The effects of extensive forebrain lesions on visual discriminative performance in turtles (Chrysemys picta picta)

Brain Research, 192 (1980) 327-337

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© Elsevier/North-Holland Biomedical Press

T H E EFFECTS OF EXTENSIVE F O R E B R A I N LESIONS ON VISUAL DISCRIMINATIVE P E R F O R M A N C E IN T U R T L E S ( C H R Y S E M Y S PICTA PICTA)

ANTON REINER and ALICE SCHADE POWERS Department of Psychiatry and Behavioral Science, Health Sciences Center, SUNY at Stony Brook, Stony Brook, N.Y. 11794 and (A.S.P.) Department of Psychology, Bryn Mawr College, Bryn Mawr, Pa. 19010 (U.S.A.)

(Accepted December 13th, 1979) Key words: turtle - - visual discrimination -- lesions -- lateral forebrain bundle - - dorsal thalamus

SUMMARY Though anatomical research has demonstrated major ascending telencephalically directed visual channels in reptiles, little behavioral research has examined reptilian forebrain visual functions. The present study reports the effects of extensive forebrain lesions, involving either severe destruction of dorsal thalamus or disruption of the fibers of the lateral forebrain bundle (by lesions of the basolateral telencephalon), upon visual discriminative performance in the turtle. Such lesions, which extensively damage the ascending visual pathways, rendered turtles incapable of relearning preoperatively acquired visual discriminative problems. The magnitude of the visual impairments observed following such forebrain lesions suggest a major role on the part of the forebrain in visual processing in reptiles.

INTRODUCTION Lesion studies in birds have shown that anatomically defined forebrain visual structures play an important role in avian visual functions. Thus, lesions of nucleus rotundus, a thalamic structure shown to receive input almost exclusively from the tectum 3,~6,47, severely impair pigeons in their ability to perform pattern and intensity discriminations 16,17. Similarly, lesions of the ectostriatum, a telencephalic structure shown to receive input from nucleus rotundus3, 24, also result in severe impairments in pattern and intensity discrimination in pigeons16, is. The ectostriatum and nucleus rotundus make up the forebrain components of the so-called tectofugal visual pathway in birds. An additional telencephalically directed visual pathway, the thalamofugal,

328 has been described in birds 2:). Lesions of both the diencephalic and telencephalic components of the thalamofugal visual pathway also impair visual functions ill pigeons19,~'~,:3~. The results of these behavioral experiments in birds support the suggestion of Karten22, 32 that forebrain organization in birds bears a great resemblance to that in mammals. Despite superficial differences in terms of the arrangement of cell masses, the forebrains of both mammals and birds appear characteristically to possess similar sensory lemniscal pathways that are involved in processing exteroceptive input. For example, although avian telencephalic visual tissue is not arranged in a neocortical fashion, as are the striate and extrastriate visual cortices of mammals, comparable forebrain cell groups and pathways are involved in processing visual input. In other non-mammalian vertebrate classes research has indicated the existence of ascending telencephalically-directed sensory channels 6,s,9,12 14,~0,29,31,3~,39-:H.~s. However, behavioral investigation into the functions of such forebrain sensory regions has been limited 2,1°,15,45. The present report offers further data from a series of behavioral experiments carried out on the forebrain components of the tectofugal visual pathway in a reptile, the eastern painted turtle (Chrysemys picta picta) ~,~. Previous research from our laboratory has shown that lesions of nucleus rotundus, the diencephalic component of the ascending tectofugal visual pathway, impair turtles in their ability to perform both visual intensity and pattern discriminations 45. The present report describes the effects of more extensive diencephalic lesions, involving destruction of the entire dorsal thalamus. In addition, the present report offers the first behavioral evidence that the telencephalon plays a major role in visual discriminative behavior in reptiles. MATERIALS AND METHODS Three turtles were trained to perform an intensity discrimination (0.4 log units difference in luminance between stimuli), while one turtle was trained on a pattern problem (three vertical stripes vs three horizontal stripes). Behavioral training procedures and apparatus have been described elsewhere 45 and will be but briefly reviewed here. A black Plexiglas enclosure was used. Two transparent response keys were located on the front wall of this chamber. Stimuli could be presented to the animal inside the chamber through each response key via rearmounted projectors. Gerber's beef baby food (delivered into the chamber in 0.3 ml quantities via a pumpoperated tubing system) was used as the reinforcer. After pretraining, the turtles learned either the simultaneous pattern task or the simultaneous intensity task. Bright was designated the correct stimulus for the three turtles trained on the simultaneous intensity problem and vertical was designated correct stimulus for the turtle trained on the simultaneous pattern problem. Twenty trials were presented per session, one session per day. A given turtle was preoperatively trained on the intensity problem until it performed at or above 8 0 ~ correct for two consecutive days, or on the pattern problem until it performed at 90 ~ correct or better for two consecutive days. After they had reached preoperative criterion, two of the turtles trained on the

