Susan Harrison

A comparison of the effects of fornix transection and sulcus principalis ablation upon spatial learning by monkeys

In each of three experiments with Cynomolgus monkeys (Macaca fascicularis), there was a group of normal control animals, a group with bilateral cortical ablations in the principal sulcus, and a group with fornix transection. In Expt. 1, half of each group learned problems in which the position of a pair of visual stimuli, to the monkeys left or right, indicated which of the visual stimuli was the correct (rewarded) one. The other animals learned problems in which visual stimuli indicated, irrespective of their own spatial position, whether reward was to be found on the monkeys left or on the right. The animals with fornix transection were impaired in both tasks. The animals with sulcus principalis ablation were also impaired in both tasks. The impairment caused by fornix transection was more severe than that caused by sulcus principalis ablation. Within each of the two operated groups, the degree of impairment in the two tasks was equal, when assessed in proportion to the difficulty of each task for control animals. Expt. 2 showed that neither of the operated groups was impaired in visual discrimination learning with spatial position irrelevant. Expt. 3 tested spatial discrimination learning (acquisition and reversal of a left-right discrimination) with irrelevant visual cues. Here the fornix-transected group was impaired but the group with sulcus principalis ablations was normal. It is suggested, on the basis of these findings and previous results, that fornix transection produces a general deficit in remembering the spatial arrangement of whole scenes, while sulcus principalis ablation produces a deficit in high-order integration involving spatial information.

Effects of fornix transection upon associative memory in monkeys: role of the hippocampus in learned action.

Thirty-three monkeys took part in seven experiments designed to elucidate further the effect of fornix transection on learning and memory. In the first experiment the monkeys had to remember whether stimulus objects had previously been paired with reward or no reward, and they had to use this memory to guide choice between stimulus objects at retention tests according to an arbitrary rule which they had learned: to choose objects previously paired with no reward in preference to objects previously paired with reward. Fornix transection produced a severe and permanent impairment in this task. In the second experiment the monkeys also had to remember object-reward associations but the performance rule was more natural: to choose objects previously paired with reward. Here fornix transection had no effect. The third experiment required the monkeys to remember, given a stimulus object, which of two events of equal valence had previously been the outcome of displacing that object. The two events were either a peanut and a sultana or a black penny and a white penny of equal secondary reinforcing value. Performance was unimpaired by fornix transection. The fourth experiment also demonstrated, in a different paradigm, unimpaired recall of sensory events. The fifth experiment demonstrated an impairment following fornix transection in acquisition of simultaneous spatial-visual conditional discriminations; the sixth demonstrated normal learning by fornix-transected monkeys of a successive spatial-visual conditional discrimination and the seventh demonstrated unimpaired acquisition of a simultaneous auditory-visual conditional discrimination. These results, when considered in detail and together, are incompatible with existing hypotheses of hippocampal function. A new hypothesis is discussed.

Effects of fornix transection on spontaneous and trained non-matching by monkeys

Three monkeys with fornix transection and three normal control monkeys performed a series of tasks which were variations of delayed non-matching. Experiment 1 showed that even at short retention intervals fornix transection impaired the spontaneous tendency to explore novel objects. Experiment 2 provided differential reward for non-matching and showed that the fornix-transected monkeys learned and performed non-matching normally even though the sample-match retention intervals were long throughout the experiment. Experiment 3 showed that non-matching performance was transiently more disrupted in fornix-transected than in normal monkeys when the testing procedure was changed, in a variety of ways, while maintaining the basic non-match rule. Experiment 4 required the monkeys to discriminate objects they had displaced from objects they had seen but not displaced; fornix transection produced in this task a substantial and stable impairment. These four experiments require a revised interpretation of the effects of fornix transection upon recognition memory and exploration. Particularly they contradict the hypothesis, suggested by previous experiments, that fornix transection produces a defect in discrimination of stimulus familiarity in long-term but not in short-term memory. They suggest rather that fornix transection impairs memory of instrumental responses.

Inferotemporal-frontal disconnection and fornix transection in visuomotor conditional learning by monkeys

The first 2 experiments examined the ability of monkeys (Macaca fascicularis) to learn a series of visuomotor conditional discrimination problems for food reward. In each discrimination problem there were 2 visual stimuli, which were different from those in any previous discrimination problem. Each trial within a problem presented either one visual stimulus or the other, and the stimulus indicated which of 2 motor responses, tap or hold, was correct; the motor responses were defined in such a way as to be mutually exclusive. Successive problems were each trained to a criterion of correct performance. In the first experiment, it was found that fornix transection did not impair monkeys learning rate in this task. This result contrasts with previous results showing an impairment of learning rate following fornix transection in visuo-motor conditional discriminations in which the 2 motor responses were differentiated from each other by their spatial position or direction. The present result shows that the earlier demonstrated impairments are specific to spatial responses. In the second experiment, learning rate in the present task was found to be impaired by the combination of a unilateral inferotemporal ablation, contralateral to the hand used in the task by the animal, with a transection of the anterior corpus callosum. This result suggests that cortico-cortical interaction between the inferotemporal area and the frontal lobe contralateral to the hand in use is necessary for efficient learning in this task. The third experiment examined simultaneous 2-choice visual discrimination learning in the animals which had participated in experiment 2. In contrast to the results of Expt. 2, learning rate in this task was unimpaired. Experiment 3 shows that the impairment observed in Expt. 2 is not a general impairment of visual learning.

Reversal learning by fornix-transected monkeys

Experiment 1 examined visual reversal learning and in Experiment 2 monkeys were trained to criterion in a serial reversal set between “FR” and “DRO” response requirements. In both cases impairments were observed in fornix-transected monkeys. These results are discussed in connection with previous findings that in serial reversals damage to the hippocampal system in monkeys causes a deficit in spatial but not in visual learning. A unified account is proposed.

Role of the dorsal prestriate cortex in visuospatial configural discrimination by monkeys

Cynomolgus monkeys (Macaca fascicularis) learned a series of visuospatial configural discriminations in which particular discriminative stimulus objects were rewarded only in particular spatial locations. For example, object X was rewarded if it was on the left but not if it was on the right. After ablation of part of the dorsal prestriate cortex they were impaired in learning discriminations of this kind. The same animals were not impaired in learning visual object discriminations in which spatial position was irrelevant, nor in learning spatial discriminations in which object identity was irrelevant. The results were compared with previously reported results from fornix transection in the same tasks; the deficit following dorsal prestriate ablation in visuospatial configural discrimination learning was similar in severity to that which followed fornix transection. The results show that the dorsal prestriate area has a more general role in visuospatial processing than was known hitherto, and they suggest that it interacts with the hippocampal formation and fornix in visuospatial memory tasks.