Juan Pedro Vargas

The effects of telencephalic pallial lesions on spatial, temporal, and emotional learning in goldfish

In mammals, the pallial amygdala is implicated in emotional learning and memory, whereas the hippocampus is involved in spatial, contextual, or relational memory. This review presents a set of experiments aimed to study the involvement of the dorsomedial and dorsolateral telencephalon of goldfish in spatial and active avoidance learning. Results showed that (1) medial lesions impaired both acquisition and retention of conditioned avoidance response in two-way active avoidance learning experiments with stimuli overlapping (emotional factor) and with an interstimuli gap (temporal and emotional factors), and (2) the medial lesion did not affect spatial learning (spatial, contextual, or relational factors). In contrast, lateral lesions did not impair conditioned avoidance response with stimuli overlapping, but affected conditioned avoidance response with an interstimuli gap and spatial learning. These results support the presence of two differentiated memory systems in teleost fish based on discrete pallial regions: emotional (dorsomedial telencephalon) and spatial/temporal or relational (dorsolateral telencephalon). Furthermore, these functional data support the homology between the medial pallium of the teleost and the pallial amygdala of land vertebrates, and between the teleost lateral pallium and the mammalian hippocampus.

Spatial memory and hippocampal pallium through vertebrate evolution: insights from reptiles and teleost fish.

The forebrain of vertebrates shows great morphological variation and specialized adaptations. However, an increasing amount of neuroanatomical and functional data reveal that the evolution of the vertebrate forebrain could have been more conservative than previously realized. For example, the pallial region of the teleost telencephalon contains subdivisions presumably homologous with various pallial areas in amniotes, including possibly a homologue of the medial pallium or hippocampus. In mammals and birds, the hippocampus is critical for encoding complex spatial information to form map-like cognitive representations of the environment. Here, we present data showing that the pallial areas of reptiles and fish, previously proposed as homologous to the hippocampus of mammals and birds on an anatomical basis, are similarly involved in spatial memory and navigation by map-like or relational representations of the allocentric space. These data suggest that early in vertebrate evolution, the medial pallium of an ancestral fish group that gave rise to the extant vertebrates became specialized for processing and encoding complex spatial information, and that this functional trait has been retained through the evolution of each independent vertebrate lineage.

Spatial learning and memory deficits after telencephalic ablation in Goldfish trained in place and turn maze procedures

The present work investigated whether the fish telencephalon is involved in spatial learning based on place strategies in a manner similar to mammalian hippocampus. Goldfish were trained in a 4-arm maze in a room with relevant spatial cues. Sham and to-be-ablated subjects were trained in each of 4 experimental procedures designed as follows: place, turn, place-turn, and control. After acquisition, complete ablations of both telencephalic hemispheres for the experimental groups were carried out. The results showed that ablation exclusively impaired performance in animals using place strategies; in these, accuracy fell to chance level during both postsurgery retraining and reversal periods. In the other groups, ablation of the telencephalon did not induce any significant deficit. These results suggest that the fish telencephalon plays a crucial role in complex place learning.

Encoding of geometric and featural spatial information by goldfish (Carassius auratus)

Goldfish (Carassius auratus) were trained in different place-finding tasks as a means of analyzing their ability to encode the geometric and the featural properties of the environment. Results showed that goldfish could encode and use both geometric and featural information to navigate. Goldfish trained in a maplike, or relational, procedure encoded both types of information in a single representation. In contrast, fish trained in a directly cued procedure developed 2 independent and competing strategies. These results suggest that the geometric properties of the spatial arrangement and discrete landmarks are sensitive to encoding in a maplike or relational system, whereas different sources of spatial information are encoded in a single and flexible representation of the environment.

PERFORMANCE OF GOLDFISH TRAINED IN ALLOCENTRIC AND EGOCENTRIC MAZE PROCEDURES SUGGESTS THE PRESENCE OF A COGNITIVE MAPPING SYSTEM IN FISHES

Goldfish were trained to obtain food in a four-arm maze placed in a room with relevant spatial cues. Four experimental conditions were run: allocentric, egocentric, egocentric + allocentric, and control. Relative to controls, all groups were able to solve the different tasks with high accuracy after 1 week of training. Subsequent transfer tests revealed place and response strategies for allocentric and egocentric groups, respectively, and both types of strategies for the ego-allocentric group. Moreover, the allocentric group showed the capacity to choose the appropriate trajectory toward the goal, even from novel starting points, presumably by using the distal cues as a whole. The results suggest that, in addition to using egocentric strategies, goldfish are able to solve spatial tasks on the basis of allocentric frames of reference and to build complex spatial cognitive representations of their environment.

Hippocampal formation is required for geometric navigation in pigeons.