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Fig. l. Photomicrograph and line drawing of a Nissl-stained section through the internal capsular level of the turtle forebrain. The dorsal peduncle (PD) and ventral peduncle (PV) of the lateral forebrain bundle (LFB) course through the basolateral margin of the telencephalon. The LFB contains the telencephalically directed efferent projections of a variety of diencephalic and mesencephalic structures, as well as the extratelencephalic efferent projections of the dorsal cortex and striatal complex. For abbreviations see the list at the end of the paper.

intensity problem (3 and 32) received bilateral electrolytic lesions of the dorsal thalamus. The remaining two turtles (31 and 45) received bilateral electrolytic lesions of the basal telencephalon. The level of the turtle brain at which the lesions were targeted in turtles 31 and 45 is illustrated in Fig. 1. The dorsal and ventral peduncles of the lateral forebrain bundle course through the basal telencephalon at this level. The dorsal peduncle contains the radiations of the dorsal thalamus upon the D V R and dorsal cortex while the ventral peduncle interconnects the subthalamus and tegmentum with the paleostriatal region of the telencephalon14,21,33,34, 42. Lesions of the basal telencephalon thus disrupt the interconnections of lateral telencephalic regions with a variety of brain stem regions. Lesion parameters were 2.0 mA for 20 sec. Surgery was performed under EquiThesin anesthesia (0.2 ml/100 g body weight), using stereotaxic procedures. Coordinates for the target structures were obtained from the stereotaxic atlas of Powers and Reiner 38. Following surgery, all four turtles required extended postoperative recovery and remedial training before an attempt could be made to retrain them on their preoperative discriminative problems. Turtle 32 required 4 months, turtles 3 and 45 two months, and turtle 31 two weeks. Following extensive postoperative discriminative training, during which none of the 4 animals relearned, the turtles were sacrificed and perfused transcardially with saline followed

330 by H e i d e n h a i n ' s fixative. The brains were removed, sectioned, m o u n t e d , and stained with cresyl violet. The extent and locus o f lesion d a m a g e was reconstructed. RESULTS

Fig. 2 illustrates the lesion d a m a g e in turtles 3 a n d 32. In b o t h turtles, the lesions were similar; nearly the entirety o f the d o r s a l t h a l a m u s was destroyed. Nucleus r o t u n d u s was completely destroyed, as were the p e r i r o t u n d a l nuclei, d o r s o m e d i a l i s

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Fig. 3. Preoperativeand postoperative learning curves for turtles (3 and 32) with extensivedestruction of dorsal thalamus. Although given lengthy postoperative training, these turtles never relearned the discriminativeproblem. Discriminativeperformanceremainedat chancelevelthroughout postoperative training. anterior and dorsolateralis anterior. In addition, both the dorsal geniculate nucleus (which relays visual information to the dorsal cortex of the telencephalon in turtles 1~-14) and nucleus reuniens (which probably relays auditory information to the telencephalon (refs. 33, 39, 40)) were extensively destroyed. Fig. 3 presents the behavioral data for these two turtles. Although postoperative training was carried out for three times as many postoperative sessions as preoperative, neither turtle ever relearned the intensity problem. More dramatically, neither turtle seemed capable of above chance performance, the percent correct performance fluctuating about the fifty percent level from session to session. Turtles 31 and 45 sustained bilateral lesions of the basolateral wall of the telencephalon (see Fig. 4), with some damage to the DVR (in the case of turtle 31 the DVR was completely destroyed bilaterally). As a result of such lesions, both turtles 45 and 31 sustained extensive bilateral damage to the lateral forebrain bundle. In turtle 45, both the dorsal and ventral peduncles were extensively destroyed. In turtle 31, the dorsal peduncle was extensively damaged bilaterally, with only slight damage to the ventral peduncle. In turtle 45, extensive bilateral retrograde cell loss was evident in nucleus rotundus. Retrograde cell changes were evident bilaterally in nucleus rotundus in turtle 31, but not so strikingly as in turtle 45. Retrograde cell loss in nucleus rotundus is a recognized concomitant of LFB lesions in reptiles30,3L Since the LFB interconnects the thalamus and tegmentum with a variety of lateral telencephalic regions, LFB destruction interrupts a variety of systems entering and leaving the telencephalon 14,a3,a4. Fig. 5 presents the behavioral data for turtles 31 and 45. Neither turtle ever performed at criterion level (80 ~ for turtle 3 l, 90 ~ for turtle 45) for even a single postoperative day. Both turtles showed some improvement with training, however, consistently performing above chance during the latter half of postoperative training. DISCUSSION The present experiments indicate that diencephalic and telencephalic regions

