Cosme Salas

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.

Avoidance Response in Goldfish: Emotional and Temporal Involvement of Medial and Lateral Telencephalic Pallium

The hippocampus and the amygdala are involved in avoidance learning in mammals. The medial and lateral pallia of actinopterygian fish have been proposed as homologous to the mammalian pallial amygdala and hippocampus, respectively, on the basis of neuroanatomical findings. This work was aimed at studying the effects of ablation of the medial telencephalic pallia (MP) and lateral telencephalic pallia (LP) in goldfish on the retention of a conditioned avoidance response previously acquired in two experimental conditions. In the first experiment, fish were trained in nontrace avoidance conditioning. In the second experiment, fish were trained in trace avoidance conditioning in which temporal cues were crucial for the learning process. An MP lesion affected the retention of the avoidance response in both procedures; in contrast, an LP lesion impaired the retention only in the trace-conditioning procedure. These data support the presence of two different systems of memory in fish, based on discrete telencephalic areas: the MP, involved in an emotional memory system; and the LP, involved in a spatial, relational, or temporal memory system. Moreover, these differential effects were similar to those produced by amygdalar and hippocampal lesions in mammals. We conclude that these specialized systems of memory could have appeared early during phylogenesis and could have been conserved throughout vertebrate evolution.

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.

Hallmarks of a common forebrain vertebrate plan: Specialized pallial areas for spatial, temporal and emotional memory in actinopterygian fish

In mammals and birds different pallial forebrain areas participate in separate memory systems. In particular, the hippocampal pallium is implicated in spatial memory and temporal attribute processing, whereas the amygdalar pallium is involved in emotional memory. Here we analyze the involvement of teleost fish lateral and medial pallia, proposed as homologous to the hippocampus and amygdala, respectively, in a variety of learning and memory tasks, such as spatial memory; reversal learning; delay or trace motor classical conditioning; heart rate, emotional classical conditioning; and two way active avoidance conditioning. Results show that the damage to the lateral pallium produces a profound deficit in spatial learning and memory in teleost fish. In addition, lateral pallium lesions produce a significant deficit in trace classical conditioning, whereas they have no significant effects on delay conditioning, or in heart rate conditioning. In contrast, medial pallium lesions disrupt emotional, heart rate conditioning and avoidance conditioning, but spare spatial memory and temporal stimulus processing. These data demonstrate a striking functional similarity between the medial and lateral pallia of teleost fish and the pallial amygdala and hippocampal pallium of land vertebrates, respectively. The reviewed evidence suggest that these two separate memory systems, the hippocampus-dependent spatial, relational or temporal memory system, and the amygdala based emotional memory system, could have appeared early during evolution, having conserved their functional identity through vertebrate phylogenesis.

Evolution of Forebrain and Spatial Cognition in Vertebrates: Conservation across Diversity

Historically the dominant trend in comparative brain and behavior research has emphasized the differences in cognition and its neural basis among species. In fact, the vertebrate forebrain shows a remarkable range of diversity and specialized adaptations. Probably the major morphological variation is that observed in the telencephalon of the actinopterygian fish, which undergoes a process of eversion during embryonic development, relative to the telencephalon of non-actinopterygians (for instance, amniotes), which develops by a process of evagination. These different developmental processes produce notable variation, mainly two solid telencephalic hemispheres separated by a unique ventricle in the actinopterygian radiation that contrasts with the hemispheres with internal ventricles in other groups. However, an increasing amount of evidence reveals that the forebrain of vertebrates, whether everted or evaginated, presents a common pattern of basic organization that supports highly conserved cognitive functions. We analyze here recent data indicating a close functional similarity between spatial cognition mechanisms in different groups of vertebrates, mammals, birds, reptiles, and teleost fish, and we show in addition that they rely on homologous neural mechanisms. Thus, recent functional and behavioral comparative evidence is added to the developmental and neuroanatomical data suggesting that the evolution of cognitive capabilities and their neural basis in vertebrates could have been more conservative than previously realized.

Neuropsychology of learning and memory in teleost fish.

Traditionally, brain and behavior evolution was viewed as an anagenetic process that occurred in successive stages of increasing complexity and advancement. Fishes, considered the most primitive vertebrates, were supposed to have a scarcely differentiated telencephalon, and limited learning capabilities. However, recent developmental, neuroanatomical, and functional data indicate that the evolution of brain and behavior may have been more conservative than previously thought. Experimental data suggest that the properties and neural basis of learning and memory are notably similar among teleost fish and land vertebrates. For example, lesion studies show that the teleost cerebellum is essential in classical conditioning of discrete motor responses. The lateral telencephalic pallium of the teleost fish, proposed as homologous to the hippocampus, is selectively involved in spatial learning and memory, and in trace classical conditioning. In contrast, the medial pallium, considered homologous to the amygdala, is involved in emotional conditioning in teleost fish. The data reviewed here show a remarkable parallelism between mammals and teleost fish concerning the role of different brain centers in learning and memory and cognitive processes. These evidences suggest that these separate memory systems could have appeared early during the evolution of vertebrates, having been conserved through phylogenesis.

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.

Cognitive and emotional functions of the teleost fish cerebellum.

Increasing experimental and neuropsychological evidence indicates that the cerebellum of humans and other mammals, traditionally associated with motor control, is implicated in a variety of cognitive and emotional functions. For example, the cerebellum has been identified as an essential structure in different learning processes, ranging from simple forms of associative, sensory-motor learning and emotional conditioning, to more complex, higher-order processes such as spatial cognition. Although neuroanatomical and neurophysiological data indicate that the organization of the cerebellum is notably well conserved in vertebrates, little is actually known about the cerebellar contribution to processes besides the motor domain in non-mammals. In this work, we analyzed the involvement of the teleost fish cerebellum on classical conditioning of motor and emotional responses and on spatial cognition. Cerebellum lesions in goldfish impair the classical conditioning of a simple eye-retraction response analogous to the eyeblink conditioning described in mammals. Single unit extracellular electrophysiological recording and cytochrome oxidase histochemistry also reveal the involvement of the teleost fish cerebellum in classical conditioning. Autonomic emotional responses (e.g., heart rate classical conditioning) are also impaired by cerebellum lesions in goldfish. Furthermore, goldfish with cerebellum lesions present a severe impairment in spatial cognition. In contrast, cerebellum lesions do not produce any observable motor deficit as indicated by the swimming activity or obstacle avoidance and do not interfere with the occurrence of unconditioned motor or emotional responses. These data indicate that the functional involvement of the teleost cerebellum in learning and memory is strikingly similar to mammals and suggest that the cognitive and emotional functions of the cerebellum may have evolved early in vertebrate evolution, having been conserved along the phylogenetic history of the extant vertebrate groups.