The geometric properties of bounded space have attracted considerable attention as a source of spatial information that can guide goal navigation. Although the use of geometric information to navigate has been observed in every species studied to date, the neural mechanisms that support the representation of geometric information are still debated. With the purpose of investigating this topic, we trained pigeons with lesion to the hippocampal formation to search for food in a rectangular‐shaped arena containing one wall of a different color that served as the only distinctive environmental feature. Although lesioned pigeons learned the task even faster than control animals, probe trials showed that they were insensitive to geometric information. Control animals could encode and use both geometric and feature information to locate the goal. By contrast, lesioned pigeons relied exclusively on the feature information provided by the wall of a different color. The results indicate that the avian hippocampal formation is critical for learning the geometric properties of space in homing pigeons.

Emotional and spatial learning in goldfish is dependent on different telencephalic pallial systems

In mammals, the amygdala and the hippocampus are involved in different aspects of learning. Whereas the amygdala complex is involved in emotional learning, the hippocampus plays a critical role in spatial and contextual learning. In fish, it has been suggested that the medial and lateral region of the telencephalic pallia might be the homologous neural structure to the mammalian amygdala and hippocampus, respectively. Although there is evidence of the implication of medial and lateral pallium in several learning processes, it remains unclear whether both pallial areas are involved distinctively in different learning processes. To address this issue, we examined the effect of selective ablation of the medial and lateral pallium on both two‐way avoidance and reversal spatial learning in goldfish. The results showed that medial pallium lesions selectively impaired the two‐way avoidance task. In contrast, lateral pallium ablations impaired the spatial task without affecting the avoidance performance. These results indicate that the medial and lateral pallia in fish are functionally different and necessary for emotional and spatial learning, respectively. Present data could support the hypothesis that a sketch of these regions of the limbic system, and their associated functions, were present in the common ancestor of fish and terrestrial vertebrates 400 million years ago.

Spatial learning-induced increase in the argyrophilic nucleolar organizer region of dorsolateral telencephalic neurons in goldfish

Spatial learning and memory related morphological changes in the argyrophilic nucleolar organizer region (AgNOR) of telencephalic neurons in goldfish were quantitatively evaluated by means of AgNOR neurohistochemical stain. The AgNORs and nuclei of nerve cells of two different telencephalic regions of goldfish trained in a spatial task or submitted to a similar non-contingent behavioral procedure (control group) were morphometrically evaluated. Results show that the area of AgNORs in goldfish dorsolateral telencephalic neurons increased significantly in the spatial learning group but not in control group. This effect seems to be highly specific as it did not appear in the dorsolateral area of the control group neither in the dorsomedial area of both groups. As the size of AgNORs in the nerve cell nuclei reflect the level of transcriptive activity, these morphological changes could be revealing increased protein synthesis in goldfish dorsolateral telencephalic neurons related with learning and memory. These findings could contribute to determining the subregions of the teleost telencephalon implicated in spatial learning and could indicate that the AgNOR staining technique would be a useful tool in assesing learning and memory related neuronal activity.

Spatial and non-spatial learning in turtles: the role of medial cortex.

In mammals and birds, hippocampal processing is crucial for allocentric spatial learning. In these vertebrate groups, lesions to the hippocampal formation produce selective impairments in spatial tasks that require the encoding of relationships among environmental features, but not in tasks that require the approach to a single cue or simple non-spatial discriminations. In reptiles, a great deal of anatomical evidence indicates that the medial cortex (MC) could be homologous to the hippocampus of mammals and birds; however, few studies have examined the functional role of this structure in relation to learning and memory processes. The aim of this work was to study how the MC lesions affect spatial strategies. Results of Experiment 1 showed that the MC lesion impaired the performance in animals pre-operatively trained in a place task, and although these animals were able to learn the same task after surgery, probe test revealed that learning strategies used by MC lesioned turtles were different to that observed in sham animals. Experiment 2 showed that the MC lesion did not impair the retention of the pre-operatively learned task when a single intramaze visual cue identified the goal. These results suggest that the reptilian MC and hippocampus of mammals and birds function in quite similar ways, not only in relation to those spatial functions that are impaired, but also in relation to those learning processes that are not affected.

Involvement of the telencephalon in spaced-trial avoidance learning in the goldfish (Carassius auratus)

Goldfish (Carassius auratus) received escape-avoidance training in a shuttle-response situation at a rate of a single trial per day. Widely spaced training evaluates the ability of a discriminative stimulus to control an avoidance response in the absence of stimulus carry-over effects from prior recent trials. In Experiment 1, master goldfish exhibited significantly faster avoidance learning than yoked controls. The results suggest that the shuttle response was instrumentally acquired. Experiment 2 demonstrated a significant deficit in the acquisition of avoidance behavior following ablation of the telencephalon. The implications of spaced-trial, telencephalon-dependent avoidance learning, as demonstrated in these experiments for the first time, are discussed in the context of comparative research on instrumental learning in goldfish. These results provide further support for the hypothesis that the fish telencephalon contains an emotional system that is critical for fear conditioning.