Dynamics of Goldfish Subregional Hippocampal Pallium Activity throughout Spatial Memory Formation.

The teleost fish hippocampal pallium, like the hippocampus of tetrapods, is essential for relational map-like spatial memories. In mammals, these relational memories involve the dynamic interactions among different hippocampal subregions and between the hippocampus-neocortex network, which performs specialized operations such as memory encoding and retrieval. However, how the teleost hippocampal homologue operates to achieve comparably sophisticated spatial cognition capabilities is largely unknown. In the present study, the progressive changes in the metabolic activity of the pallial regions that have been proposed as possible homologues of the mammalian hippocampus were monitored in goldfish. Quantitative cytochrome oxidase histochemistry was used to measure the level of activation along the rostrocaudal axis of the ventral (Dlv) and dorsal parts of the dorsolateral division (Dld) and in the dorsoposterior division (Dp) of the goldfish telencephalic pallium throughout the time course of the learning process of a spatial memory task. The results revealed a significant increase in spatial memory-related metabolic activity in the Dlv, but not in the Dld, suggesting that the Dlv, but not the Dld, is comparable to the amniote hippocampus. Regarding the Dlv, the level of activation of the precommissural Dlv significantly increased at training onset but progressively declined to finally return to the basal pretraining level when the animals mastered the spatial task. In contrast, the commissural Dlv activation persisted even when the acquisition phase was completed and the animal's performance reached an asymptotic level. These results suggest that, like the dentate gyrus of mammals, the goldfish precommissural Dlv seems to respond nonlinearly to increments of change in sensory input, performing pattern separation under highly dissimilar input patterns. In addition, like the CA3 of mammals, the commissural Dlv likely operates in a continuum between two modes, a pattern separation or storage operation mode at early acquisition when the change in the sensory input is high, probably driven by the precommissural Dlv output, and a pattern completion or recall operation mode when the animals have mastered the task and the change in sensory input is small. Finally, an unexpected result of the present study is the persistent activation of the area Dp throughout the complete spatial task training period, which suggests that the Dp could be an important component of the pallial network involved in spatial memory in goldfish, and supports the hypothesis proposing that the Dp is a specialized part of the hippocampal pallium network.

The lamprey pallium provides a blueprint of the mammalian motor projections from cortex.

BACKGROUND: The frontal lobe control of movement in mammals has been thought to be a specific function primarily related to the layered neocortex with its efferent connections. In contrast, we now show that the same basic organization is present even in one of the phylogenetically oldest vertebrates, the lamprey. RESULTS: Stimulation of specific sites in the pallium/cortex evokes eye, trunk, locomotor, or oral movements. The pallial projection neurons target brainstem motor centers and basal ganglia subnuclei and have prominent dendrites extending into the outer molecular layer. They exhibit the characteristic features of pyramidal neurons and elicit monosynaptic glutamatergic excitatory postsynaptic potentials in output neurons of the optic tectum, reticulospinal neurons, and, as shown earlier, basal ganglia neurons. CONCLUSIONS: Our results demonstrate marked similarities in the efferent functional connectivity and control of motor behavior between the lamprey pallium and mammalian neocortex. Thus, the lamprey motor pallium/cortex represents an evolutionary blueprint of the corresponding mammalian system.

Cerebellum and spatial cognition in goldfish.

The cerebellum of mammals has recently been linked to spatial navigation, as indicated by the results of a number of studies performed in animal models with cerebellar abnormalities. However, nothing is known about the contribution of this structure to spatial cognition in other vertebrate groups such as teleost fish. To investigate the involvement of the teleostean cerebellum in navigation, sham-operated (Sh) and cerebellum-ablated (Cb) goldfish were trained in a "hole-board" task in which they had to locate the baited feeder within a 5×5 feeder matrix surrounded by visual cues. Cb goldfish were significantly impaired in the acquisition and performance of the task, as revealed by their low spatial accuracy, the number of errors committed, and the stereotyped searching pattern exhibited relative to Sh goldfish. Probe tests, performed during the final training sessions, showed that Cb animals could not integrate experimental cues into an internal representation of the environment (as an allocentric strategy would require) and they resorted to a guiding strategy to locate the goal. The results of this experiment demonstrated that the cerebellum might have a modulatory role in the declarative component of navigation by which an animal develops an internal spatial representation. Our results constitute the first evidence of the involvement of the fish cerebellum in spatial cognition. Our results also suggest that the cognitive functions of the cerebellum may have appeared early in vertebrate evolution and been conserved throughout the phylogenetic history of extant vertebrates.

Lateral but not medial telencephalic pallium ablation impairs the use of goldfish spatial allocentric strategies in a "hole-board" task.

Strong evidence suggests that the ventral region of the lateral telencephalic pallium of teleost fish, a structure involved in allocentric spatial cognition, is homologous to the hippocampus of tetrapods. This homology was first proposed on basis of anatomical data, and subsequently confirmed by developmental, functional and behavioural studies. Nonetheless, Saito and Watanabe [30,32] claim that not the lateral but, rather, the medial pallium participates in goldfish spatial navigation and should be considered the homologue of the hippocampus. Here, we further investigate the effects of selective pallial lesions on the spatial cognition abilities of goldfish, trained in a "hole-board" analogue task, to find the baited feeder within a 5 x 5 feeder matrix surrounded by visual cues. The task in the present experiment is similar to that used by Saito and Watanabe, but including thorough probe tests that enabled to define clearly the spatial strategies employed by the animals, and, therefore, the spatial deficits caused by the pallial lesions. The results showed that the lateral, but not the medial pallium lesions, produced a dramatic impairment in the implementation of allocentric spatial strategies. Thus, only lateral pallium lesioned goldfish, like hippocampus lesioned tetrapods, failed to reach the goal when the cues in its proximity were excluded, indicating that they used a guidance strategy. These results do not replicate Saito and Watanabe's, but are consistent to previous data indicating a close functional similarity between the lateral pallium of teleost fish and the hippocampus of amniotes.

Telencephalon ablation impairs goldfish allocentric spatial learning in a "hole-board" task.

The present work analyzes the involvement of telencephalon of goldfish in spatial strategies, using a procedure analogue to the hole-board task. With this aim, goldfish with sham operation or telencephalon ablation were trained to find a baited feeder within a twenty-five feeder matrix, which maintained stable spatial relationships relative to five peripheral landmarks. After training, different types of probe tests were conducted. Although both groups learned the task, probe trials showed that whereas the sham animals used the whole configuration of cues to implement map-like strategies the telencephalic animals used a guidance strategy based on cues located in the vicinity of the baited feeder. These results confirm the role of teleost fish telencephalon in the use of allocentric strategies obtained with other spatial procedures, and indicate that the hole-board task described here for goldfish is a useful tool to assess the neural bases of spatial cognition in teleost fish.

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.