Amygdalectomy and ventromedial prefrontal ablation produce similar deficits in food choice and in simple object discrimination learning for an unseen reward

Summary Cynomolgus monkeys (Macaca fascicularis) with either bilateral amygdalectomy or bilateral ventromedial prefrontal cortical ablations showed abnormal choices between apple, lemon, olive, and meat. Not only did they choose meat or olive more often than normal animals, but also their choices were less consistent from trial to trial than the normal animals' choices were. The same animals were subsequently tested for their ability to learn 2-choice simultaneous visual discriminations between objects which they could suck. The positive object yielded fruit juice, which entered the mouth directly without being seen. Both groups of animals with lesions were severely impaired in this discrimination learning task. The reason why amygdalectomy has little effect on simple object discrimination learning in the Wisconsin General Test Apparatus, we suggest, is that the animal can there associate the visual discriminanda with the visual properties of the food reward, a mechanism which is not available when the reward is unseen. These results add to existing evidence of a close functional relationship between the amygdala and the ventromedial prefrontal cortex, and they support the proposal, derived from previous work, that the amygdala is important for associating visual stimuli with the incentive value of reinforcers.     

Cortical and tectal control of visual orientation in the gerbil: Evidence for parallel channels

Summary Two experiments were carried out with Mongolian gerbils to determine the roles of optic tectum and visual cortex in the mediation of visually guided head turns and locomotion elicited and controlled by discrete visual targets. In Experiment 1, the behavior of animals with either a sham operation, a bilateral lesion of optic tectum, or a bilateral ablation of areas 17, 18a, and 18b was recorded on videotape as they ran from the center of a circular arena toward a small visual target projected in different locations around the perimeter of the arena. The amplitude and direction of the head turns and the accuracy of their locomotor responses were reconstructed from a frame by frame analysis of the videotapes.Sham-operate gerbils made a series of head turns before running accurately and efficiently toward the target. The gerbils with lesions of areas 17, 18a, and 18b rarely made more than one head turn before running toward the perimeter of the arena. Although the single head turn they did make was often well-correlated with the position of the target in their visual field, the direction of their locomotor response was largely determined by the direction and amplitude of that head turn. As a consequence, these animals undershot the target more often than did the sham-operate animals, and even ran into the visual half field opposite the target if their head turn had also been made into that half field. Unlike the sham operates, these animals were unable to make further adjustments in their orientation toward the stimulus after their initial head turn.The head turns and locomotor behavior of the gerbils with lesions of optic tectum were even more disorganized and inaccurate than those of the posterior decorticates. Nevertheless, when the target was presented within 45° from their visual midline, their head turns and locomotor responses showed a systematic relationship with the eccentricity of the target. Their behavior to stimuli outside this central wedge of their visual field was completely disorganized and showed no relationship to the location of the target.In Experiment 2, unilateral lesions of area 17 were performed in the gerbils that had already received bilateral tectal lesions to determine whether such lesions would affect the residual ability of these animals to orient toward stimuli located within the central portion of their visual field. During retesting, these animals were able to respond to targets only if they were located in the central portion of the field ipsilateral to the cortical lesion.These results suggest that orientation to discrete visual targets is mediated by both tectal and geniculostriate pathways with the tectofugal system subserving responses to stimuli throughout the entire visual field and the corticofugal system organizing behavior to stimuli within the central portion of the visual field. It is argued that the output from these two parallel sensorimotor systems converges on common motor centers in the pontine reticular formation.Supported by Grant A6313 from the Natural Sciences and Engineering Research Council of Canada to M. A. Goodale     

The effects of pretectal and superior collicular lesions on binocular vision

Summary Monkeys with mid-brain lesions involving the pre-tectum and superior colliculi often have an odd stare, as if the visual axes were parallel and the animal was looking into the distance. Such a visuo-motor abnormality could lead to double-vision for objects close to the animal. The experiments reported here were designed to test this hypothesis of diplopia in monkeys with combined bilateral ablations of the colliculi and frontal eye-fields (area 8). These animals performed better on a task of visually-guided reaching, and in a series of visual pattern discriminations, when they viewed stimuli monocularly rather than binocularly. Monkeys with other cortical lesions showed no such monocular superiority. We propose that an abnormality of vergence eye movements provides a simple explanation for some of the so-called perceptual impairments that follow damage to the mid-brain visual pathways in monkeys     

