Telencephalic Neuronal Activation Associated with Spatial Memory in the Terrestrial Toad &lt;b&gt;&lt;i&gt;Rhinella arenarum:&lt;/i&gt;&lt;/b&gt; Participation of the Medial Pallium during Navigation by Geometry

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.

Section: Medial Pallium In Amphibiansmentioning

confidence: 99%

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

Butler

2017

“…The essential role of the hippocampus is particularly noteworthy in tasks that demand encoding of multiple elements and their spatial relationships across different individual episodes in an allocentric internal representation of the space (cognitive map) or requiring a flexible expression of spatial knowledge [O'Keefe and Nadel, 1978;Hartley et al, 2014]. Also, the hippocampal homologue of birds [Sherry and Duff, 1996;Colombo and Broadbent, 2000;Bingman and Sharp, 2006], reptiles [Rodríguez et al, 2002;López et al, 2003;Salas et al, 2003;Holding et al, 2012], and probably amphibians [Sotelo et al, 2016] is consistently involved in map-like spatial memory. From an evolutionary perspective, the similarities in neural mechanisms and functions of the hippocampus across tetrapod taxa could be indicative of a long shared neurobiological ancestry.…”

Section: Introductionmentioning

confidence: 99%

Dynamics of Goldfish Subregional Hippocampal Pallium Activity throughout Spatial Memory Formation

Ocaña

Uceda²,

Árias³

et al. 2017

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.

“…Hippocampal involvement in the representation of environmental geometry has been described in a wide variety of vertebrate groups [see Sotelo et al, 2016 for a summary]. Therefore, the medial pallium-boundary geometry coupling found in the terrestrial toad reinforces an inferred ancestral role of the hippocampus in spatial cognition.…”

Section: The Stem Hippocampus: Looking To the Medial Pallium Of Extenmentioning

confidence: 85%

“…In a seminal study, Sotelo et al [2015Sotelo et al [ , 2016 demonstrated in the terrestrial toad, Rhinella arenarum , that locating a goal location using the boundary geometry of a rectangular arena resulted in an upregulation of the immediate-early gene c-fos in the medial pallium. Hippocampal involvement in the representation of environmental geometry has been described in a wide variety of vertebrate groups [see Sotelo et al, 2016 for a summary].…”

Section: The Stem Hippocampus: Looking To the Medial Pallium Of Extenmentioning

confidence: 99%

“…The less developed telencephalon may explain in part why the medial pallium receives numerous direct/less-processed sensory inputs. As such, the medial pallium of the ancestral amphibian, like extant ones, can be considered almost the brain's "seat of cognition," controlling not only map-like representations of space but also more general aspects of simple associative/instrumental learning and memory (although it is worth noting here that the lateral pallium of the terrestrial toad has been implicated in feature-reward learning [Sotelo et al, 2016]). …”

Section: A Hypothetical Reconstruction Of Hippocampal Structural-funcmentioning

confidence: 99%

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

Bingman

Muzio

2017

Self Cite

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.