Cristina Broglio

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.

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.

Multiple spatial learning strategies in goldfish (Carassius auratus)

Abstract There is a considerable amount of evidence that mammals and birds can use different spatial learning strategies based on multiple learning and memory systems. Unfortunately, only a few studies have investigated spatial learning and memory mechanisms in other vertebrates. This study aimed to identify the strategies used by goldfish to solve two different spatial tasks in a series of three experiments. In experiment 1, two groups of goldfish (Carassius auratus) were trained either in a spatial constancy task (SC), in which visual cues signalled the goal indirectly, or in a directly cued task (DC) in which similar cues signalled the goal directly. Transfer tests were conducted to study the effects of discrete cue deletion on the performance in both tasks. In these transfer tests the performance of the animals trained in the DC task dropped to chance level when the cue that signalled the goal directly was removed. In contrast, the removal of any single cue did not disrupt SC performance. In experiment 2, fish trained in the SC or the DC task were trained with the goal reversed. Goldfish in the SC group needed fewer sessions to master the reversal task than DC animals. Finally, experiment 3 investigated the effects of a substantial modification of the geometrical features of the apparatus on the performance of animals trained in the SC or in the DC condition. The performance of DC goldfish was not affected, whereas the same change disrupted performance in the SC animals despite the presence of the visual cues. These results suggest that there are separate spatial learning and memory systems in fish. Whereas the DC animals used a typical guidance strategy, relying only on the cue that signalled the goal directly, SC fish relied on a strategy with the properties of an actual spatial mapping system. Thus, the comparative approach points to the generality of these learning strategies among vertebrates.

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.

Spatial learning in turtles

Abstract. Turtles (Pseudemys scripta) were trained in place, cue and control open-field procedures. The turtles trained in both the place and the cue procedures were able to learn their respective tasks with accuracy. Subsequent probe tests revealed that the turtles trained in the place task relied on the information provided by the extramaze cues to locate the goal. However, for these animals, no single cue was essential for performance, as accurate navigation to the goal was still possible when subsets of extramaze cues were eliminated. Furthermore, the turtles trained in the place task were able to navigate accurately to the goal place from new start locations. These results suggest that the turtles trained in the place task used map-like, relational strategies, by encoding the simultaneous spatial relationships between the goal and the extramaze cues in an allocentric frame of reference. In contrast, the turtles trained in the cue procedure used guidance strategies, i.e. approaching the individual intramaze cue associated to the goal as it were a beacon and largely ignoring the extramaze cues. Thus, the results of this experiment suggest that turtles are able to employ spatial strategies that closely parallel those described in mammals and birds.

Place and cue learning in turtles

Turtles (Pseudemys scripta) were trained in place, cue, and control arm maze procedures. The turtles learned both tasks with accuracy. Subsequent probe and transfer trials revealed guidance and mapping strategies by the cue and the place groups, respectively. Thus, the turtles in the cue procedure solved their task by directly approaching the single individual intramaze cue associated with the goal, whereas the animals in the place task seemed to be using a maplike representation based on the encoding of simultaneous spatial relationships between the goal and the extramaze visual cues. Furthermore, the turtles in the place task were able to navigate with accuracy to the goal from unfamiliar start places, and their performance was resistant to a partial loss of relevant environmental information. The results reveal for the first time, to our knowledge, spatial learning and memory capabilities in a reptile that closely parallel those described in mammals and birds.

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.