Somatosensory cross-modal plasticity in the superior colliculus of visually deafferented rats

The effects of neonatal visual deafferentation on the final adult pattern of cortico-collicular connections from the rat primary somatosensory cortex barrel field were studied by injecting an anterograde tracer (BDA) into different locations of the barrel cortex. Collicular afferents originating in the barrel cortex normally end in the intermediate collicular strata (SGI and SAI). However, neonatal visual deafferentation caused an invasion of abundant somatosensory cortical afferents into the lateral portions of the superficial collicular strata (SGS and SO). Moreover, anterograde-labelled fibers in the intermediate strata were more densely packed in visually deafferented animals. In order to study the activity of the altered somatosensory cortico-collicular connection, the effects of two different types of whisker stimuli on c-fos expression in the SC were analyzed (apomorphine treatment and enriched environment exploration). In stimulated control animals, c-fos expression was clearly evident in neurons of the intermediate layers 2 h after whisker stimulation. Similar stimulation in adult animals that underwent neonatal visual deafferentation triggered higher levels of c-fos expression in the superficial collicular layers that were invaded by cortico-collicular axonal branches. In exploration experiments, increased levels of c-fos expression were also detected in lateral parts of the intermediate layers of visually deafferented animals. These results suggest that the ascending fibers of somatosensory cortical origin can recruit deafferented superficial collicular neurons that enabling them to participate in extravisual behavioural responses mediated by collicular circuits.     

Brain neocortex modulation of mitogen-induced interleukin 2, but not interleukin 1, production

Interleukin 2 (IL-2) production by splenic T cells stimulated by Concanavalin A was studied in mice after unilateral or bilateral brain neocortex ablation. The brain cortex was shown to modulate IL-2 production in an asymmetrical way. IL-2 levels were higher in animals with a right cortical lesion (group R) and lower in mice with a symmetrical lesion (group L) as compared to controls, differences between groups R and L being significant. Such variations of IL-2 production that were observed after unilateral lesions were abolished with bilateral cortical ablations. These results extend the immunoregulatory roles of the brain neocortex to IL-2 production by splenic T cells and may provide molecular support for neuro-immunological networks.     

Cortical suppression of the ritino-collicular pathway in the monocularly deprived cat.

1. In nine cats monocularly deprived from birth, the responses of single neurones in the superior colliculus contralateral to the deprived eye were studied. 2. In six animals most units could be driven by visual stimuli only through the ipsilateral (experienced) eye despite the fact that this colliculus receives a major input from the contralateral (deprived) retina. 3. Immediately following removal of visual cortex, including areas 17, 18 and 19, the collicular units could be driven by the deprived eye. 4. We conclude that the cortex must exert a powerful suppression of the retino-collicular input, and we argue that this suppression occurs in normal as well as in monocularly deprived animals. 5. In three animals the retinal input from the deprived eye was not suppressed but instead dominated many collicular celld, apparently to the exclusion of the cortical input from the experienced eye.     

Differential and reversal conditioning in partially neodecorticate rabbits

Normal rabbits and rabbits with extensive unilateral or bilateral neocortical lesions were required to differentiate between visual and auditory stimuli in a Pavlovian situation and then to reverse that differentiation. It was found that neocortical ablations had no effect on the initial differentiation and that the lesioned animals were superior to normals in their performance on the reversal task. The lesioned animals in particular did not show the same tendency as normals to continue responding to the negative stimulus under reversal conditions. Possible sources of the apparently greater efficiency shown by the neodecorticates are discussed.     

Effects of striatectomy and colliculectomy on achromatic thresholds in the monkey

The differential achromatic thresholds at photopic and scotopic levels of illumination were determined with normal, destriate and colliculectomized rhesus monkeys in order to evaluate the effects of removal of these 2 sets of neural structures on this primitive visual function. The discriminanda were achromatic patches subtending approximately 3.5 to 10° of visual angle. The main hypothesis was that their removal would result in a marked increase in the differential threshold though not necessarily to the same degree. This hypothesis was confirmed in the case of striate cortex removal, since the operation produced a threefold increase in threshold. The collicular ablations did not give as conclusive results since threshold increased in nearly all cases but only slightly. A second hypothesis was that the cortical ablation would affect photopic thresholds more than scotopic thresholds since the cortex had been postulated as being the only structure receiving cone input. This hypothesis was not confirmed since both photopic and scotopic thresholds increased to approximately the same extent.     

