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

Uceda, Sara; Ocaña, Francisco M.; Martín-Monzón, Isabel; Rodríguez-Expósito, B.; Durán, Emilio; Rodrı́guez, Fernando

doi:10.1016/j.bbr.2015.06.018

Cited by 31 publications

(26 citation statements)

References 61 publications

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Section: Introductionmentioning

confidence: 99%

“…Remarkably, the teleost fish hippocampal homologue, like the hippocampus of tetrapods, is also essential for map-like spatial memory [Vargas et al, 2000;Rodríguez et al, 2002;Broglio et al, 2010;Durán et al, 2010;Uceda et al, 2015]. For example, morphofunctional studies have revealed selective spatial memory-related increases in metabolic activity [Uceda et al, 2015] and in protein synthesis [Vargas et al, 2000;Broglio et al, 2010] in the neurons of the hippocampal pallium of goldfish trained in spatial tasks. In addition, it has been demonstrated that, as in mammals and birds, hippocampal pallium lesions in goldfish produce severe performance impairments in a variety of spatial learning tasks requiring allocentric, relational spatial memory strategies, but not when the task can be solved by means of nonrelational, egocentric strategies or nonspatial discriminations [Rodríguez et al, 2002;Broglio et al, 2010;Durán et al, 2010].…”

Section: Introductionmentioning

confidence: 99%

“…Since CO is a mitochondrial enzyme involved in the generation of ATP associated with cell metabolic demands, and therefore in neuronal activation, CO histochemistry is a useful tool for indexing regional functional activity in the brain [WongRiley, 1989;González-Lima and Cada, 1994]. In particular, it is useful for identifying activity changes induced by learning [Poremba et al, 1998;Conejo et al, 2010;Uceda et al, 2015]. CO histochemistry mapping has been used in mammals along with other functional brain mapping techniques, such as 14 C-2-deoxyglucose autoradiography and immediate-early-gene activation, to identify the brain structures engaged in the different phases of memory formation, contributing significantly to the identification of the hippocampus-cortical functional circuits relevant to the encoding and retrieval of spatial memories [Bontempi et al, 1999;Vazdarjanova and Guzowski, 2004;Poirier et al, 2008;Conejo et al, 2010].…”

Section: Introductionmentioning

confidence: 99%

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Dynamics of Goldfish Subregional Hippocampal Pallium Activity throughout Spatial Memory Formation

Ocaña

Uceda²,

Árias³

et al. 2017

Brain Behav Evol

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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.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Dynamics of Goldfish Subregional Hippocampal Pallium Activity throughout Spatial Memory Formation

Ocaña

Uceda²,

Árias³

et al. 2017

Brain Behav Evol

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“…The topologically corresponding parts of the brain in goldfish likewise support these same tasks: Dlv is involved in allocentric spatial learning, despite its lack of morphological features in common with the hippocampus in amniotes. The midbrain roof, which exhibits at least some morphological features in common with amniotes, is involved in egocentric spatial mapping, and Dm is involved in emotional learning and memory [Durán et al, 2002;Rodríguez et al, 2002;Salas et al, 2003;Portavella et al, 2004;Broglio et al, 2005;Broglio et al, 2010;Durán et al, 2010;Uceda et al, 2015], despite its lack of morphological similarity to the amniote amygdala.…”

Section: Medial Pallium In Actinopterygian Fishesmentioning

confidence: 99%

Of Horse-Caterpillars and Homologies: Evolution of the Hippocampus and Its Name

Butler

2017

Brain Behav Evol

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The hippocampus was first named in mammals based on the appearance of its gross morphological features, one end of it being fancied to resemble the head of a horse and the rest of it a silkworm, or caterpillar. A hippocampus, occupying the most medial part of the telencephalic pallium, has subsequently been identified in diverse nonmammalian taxa, but in which the “horse-caterpillar” morphology is lacking. While some strikingly similar functional similarities have been identified, questions of its homology (“sameness”) across these taxa and about the very fundamental relationship of structure to function in central nervous system structures remain open. The hippocampal formation of amniotes participates in allocentric (external landmark) spatial navigation, memory, and attention to novel stimuli, and these functions generally are shared across amniotes despite variation in its morphological features. Substantially greater deviation in its morphology occurs in anamniotes, including amphibians and ray-finned fishes (actinopterygians), but its functions of allocentric spatial navigation and/or memory have been found to be preserved by studies in these taxa. Its shared functional roles cannot be used as evidence of structural homology, but given that other criteria indicate homology of the medial pallial derivative across these clades, the similar functions themselves may be regarded as homologous functions if they are based on the same cellular mechanisms and connections. The question arises as to whether the similar functions are performed by as yet undiscovered, shared morphological features or by different features that accomplish the same results via different mechanisms of neural function.

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“…Training goldfish in the spatial constancy task (but not in a cued version of the same task) produces an increase in the synthesis of proteins that is selective to the neurons of Dlv [76] [79] (Figure 4C), as indicated by the enlargement of the nucleolar organizing regions (the organelles associated with the synthesis of ribosomal proteins) [80]. Cytochrome oxidase histochemistry, an approach that permits to determine the brain regions undergoing long-term training-dependent metabolic changes [81]- [84], shows that training goldfish in the spatial constancy task increases the activity in Dlv but not in Dld [85]. Consistent data obtained in neuroecological studies show that increased spatial behavior demands correlate with larger Dlv in several species of teleost fishes [86] [87].…”

Section: Map-like Memories and Hippocampal Pallium In Anamniotesmentioning

confidence: 99%

Hippocampal Pallium and Map-Like Memories through Vertebrate Evolution

Broglio¹,

Martín-Monzón²,

Ocaña³

et al. 2015

JBBS

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The hippocampus in humans and other mammals is essential for episodic and relational memories. Comparative evidence indicates that a hippocampal pallium homologue is present in birds, reptiles, amphibians, ray-finned fishes, cartilaginous fishes and agnathans. Some of their characteristics, such as the topological position and the pattern of connectivity, appear remarkably well conserved. We review here substantial data showing that in all the vertebrate groups studied up to date, from fish to mammals, the hippocampus plays a fundamental role in spatial memory. In these vertebrates groups, the hippocampal pallium homologue is involved in the use of map-like, relational representations of the objective space that provide stable allocentric frames of reference, thus allowing flexible navigation. These similarities suggest a common evolutionary ancestry and indicate that the functional properties of the hippocampus appear early in the vertebrate phylogenesis and are retained through the independent evolution of the vertebrate lineages.

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

Cited by 31 publications

References 61 publications

Dynamics of Goldfish Subregional Hippocampal Pallium Activity throughout Spatial Memory Formation

Dynamics of Goldfish Subregional Hippocampal Pallium Activity throughout Spatial Memory Formation

Of Horse-Caterpillars and Homologies: Evolution of the Hippocampus and Its Name

Hippocampal Pallium and Map-Like Memories through Vertebrate Evolution

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