A. Gómez

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.

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.

Selective involvement of the goldfish lateral pallium in spatial memory

The involvement of the main pallial subdivisions of the teleost telencephalic pallium in spatial cognition was evaluated in a series of three experiments. The first two compared the effects of lesions selective to the lateral (LP), medial (MP) and dorsal (DP) telencephalic pallium of goldfish, on the retention and the reversal learning of a spatial constancy task which requires the use of allocentric or relational strategies. The results showed that LP lesions produced a selective impairment on the capability of goldfish to solve the spatial task previously learned and on the reversal learning of the same procedure, whereas MP and DP lesions did not produce observable deficits. The third experiment evaluated, by means of the AgNOR stain, learning-dependent changes of the neuronal transcription activity in the pallium of goldfish trained in the spatial constancy task or in a cue version of the same procedure, which only differed on their spatial cognition demands. The results revealed that training in the spatial task produced an increment in the transcriptive activity which was selective to the neurons of the ventral lateral pallium, as indicated by increases in the size of the nucleolar organizing region (NOR), the nucleolar organelles associated with the synthesis of ribosomal proteins. In contrast, training in the cue version did not produced observable changes. These data, revealing a striking functional similarity between the lateral telencephalic pallium of the teleost fish and the amniote hippocampus, provide additional evidence regarding the homology of both structures.

Dorsomedial pallium lesions impair taste aversion learning in goldfish

The present work shows that the dorsomedial telencephalic pallium of teleost fish, proposed as homologous to the amygdala of mammals, is involved in taste aversion learning (TAL). To analyze the behavioral properties of TAL in goldfish, in Experiment 1, we used a delayed procedure similar to that employed with mammals, which consists of the presentation of two flavors on different days, one followed by lithium chloride and the other by saline, both after a 10-min delay. The results showed that goldfish developed a strong aversion to the gustatory stimulus followed by visceral discomfort and that, as in mammals, this learning was rapidly acquired, highly flexible and maintained for a long time. Experiment 2 showed that dorsomedial pallium lesions and the ablation of the telencephalic lobes impaired the acquisition of taste aversion in goldfish, whereas damage to the dorsolateral pallium (hippocampus homologue) or cerebellar corpus did not produce significant changes in this learning. Experiment 3 showed that these TAL deficits were not due to a lesion-related disruption of taste discrimination; goldfish with telencephalon ablation were able to learn to distinguish between the two tested flavors in a differential conditioning procedure. These functional data demonstrate that the dorsomedial pallium in teleosts is, like the amygdala, an essential component of the telencephalon-dependent taste aversion memory system and provide further support concerning the homology between both structures.

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.

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.

Goldfish hippocampal pallium is essential to associate temporally discontiguous events

HighlightsTeleostean Dlv lesions impair trace but not delay heart rate classical conditioning.Dlv telencephalic area is essential to form temporal associative memories.The hippocampal role in relational memory seems to be conserved across vertebrates. Abstract There is general agreement that the hippocampus of vertebrates, from fish to mammals, is involved in map‐like spatial memory. However, in mammals the role of the hippocampus goes beyond the spatial domain as it is also involved in binding the temporally separate events that compose episodic memories. In this regard, the hippocampus of mammals is essential for trace classical conditioning, in which a stimulus‐free time gap separates the conditioned stimulus (CS) and the unconditioned stimulus (US), but not for delay conditioning, in which both stimuli coincide in time. Although the involvement of the hippocampus in encoding relational memories based on a temporal frame‐work has been extensively studied in mammals, there is scarce evidence about the possible contribution of the hippocampus of non‐mammalian vertebrates to the temporal, non‐spatial dimension of relational memories. The present work was aimed to determine if the ventral part of the lateral division of the area dorsalis telencephali (Dlv) of goldfish, proposed as homologous to the hippocampus of mammals, is also involved in trace classical conditioning. With this purpose, goldfish with lesions in Dlv, complete telencephalon ablation and sham operation, were trained in delay and trace heart rate classical conditioning. Dlv lesions severely impaired the acquisition of the conditioned response when a stimulus‐free time gap was elapsed between the CS and the US (trace conditioning), but not when both stimuli overlapped in time (delay conditioning), revealing that this region, like the hippocampus of mammals, is essential to form the temporal associative memories required by trace conditioning. Present data suggest that the presence of a hippocampal pallium involved in relational, episodic‐like memory that preserves both the spatial and the temporal dimensions of past events, could be a primitive feature of the vertebrate brain that has been conserved through evolution.

Relational and procedural memory systems in the goldfish brain revealed by trace and delay eyeblink-like conditioning

The presence of multiple memory systems supported by different neural substrata has been demonstrated in animal and human studies. In mammals, two variants of eyeblink classical conditioning, differing only in the temporal relationships between the conditioned stimulus (CS) and the unconditioned stimulus (US), have been widely used to study the neural substrata of these different memory systems. Delay conditioning, in which both stimuli coincide in time, depends on a non-relational memory system supported by the cerebellum and associated brainstem circuits. In contrast, trace conditioning, in which a stimulus-free time gap separates the CS and the US, requires a declarative or relational memory system, thus depending on forebrain structures in addition to the cerebellum. The distinction between the explicit or relational and the implicit or procedural memory systems that support trace and delay classical conditioning has been extensively studied in mammals, but studies in other vertebrate groups are relatively scarce. In the present experiment we analyzed the differential involvement of the cerebellum and the telencephalon in delay and trace eyeblink-like classical conditioning in goldfish. The results show that whereas the cerebellum lesion prevented the eyeblink-like conditioning in both procedures, the telencephalon ablation impaired exclusively the acquisition of the trace conditioning. These data showing that comparable neural systems support delay and trace eyeblink conditioning in teleost fish and mammals suggest that these separate memory systems and their neural bases could be a shared ancestral brain feature of the vertebrate lineage.