Effects of serial lesions of somatosensory cortex and further neodecortication on tactile retention in rats

Four groups of rats with bilateral lesions of somatosensory cortex and one of animals sustaining only sham operations were tested for retention of a difficult tactile discrimination. Two of the lesion groups had serial ablations, in one case with interoperative testing, and two had one-stage lesions. Bilateral ablations of somatosensory cortex severely retarded retention in all lesion groups relative to the control group and serial and one-stage groups did not differ from each other. The sham operated rats then experienced lesions of cortex anterior and posterior to the somatosensory areas. These lesions only marginally affected retention. Somatosensory cortex then was ablated and severe performance decrements were seen. Removal of additional neocortex in animals that previously had relearned the discrimination after somatosensory cortex lesions also resulted in very poor retention. These data demonstrate the importance of the somatosensory cortex in mediating tactile discriminations and suggest that non-somatosensory cortex may play a role in recovery after somatosensory cortical lesions.     

The nature of the visual discrimination impairment after neonatal or adult ablation of superior colliculi in rats

Summary The superior colliculi were removed in rats at either one or five days of age or in adulthood. Seven months later they were tested on four successively presented two-choice intensity discriminations. The intensity difference between the discriminanda was reduced across the four problems to encourage choice by comparison. The purpose was to establish whether impoverished scanning is a feature of rats with collicular lesions and whether the age at which the lesion is incurred is important. The number of door-push and approach errors made in reaching criterion were used as measures of performance and the number of head-scans during acquisition was counted. The results provide no evidence that either one- or five-day operated rats exhibit sparing or recovery of the ability to scan discriminanda since all operated animals were impaired. Furthermore, novel retinal projections, present in one-day operated animals, fail to mediate such sparing. Finally, the results did not demonstrate a selective increase in approach errors following collicular lesions and were therefore inconsistent with the view that the impairment is one of visually-guided locomotion. It is concluded that visual discrimination learning is impaired following collicular lesions in circumstances where scanning of discriminanda is required for efficient performance.     

Effects of bilateral frontal lesions on habituation of the head-shake response in the rat

This experiment investigated the effects of bilateral frontal cortical lesions on the frequency and shape of the habituation curve of the head-shake response, elicited by stimulating the ear with a stream of air, in the rat. The results from an initial procedural-control group indicated that the damage done to the ear by mounting the rats in a stereotaxic was sufficient to increase responding. The results from the basic experiment, using a before-after design, indicated that bilateral frontal cortical lesions led to an overall increase in responding but had no effect on the shape of the habituation curve over trials. The responding of control animals given bilateral cortical lesions in the occipito-parietal area had no effect on responding. The results suggest that the frontal cortex, at least in the rat, is not involved in habituation of all responses.     

Long-term deficits after somatosensory cortical lesions in rats.

Rats having either sham operations or one-stage bilateral lesions of the two somatosensory areas of the cortex were tested for acquisition of five tactile discriminations after postoperative recovery intervals of 14, 35, 180, 365 or 730 days. The group with lesions performed worse than its time-matched control group in every instance, and there was no evidence for recovery of function with the longer postoperative recovery periods. These results suggest that time per se is not a significant determinant of restitution after somatosensory cortical ablations.     

The role of the cortical parts of the cerebellar hemispheres in discrimination learning of cats

Summary Eighteen cats were used as subjects in a study which investigated the effects of bilateral cortical cerebellar hemispheric ablations upon light-dark discrimination learning. From the operated control group (8 animals), 5 were tested two weeks and 3 three weeks postoperatively. From the experimental group (10 animals) 4 were tested two weeks and 6 three weeks postoperatively. The discrimination task consisted of an instrumentally conditioned bar-pressing response. The results showed that almost during the entire 23-day learning period, the experimental cats performed more poorly on the discrimination task than their controls. It is hypothesized that the difference between the two groups of animals derives from the disturbance (caused by the ablation) of the connections between the cerebellum and other structures involved in the habituation process.Mit Unterstützung der Deutschen Forschungsgemeinschaft.     