332

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play a major role in visual discriminative functions in the turtle. Such a result may not be surprising since telencephalically-directed visual lemniscal pathways that relay via discrete dorsal thatamic cell masses have been described in a variety of reptiles ~,s,12-14, 31,34,4t. The severity of the observed deficits following either dorsal thalamic destruction or disruption of the LFB at basolateral telencephalic levels, however, is surprising. Bilateral disruption of the fibers of the LFB and extensive bilateral dorsal thalamic destruction both render turtles incapable of relearning a preoperatively acquired visual discriminative problem, at least within the time limits allowed in the present experiments. Although such extensive lesions may have affected a variety of nonvisual as well as visual functions, the observed discriminative impairments seem largely attributable to a loss in visual functions rather than to a change in arousal,

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motivation or motor functions. The turtles seemed normal in their activity levels, their feeding behavior (both inside and outside the experimental chamber) and their motor functions. The turtles were postoperatively capable of performing the response requirements of the experimental situation (depressing the response keys, eating at the food magazine, etc.), but were never able to relearn the visual discriminative problem. These observations imply that, in all likelihood, the impairments in visual discriminative performance stemmed mainly from an impairment in either the sensory, perceptual or associational aspect of visual functions. In a previous report, we noted that turtles with extensive destruction of nucleus rotundus (the diencephalic component of the ascending tectofugal visual pathway) were also incapable of the postoperative reacquisition of a visual discriminative problem 45. Turtles with extensive destruction of nucleus rotundus, however, did possess some intact visual discriminative ability, since these turtles did perform above chance (but below criterion levels). Turtles with destruction of nearly the entirety of the dorsal thalamus are seemingly more visually impaired than turtles with only nucleus rotundus destruction, since turtles with extensive dorsal thalamic destruction neither relearn postoperatively nor perform above chance. The greater deficit following dorsal thalamic destruction may reflect the additional destruction of the dorsal geniculate nucleus (the diencephalic component of the thalamofugal visual pathway 12, 13). In birds, nucleus rotundus destruction combined with destruction of the nucleus opticus principalis thalami (the diencephalic component of the avian thalamofugal visual pathway) results in a greater impairment than does nucleus rotundus destruction alone 19. A similar mechanism may be in operation in the case of dorsal thalamic lesions in turtles. The possibility that some nonvisual dorsal thalamic structures in turtles play a nonspecific role in visual discriminative functions cannot, however, be excluded. The visual discriminative impairments observed following disruption of LFB fibers via lesions of basolateral telencephalon are a striking feature of the present experiments. Previous research had failed to indicate a measurable role for ana-

