal and each viewing condition Postoperative

Preoperative Subject

no.

B

L

R

B

L

R

1 2 3 4

5.16 5.16 4.66 7.09 3.44 4.25 4.55

2.23 3.44

2.23 7.14 3.14 2.53 5.77 4.86 5.16

5.46 4.55 3.54 4.75 1.82 5.87 2.53

1.92 1.62

3.95 2.53 0.81 2.43 1.62 5.46 3.24

5 6 7

a

5.77 1.52 1.11 1.32

a

4.55 0.81 1.62 1.22

a Data were not available; B: binocular, L: monocular left, R: monocular right.

Fig. 2. Correlation between the grain-grit discrimination indices (GGI) for each pigeon plus viewing condition and the structure loss within the ION and EION. Positive index values indicate an increase in the postoperative discrimination performance; negative values indicate a decrease. The multiple linear-regression analysis revealed a significant correlation between the GGI and the lesion size of ION (P < 0.001). Neither the EION lesion nor the combination of both lesions displayed any significant influence in the grain-grit discrimination task.

A lesion study on the pigeon's centrifugal visual system

231

Fig. 3. Correlation between the visual-acuity indices ( VAI) for each pigeon plus viewing condition and the extent of ION and EION damage in all subjects. Positive index values indicate an increase in the postoperative visual-acuity performance; negative values indicate a decrease. The multiple linear-regression analysis revealed no significant correlation between the K4/and the extent of damage within the ION, EION, and the combination of both.

20 40

ION

so 80 100%

80

EION

tion (Table 2). Negative indices indicate decreased postoperative spatial resolution. This was the case in all animals, except two that showed an increased spatial resolution (Nos. 1 and 6). Since pigeon No. 3 did not reach the preoperative spatialresolution criterion of 75% correct, the threshold corresponding to 60% was instead determined for this subject. A multiple linear-regression analysis was performed with VAI as the dependent variable and the volume losses of ION and EION, as well as their interactions as predictive factors. Although the regression model significantly fitted the data (F = 5.39, P < 0.01, R2 = 0.488), neither ION (F = 0.07, P = 0.80) or EION {F = 0.04, P = 0.84) nor combined ION and EION lesion values ( F = 1.77, P = 0.20) showed any significant effect on spatialresolution decrements of the pigeons. Fig. 3 presents the correlation between the VAI values and the extent of ION and EION damages in all pigeons. Thus, neither of these structures determines visual-acuity performance.

Early detection of moving objects in the lateral visual field (experiment 3) To assess changes in the moving-shadow detection, an early detection index (EDI) was calculated as (EDposlop ~ EDprtop/ EDposxop + EDpreop) for each bird and both monocular conditions (Table 2). Pigeon No. 3 only reached the required stable pecking rate after surgery in the left viewing condition. None of the birds displayed postoperatively consistent early-detection changes; their response latency either increased or decreased irrespective of lesion size. Consequently, the multiple linearregression analysis did not significantly fit the data values (F = 1.61, P = 0.25, R2 = 0.326) and the regression analysis revealed no significant correlation between EDI and lesion size of ION (F = 0.11, P = 0.75), EION (F = 0.08, P = 0.78), or the combination of both structures (F = 1.39, P = 0.27). Fig. 4 summarizes the results graphically. Thus, neither ION nor

80

EION

100%

Fig. 4. Correlation between the early detection indices (EDI) for each pigeon plus both monocular viewing conditions and the extent of ION and EION damage in all subjects. Positive index values indicate shorter response latencies in the postoperative earlydetection response; negative index values indicate longer latencies in the postoperative early-detection response. The multiple linear-regression analysis revealed no significant correlation between the EDI and the lesion size of the ION, EION, or the combination of both. The "%" axes were inverted since otherwise the plane of the linear regression would have been obscured.