Amphetamine-induced recovery of visual cliff performance after bilateral visual cortex ablation in cats: measurements of depth perception thresholds

After bilateral visual cortex ablation, cats exhibit a loss of depth perception as measured on a visual cliff, which recovers following administration of d-amphetamine. In this Study, 3 amphetamine-treated cats with visual cortex ablations showed a rapid and enduring recovery, with 2 of these animals obtaining levels of performance seen only with binocular vision, suggesting a restoration of binocular depth perception. Cats with asymmetrical lesions showed only a transient improvement during amphetamine treatment, and some animals not displaying autonomic signs of amphetamine intoxication did not improve. Saline-treated cats showed no signs of improvement, and the effect of amphetamine was blocked by the catecholaminergic antagonist haloperidol. These results indicate that amphetamine can induce an enduring recovery from a behavioral deficit after brain injury, which if left untreated would not spontaneously recover.     

Effects of serial lesions of somatosensory cortex and further neodecortication on retention of a rough-smooth discrimination in rats

Summary Five groups of rats with bilateral lesions of the somatosensory cortex and one of animals sustaining only sham operations were tested for retention of a rough-smooth discrimination. Two of the lesion groups had sequential unilateral ablations, in one case with interoperative testing, and three groups had one-stage bilateral lesions. The two groups of animals with serial lesions did not differ from each other or from sham operates in relearning the task. Rats with one-stage lesions and preoperative overtraining also performed well, but the other one-stage groups showed deficits relative to control and serial lesion groups. In the second experiment the sham operated rats from Experiment 1 experienced lesions anterior and posterior to the somatosensory zones. These lesions did not affect retention. Somatosensory cortex then was ablated in one operation and severe performance decrements were seen. Removal of additional neocortex in a sample of animals that had relearned the discrimination after one-stage somatosensory cortex lesions (Exp. 1) also affected retention. In contrast, retention was not impaired on some of the measures in those animals that originally had two-stage ablations. The findings from these two experiments show that some ablation effects can be circumvented with overtraining or serial lesion techniques. The data also indicate that non-somatosensory cortex may play a role in recovery after somatic cortex lesions, but that the substrates underlying recovery might, not be the same after one-stage and two-stage ablations.     

A functional analysis of the collicular output pathways: a dissociation of deficits following lesions of the dorsal tegmental decussation and the ipsilateral collicular efferent bundle in the Mongolian gerbil

Summary Mongolian gerbils received either lesions of the superior colliculus, small lesions of the uncrossed efferents of the superior colliculus, knifecuts of the dorsal tegmental decussation, or sham operations. The animals were subsequently tested for avoidance of overhead visual threat, orientation and locomotion toward small targets, and negotiation of a large barrier in order to reach a small target. Animals with collicular lesions showed no responses to overhead threat and had severe deficits in orienting to small targets. Animals with lesions of the uncrossed tectal efferents showed diminished responses to overhead threat but had no deficits in orienting to targets. Animals with lesions of the dorsal tegmental decussation showed only slight reductions in responses to overhead threats but clear impairments in the orientation tasks. The impairments in orientation, however, were less severe than those seen in collicular animals. Animals in all groups were able to negotiate barriers efficiently. These results suggest that separate output pathways of the superior colliculus mediate different types of visuomotor behaviours. The results further suggest that visual orientation to small targets does not depend completely on output through the predorsal bundle, but must also involve other collicular outputs.     

The effects of unilateral and bilateral cortical ablations of the cerebellar hemisphere upon learning and retention of an instrumental light-dark discrimination task in adult cats

Summary Ten adult cats were used as subjects in a study which was designed to investigate the effects of cortical ablations of the cerebellar hemispheres upon learning and retention of a light-dark discrimination task. The discrimination task was instrumentally conditioned in food-deprived cats. The results of this study showed that unilateral or bilateral ablations of the cerebellar hemispheres have no effects upon retention of a learned discrimination task. The data further indicated that bilateral ablations of the cerebellar hemispheres seem to retard learning of a discrimination task during the first 5 days of the learning period. This latter effect was interpreted to be due to a dynamic period of compensation, during which, asCarrea andMettler [3] assumed, the cerebral cortex takes over the functions of the ablated parts of the cerebellum.Mit Unterstützung der Deutschen Forschungsgemeinschaft.     

