Combinatorial expression of Lef1, Lhx2, Lhx5, Lhx9, Lmo3, Lmo4, and Prox1 helps to identify comparable subdivisions in the developing hippocampal formation of mouse and chicken

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.

Section: Dynamic Pattern Of DLV Activation Across the Stages Of Spatimentioning

confidence: 99%

Dynamics of Goldfish Subregional Hippocampal Pallium Activity throughout Spatial Memory Formation

Ocaña

Uceda²,

Árias³

et al. 2017

“…The PHi, together with the hippocampus, in birds is considered the homologous region of the hippocampal complex in mammals [Abellan et al, 2014;reviews in Reiner et al, 2004;Striedter, 2005;Atoji and Wild, 2006;Papp et al, 2007]. During mouse development, the FoxP1 protein appears on E17.5 in the outer layers of the hippocampal complex [Ferland et al, 2003].…”

Section: Discussionmentioning

confidence: 99%

“…1 a, b). Abellan et al [2014] proposed a new rostral subdivision which could correspond to or include our PHiA at rostral levels. The PHi is a cortical structure, and at least 3 distinct layers have been described in the 5 parahippocampal subdivisions: the inner layer close to the ventricle, called the periventricular layer; the intermediate layer, also called the cortical plate, and the outer layer close to the pial surface, called the superficial layer.…”

Section: Foxp1 Expression Pattern In the Parahippocampal Domain Of Qumentioning

confidence: 99%

“…The PHi is subdivided into 5 radial subdomains which show a cortical structure [Redies et al, 2001, Kovjanic andRedies, 2003;Puelles et al, 2007;Garcia-Calero and Puelles, 2009]. Recently, Abellan et al [2014] added a new rostral subdivision in the chicken PHi. Differences in the molecular profile and cytoarchitecture of this region among species could shed light on the parahippocampal function in birds.…”

mentioning

confidence: 99%

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FoxP1 Protein Shows Differential Layer Expression in the Parahippocampal Domain among Bird Species

Garcı́a-Calero

2016

Different bird orders show diversity in neural capabilities supported by variations in brain morphology. The parahippocampal domain in the medial pallium, together with the hippocampus proper, plays an important role in memory skills. In the present work, we analyze the expression pattern of the FoxP1 protein in the parahippocampal area of four different bird species: the nonvocal learner birds quail and chicken (Galliformes) and two vocal learner birds, i.e. the zebra finch (Passeriformes) and the budgerigar (Psittaciformes), at different developmental and adult stages. We also analyze the expression of the calbindin protein in quails and zebra finches. We observed differences in the FoxP1 parahippocampal layer among bird species. In quails, chickens, and budgerigar, FoxP1 cells were located in the outer layers of the lateral and caudolateral parahippocampal sectors. In contrast, FoxP1 immunoreactive cells appeared in the inner layer of the same sectors in the zebra finch parahippocampal domain. These differences suggest two possibilities: either the FoxP1-positive cells described in quails, chickens, and budgerigars are a different population than the one described in the zebra finch, or there are changes in the pattern of radial migration in the parahippocampal area among birds. In the present study, we show that FoxP1 expression is more similar between quails, chickens, and budgerigars than between budgerigars and zebra finches in the parahippocampal area. This result contrasts with previous data in other telencephalic structures, like the calbindin-positive projection neurons described in the striatum of budgerigars and zebra finches but not in quails and chickens. All of these data point to diversity in the evolution of different morphological characters and, therefore, a mosaic model for telencephalic evolution in birds.

“…Briefly, it is one thing to ask the perfectly meaningful evolutionary question "what subdivision of the amphibian, reptile, or avian HF shares a common evolutionary origin with the dentate gyrus of the mammalian hippocampus?" [Abellán et al, 2014;Hevner, 2016]. By contrast, the question "what subdivision of the avian HF is dentate gyrus?"…”

mentioning

confidence: 97%

Reflections on the Structural-Functional Evolution of the Hippocampus: What Is the Big Deal about a Dentate Gyrus

Bingman

Muzio

2017

The vertebrate hippocampal formation has been central in discussions of comparative cognition, nurturing an interest in understanding the evolution of variation in hippocampal organization among vertebrate taxa and the functional consequences of that variation. Assuming some similarity between the medial pallium of extant amphibians and the hippocampus of stem tetrapods, we propose the hypothesis that the hippocampus of modern amniotes began with a medial pallium characterized by a relatively undifferentiated cytoarchitecture, more direct thalamic and olfactory sensory inputs, and a broad role in associative learning and memory processes that nonetheless included the map-like representation of space. From this modest beginning evolved the cognitively more specialized hippocampal formation of birds and the hippocampus of mammals with its confounding dentate gyrus. Much has been made of trying to identify a dentate homologue in birds, but there are compelling reasons to believe no such structural homologue/functional equivalent exists. The uniqueness of the mammalian dentate then raises the question of what might be the functional consequences of a hippocampus with a dentate compared to one without. One might be tempted to speculate that the presence of a dentate gyrus facilitates so-called pattern separation, but birds with their suspected dentate-less hippocampus display excellent hippocampal-dependent pattern separation relying on space. Perhaps one consequence of a dentate is a hippocampus better designed to process a broader array of stimuli beyond space to more robustly support episodic memory. What is clear is that any meaningful reconstruction of hippocampal evolution and the eventual identification of any subdivisional homologies will require more data on the neurobiological and functional properties of the nonmammalian hippocampus, particularly those of amphibians and reptiles.