U. Hahmann and O. Giinturkun

232 EION seems to be involved in the early detection of moving stimuli, at least with the method employed here.

Discussion The results of the present study clearly demonstrate task-specific performance attenuations after lesions of the centrifugal visual system. The fact that only ION, and not EION damage, correlated with a postoperative decline in the grain-grit discrimination procedure makes it additionally likely that these two CVS components subserve different functions. This assumption is supported by recent anatomical studies demonstrating different modes of intraretinal termination of ION and EION (Catsicas et al., 1987a; Fritzsch et al., 1990). Weidner et al. (1987) suggested that the ION is part of a neuronal circuit dealing with the special demands of ground-feeding birds. The grain-grit discrimination procedure used in the present study resembles closely the natural feeding situation with which wild pigeons are usually confronted, and the deficits in this task after ION lesions support the hypothesis of Weidner et al. (1987). Our results are also in accordance with the results of a similar task employed by Rogers and Miles (1972). During the grain-grit discrimination experiment as used in the present study, the animals had to search for a standard type of grain against an extremely noisy background consisting of a mosaic of contrast variations, brightness alterations, and partly obscured patterns. Electrophysiological studies (Miles, 1912b) demonstrated an effect of ION stimulation on the disinhibition of retinal ganglion cell receptive-field surrounds and the facilitation of the excitatory field centers. The first mechanism would sacrifice contrast sensitivity for responsiveness to a wide range of target forms and would thus confer improved detectability. The second mechanism, on the other hand, would increase sensitivity to small objects without loosening constraints on shape and size, thus enhancing the discriminative capacity of the visual system. Both mechanisms would enable pigeons to adapt to local optic background variations within the context of feeding, a process called "highlighting" in Uchiyama's (1989) excellent overview. While this could be the functional framework within which the ION operates, it is not the context in which the EION appears to be involved. The results of the visual acuity task (experiment 2) indicate that under the conditions used, spatial-resolution capacity is unimpaired by electrocoagulation lesions of ION and EION. Our findings are in accord with the results of a similar study by Knipling (1978). He found no deficits in near-field visual acuity after transection of the isthmo-optic tract, which is the pathway of the efferent fibers to the retina. Since the electrophysiological studies of Miles (19726) and Holden and Powell (1972) demonstrated that a large number of ION units show a preference for target movements in the anterior visual field and habituate rapidly to repetitive stimulation, several authors have suggested a role of the CVS in early detection of predators (Holden, 1990). This was additionally supported by the fact that CVS terminals innervate the horizontal and inferior parts of the contralateral retina (Hayes & Holden, 1983), on which a distant predator would first cast an image. Furthermore, the behavioral studies of Rogers and Miles (1972) showed that ION lesions altered the chick's ability to detect slowly moving targets introduced into their posterior visual field. The present results do not support the hypothesis that any

CVS subcomponent is involved in an early-detection mechanism. The statistical analysis demonstrates that there was not even a tendency for an interaction of lesion extents and behavioral values. The early-detection hypothesis also seems to us to be questionable on logical grounds. In a situation in which instantaneous escape after detecting a predator is the only possible way to survive, an efferent system which projects back to the retina to refine the optic signal hardly seems to be adaptive. The present study demonstrates that ION lesions result in significant deficits in the grain-grit discrimination. Pigeons, pecking a seed, make convergent eye movements so that the binocular frontal field below the eye-beak axis is represented in the retinal red fields (Martinoya et al., 1984; Erichsen et al., 1989; Nalbach et al., 1990; but see Hayes et al., 1987). The animals of the present study maintained their usual pecking posture with an eye-grain distance of 3.5-5 cm while feeding from the tray in the grain-grit experiment. Thus, it can be assumed that the relevant stimuli were also projected on their red fields. Anatomical studies of Hayes and Holden (1983) in pigeons demonstrated that the centrifugal terminal arborizations are concentrated in a horizontal band of the retina and are virtually absent in the red field. Thus, ION lesions result in task-specific deficits although ION terminals are absent in those retinal areas on which the relevant stimuli project. Intraretinal projections could solve this puzzling discrepancy, and indeed, there is evidence that long intraretinal projection systems exist. Catsicas et al. (19876) described neurons in the inner nuclear layer of the ventral half of the retina, which project topographically onto the dorsal retina. Catsicas et al. (19876) speculate that the intraretinal connections may be involved in a system for selective switching of attention between the upper and lower halves of the visual field under partial centrifugal control. Furthermore, Ehrlich et al. (1987) identified substance P-like immunoreactive amacrine cells in the horizontal meridian of the chick's retina with long-distance intraretinal projections. The neuronal systems identified by Catsicas et al. (19876) and Ehrlich et al. (1987) are both located in those parts of the retina in which the majority of centrifugal axons terminate (Hayes & Holden, 1983; Catsicas et al., 1987a). We therefore speculate that the centrifugal projection may make synaptic contacts upon these intraretinal projection neurons and could thereby influence the neuronal activity within the red field in pigeons.

Acknowledgments We thank Andi Wohlschlager for invaluable technical assistance during conduct of the study and help with the statistical analysis. We also gratefully acknowledge Juan Delius and Julia Wheatley for critically reading the manuscript. This research was supported by a grant from the Deutsche Forschungsgemeinschaft and a SClENCE-plan grant from the European Community.

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