Dissociated effects of perirhinal cortex ablation,fornix transection and amygdalectomy: evidence for multiple memory systems in the primate temporal lobe

Four experiments were performed with macaque monkeys (rhesus, Macaca mulatta, and cynomolgus, M.fascicularis). In experiment 1 six rhesus monkeys learned pre-operatively to perform delayed matching-to-sample, with complex naturalistic scenes as the stimulus material. Three of these monkeys then received bilateral ablations of the perirhinal cortex, while the other three received fornix transection. Both groups showed an impairment postoperatively, but the effect of perirhinal cortex ablation was significantly more severe than the effect of fornix transection. In experiment 2 the same animals, together with three normal, control rhesus monkeys,which had a similar training history, performed simple, spatial discrimination learning in a Wisconsin General Test Apparatus. The animals with fornix transection were impaired, but the animals with ablations of perirhinal cortex were not. In experiment 3 the nine animals from experiment 2 were tested for the acquisition of systematic preferences among four novel foods (apple, lemon, olive, meat). Their results were compared with those from a previously published experiment with normal and amygdalectomized cynomolgus monkeys which had been given the same food preference test. Amygdalectomy produced a significant disruption of food preference learning but the other two lesions (fornix transection and perirhinal cortex ablation) did not. In experiment 4, 16 rhesus monkeys (9 normal controls, 4 with perirhinal cortex ablation, and 3 with fornix transection) learned to discriminate among complex naturalistic scenes, in a task in which each scene was presented only once per day in the main part of the experiment. The two operated groups were impaired, and there was no significant difference between the severity of the impairments. Thus, the effects of perirhinal cortex ablation can be doubly dissociated from the effects of fornix transection (experiments 1 and 2) and both can be dissociated from the effects of amygdalectomy (experiment 3). Furthermore, the results of experiment 4 show that the effects of perirhinal cortex ablation are not limited to tasks of memory over short retention intervals. On the basis of the presently reported data and other known effects of perirhinal cortex ablation, it is suggested that this ablation produces an impairment in knowledge (semantic memory) about objects.     

Area 21a of cat visual cortex strongly modulates neuronal activities in the superior colliculus

We have examined the influence of cortico-tectal projections from one of the pattern-processing extrastriate visual cortical areas, area 21a, on the responses to visual stimuli of single neurones in the superior colliculi of adult cats. For this purpose area 21a was briefly inactivated by cooling to 10 °C using a Peltier device. Responses to visual stimuli before and during cooling as well as after rewarming ipsilateral area 21a were compared. In addition, in a subpopulation of collicular neurones we have studied the effects of reversible inactivation of ipsilateral striate cortex (area 17, area V1). When area 21a was cooled, the temperature of area 17 was kept at 36 °C and vice versa. In the majority of cases (41/65; 63 %), irrespective of the velocity response profiles of collicular neurones, inactivation of area 21a resulted in a significant decrease in magnitude of responses of neurones in the ipsilateral colliculus and only in a small proportion of cells (2/65; 3.1 %) was there a significant increase in the magnitude of responses. Inactivation of area 21a resulted in significant changes in the magnitude of responses of collicular cells located not only in the retino-recipient layers but also in the stratum griseum intermediale. In most cases, reversible inactivation of area 17 resulted in a greater reduction in the magnitude of responses of collicular cells than inactivation of area 21a. Reversible inactivation of area 21a also affected the direction selectivity indices and length tuning of most collicular cells tested.     

Effects on visual search of lesions of the superior colliculus in infant or adult rats

Summary The superior colliculus was removed from rats at either one or five days of age or in maturity. Four months later they were tested on two versions of a visual search task. Experiment 1 required animals to retrieve food pellets concealed in a depression in the top of identical narrow pillars arranged in an arena. Rats with lesions of the superior colliculus, regardless of the age at operation, showed a large number of return errors compared with sham-operated controls. Return errors were defined as occasions on which the animal returned to pillars that had previously been visited on that trial, before every pillar had been visited at least once. Experiment 2 compared the ability of infantand adult-operated animals to detect and locate a single, baited white pillar in an array of black ones. There were no group differences in response latencies to targets presented in the rostral visual field (within 40° of the midline). However, animals operated on in adulthood or at 5 days of age were slower than both sham-operated animals and animals operated on at one day of age in their responses to more peripheral targets. The latter two groups were indistinguishable.