334 tomically defined telencephalic visual areas (DVR and dorsal cortex) in reptilian visual discriminative functions z. The present results, thus, represent the first experimental demonstration that telencephalic regions in reptiles play a major role in visual functions. The most likely basis of the visual impairments observed following LFB damage is the disruption of the visual lemniscal pathways to the telencephalon. In addition to the connections of the rotundo-DVR system, fibers of the dorsal geniculate nucleus (the diencephalic component of the thalamofugal visual pathway) course via the LFB to the dorsal cortex (the telencephalic component of the thalamofugal visual pathwayV),la). In other studies of the visual functions of the telencephalon in turtles we have found that complete bilateral destruction of the DVR does result in postoperative losses in visual discriminative performance 46. However, damage to the connections of structures not directly related to vision, such as the striatum, may have contributed to the LFB impairment. Several investigators have studied the effects of discrete telencephalic lesions on species-typical behavior in lizards and caimanll,27, 49. These investigators have noted that lesions of the basolateral wall of the telencephalon result in a greatly decreased responsivity to visual social signals. These results in lizards and caiman are consistent with the presently observed visual discriminative impairments in turtles following lesions of basolateral telencephalon. The present results suggest that the alterations in species-typical behavior in lizards and caiman following basolateral telencephalic lesions may at least in part be attributable to impairments in visual functioning consequent to the disruption of LFB fibers. The present data indicate a greater severity in the impairments in discriminative performance following dorsal thalamic lesions than following LFB lesions. Turtles with dorsal thalamic lesions performed at chance levels throughout discriminative training while turtles with LFB lesions performed above chance during the latter half of discriminative training. Since the known projections of the dorsal thalamus are to the telencephalon via the LFB14, 34, lesions of the dorsal thalamus and LFB might be expected to yield similar effects upon discriminative performance. The mechanism by which dorsal thalamic lesions produce greater impairments than LFB lesions is unclear. One explanation for such results might be that the dorsal thalamus plays a greater role in sensory processing than does the telencephalon in turtles. To do this the dorsal thalamus would have to have extratelencephalic as well as telencephalic projections. The reported absence of retrograde cell loss (except in nucleus rotundus 3°) following telencephalic extirpation supports the idea that the dorsal thalamus has sustaining extratelencephalic projections. In birds, the ventral geniculate nucleus has been noted to project to the tectum 7, and the mesodiencephalic junctional cell groups, nucleus spiriformis medialis (SpM) 2~ and spiriformis lateralis (SpL) ~ have been reported to project to cerebellum and tectum, respectively. In turtles, a ventral geniculate nucleus projection upon the tectum (unpublished observations) has been observed. The chelonian equivalent of SpL, the dorsal nucleus of the posterior commissure (nDCP) also projects to the tectum 43, but no clear-cut equivalent of SpM has been identified in turtles 44. However, the nDCP and the ventral geniculate nucleus sustained only slight damage in the turtles with dorsal thalamic destruction. Thus,

335 although several dorsal thalamic and mesodiencephalic junctional cell groups that project extratelencephalically have been described in reptiles, these structures were apparently not involved in the differential effects of dorsal thalamic and LFB lesions. Although the precise basis of the presently observed impairments is not entirely clear, the existence of such severe impairments following damage to the LFB or dorsal thalamus is of interest. A previous generation of researchers had concluded that little processing of nonolfactory sensory input occurred in the forebrains of non-mammalian vertebrates 1,15. Recent anatomical research has suggested that earlier notions might be in error by demonstrating the existence of a wide variety of sensory projections to the dorsal thalamus and telencephalon in nonmammalian vertebrates, but few functional investigations have been carried out 2,1°,2s. Our present data (in conjunction with our other reports 45,46) clearly indicate that forebrain regions in turtles play major roles in visual discriminative functions. Thus, the forebrain participates significantly in the processing of sensory input not only in mammals and birds, but in reptiles as well. ABBREVIATIONS AT Area triangularis CN Core nucleus cd Cortexdorsalis cdm Cortexdorsomedialis cm Cortexmedialis cp Cortexpyriformis DLA Nucleusdorsolateralis anterior DMA Nucleusdorsomedialis anterior DVR Dorsal ventricular ridge d Area d FPL (LFB) Fasciculus prosencephali lateralis (lateral forebrain bundle) GLd Nucleusgeniculatus lateralis pars dorsalis GLv Nucleusgeniculatus lateralis pars ventralis GP Globuspallidus

NGP NLM NPd NPv nBOR PA PD PT PV R Re TO TT V

Nucleus geniculatus pretectalis Nucleus lentiformis mesencephali Nucleus pretectalis dorsalis Nucleus pretectalis ventralis Nucleus of the basal optic root Paleostriatum augmentatum Peduncularis dorsalis fasciculi prosencephali lateralis Pallial thickening Peduncularis ventralis fasciculi prosencephali lateralis Nucleus rotundus Nucleus reuniens Tractus opticus Tractus tecto-thalamicus Ventriculus

ACKNOWLEDGEMENTS This research is based on a dissertation submitted by the first author to the Graduate School of Arts and Sciences, Bryn Mawr College, in partial fulfillment of the requirements for the P h . D . degree. The research was supported by the National Institute of Mental Health Grant 159023 to R. C. Gonzales and by National Eye Institute Grant 01657 to A.S.P.

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