Emilio Durán

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.

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.

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.

Cerebellum lesion impairs eyeblink-like classical conditioning in goldfish.

The cerebellum of mammals is an essential component of the neural circuitry underlying classical conditioning of eyeblink and other discrete responses. Although the neuroanatomical organization of the cerebellum is notably well conserved in vertebrates, little is actually known about the cerebellar learning functions in nonmammal vertebrate groups. In this work we studied whether the cerebellum of teleost fish plays a critical role in the classical conditioning of a motor response. In Experiment 1, we classically conditioned goldfish in a procedure analogous to the eyeblink conditioning paradigm commonly used in mammals. Goldfish were able to learn to express an eyeblink-like conditioned response to a predictive light (conditioned stimulus) that was paired with a mild electric shock (unconditioned stimulus). The application of unpaired and extinction control procedures demonstrated that also in teleosts the learning of this motor response depends on associative rules. In Experiment 2 we studied whether classical conditioning of this response is critically dependent on the cerebellum and independent of telencephalic structures as occurs in mammals. Cerebellum lesion prevented the acquisition of the eyeblink-like conditioned response whereas telencephalon ablation did not impair the learning of this response. No deficit was observed following lesions in the performance of the unconditioned response or in the percentage of spontaneous responses. These results suggest that cerebellum ablation in goldfish affects a critical component of the circuitry necessary for the acquisition of the conditioned response but does not interfere with the ability of the animal to perform the response itself. The striking similarity in the role of cerebellum in classical conditioning of a motor response between teleost fish and mammals suggests that this learning function of the cerebellum could be a primitive feature of the vertebrate brain that has been conserved through evolution.

1.26 – Spatial Learning in Fish

Fish possess well-developed abilities for spatial orientation and navigation. Their spatial behavior is a flexible and adaptive process that involves a variety of cognitive phenomena and diverse learning and memory mechanisms. Fish can use diverse sources of spatial information from different sensory modalities and rely on a variety of spatial strategies that parallel those described in land vertebrates. These multiple, separate spatial learning and memory systems present particular properties and are based on a variety of neural substrata. Egocentric orientation mechanisms are based on the function of the brainstem, cerebellum, or optic tectum. Map-like, allocentric spatial memory representations depend on the lateral telencephalic pallium, suspected to be homologous to the hippocampus of land vertebrates. The close functional similarity between the spatial cognition mechanisms and their neural basis in different groups of vertebrates suggests that the evolution of these cognitive capabilities may be a conserved trait.

Variation in Brain Organization of Coral Reef Fish Larvae according to Life History Traits

In coral reefs, one of the great mysteries of teleost fish ecology is how larvae locate the relatively rare patches of habitat to which they recruit. The recruitment of fish larvae to a reef, after a pelagic phase lasting between 10 and 120 days, depends strongly on larval ability to swim and detect predators, prey and suitable habitat via sensory cues. However, no information is available about the relationship between brain organization in fish larvae and their sensory and swimming abilities at recruitment. For the first time, we explore the structural diversity of brain organization (comparative sizes of brain subdivisions: telencephalon, mesencephalon, cerebellum, vagal lobe and inferior lobe) among larvae of 25 coral reef fish species. We then investigate links between variation in brain organization and life history traits (swimming ability, pelagic larval duration, social behavior, diel activity and cue use relying on sensory perception). After accounting for phylogeny with independent contrasts, we found that brain organization covaried with some life history traits: (1) fish larvae with good swimming ability (>20 cm/s), a long pelagic duration (>30 days), diurnal activity and strong use of cues relying on sensory perception for detection of recruitment habitat had a larger cerebellum than other species. (2) Fish larvae with a short pelagic duration (<30 days) and nocturnal activity had a larger mesencephalon and telencephalon. Lastly, (3) fish larvae exhibiting solitary behavior during their oceanic phase had larger inferior and vagal lobes. Overall, we hypothesize that a well-developed cerebellum may allow fish larvae to improve their chances of successful recruitment after a long pelagic phase in the ocean. Our study is the first one to bring together quantitative information on brain organization and the relative development of major brain subdivisions across coral reef fish larvae, and more specifically to address the way in which this variation correlates with the recruitment process.

Spatial learning-related changes in metabolic brain activity contribute to the delimitation of the hippocampal pallium in goldfish.

Comparative neuroanatomical, developmental and functional evidence suggests that the lateral division of the area dorsalis telencephali (Dl) of the teleost fish is homologous to the hippocampus of tetrapods. Nonetheless, some important aspects of the organization of the hippocampal pallium of teleosts are still under discussion and conflicting hypotheses regarding the extension and demarcation of this region have been proposed. Thus, whereas some authors suggest that the entire Dl region, including its dorsal (Dld) and ventral (Dlv) subdivisions, is homologue to the mammalian hippocampus, others claim that only Dlv should be considered as such. To further elucidate this debate, we investigated the role of Dld and Dlv in one of the most unambiguous functions of the hippocampus, spatial learning. We trained goldfish in a spatial constancy task and mapped the activity of Dld, Dlv, and the medial division of the area dorsalis telencephali (Dm) by means of cytochrome oxidase (CO) histochemistry. The results revealed that training goldfish in the spatial constancy task significantly increased the metabolic activity in Dlv, but not in Dld or Dm, suggesting that only Dlv is critically involved in spatial learning and in this regard comparable to the hippocampus. These data provide additional functional support to the hypotheses that consider Dl as a heterogeneous pallial region and propose that Dlv, but not Dld, might be homologous to the hippocampus.

Observations on the Brain Development of the Sturgeon Acipenser naccarii

The remarkable range of evolutionary diversification of ray-finned fishes, reflected in the number of species and environmental adaptations, is also evident in their brain structure. Among the ray-finned fishes, the Chondrostei, an early branch of the actinopterygian line, are usually considered the extant taxa most closely related to the primitive actinopterygians living in the Paleozoic Era, and sharing with them numerous characteristics. Unfortunately, current knowledge of the ontogenesis of the central nervous system and behaviour of the chondrosteans is rudimentary, despite their evolutionary importance. Thus, the study of the morphologic and functional organization of the chondrostean lineage brain is an essential step in identifying the primitive and derived traits. The present work summarizes recent data on the gross morphology and cytoarchitecture of the brain of the sturgeon Acipenser naccarii, during ontogenesis. In addition, the main changes in the development of the five main brain subdivisions have been compared to the onset of different types of behaviour that provide a rough index of sensory and motor maturation.