The Hippocampus of Nonmammalian Vertebrates

Bingman, Verner P.; Rodrı́guez, Fernando; Salas, Cosme

doi:10.1016/b978-0-12-804042-3.00013-0

Cited by 13 publications

(10 citation statements)

References 95 publications

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“…We focus on two classic questions [Smith, 1910]: (i) how much of the reptilian cortex represents the hippocampal formation, and (ii) what is its nature, i.e., what are its subdivisions and functional specializations? For studies on cortical volume changes in relation to spatial navigation [Day et al, 1999;Ladage et al, 2009] we direct the reader to excellent reviews that also incorporate a broader phylogenetic perspective [Roth et al, 2010;Broglio et al, 2015;Murray et al, 2016;Striedter, 2016;Bingman et al, 2017]. Similarly, we omit studies on cortical interneurons in reptiles [reviewed in Reiner, 1991;Guirado and Davila, 1999;Naumann and Laurent, 2017], since, despite extensive knowledge about cell type diversity of mammalian hippocampal interneurons, their function remains poorly understood [Grieves and Jeffery, 2017].…”

Section: The Hippocampus In Pieces and Patchesmentioning

confidence: 99%

“…In turtles, zinc-positive intrinsic connections may be missing , and the cytoarchitecture is dramatically less distinct. We propose that the indistinct cellular architecture of turtle medial cortex exemplifies a trend that is amplified in their close relatives, crocodiles and birds [Craigie, 1935], leading to the question as to whether birds have any medial cortex region similar to the dentate gyrus at all [Striedter, 2016;Bingman et al, 2017].…”

Section: The Hippocampus In Pieces and Patchesmentioning

confidence: 99%

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On the Value of Reptilian Brains to Map the Evolution of the Hippocampal Formation

Reiter

Liaw²,

Yamawaki³

et al. 2017

Brain Behav Evol

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Our ability to navigate through the world depends on the function of the hippocampus. This old cortical structure plays a critical role in spatial navigation in mammals and in a variety of processes, including declarative and episodic memory and social behavior. Intense research has revealed much about hippocampal anatomy, physiology, and computation; yet, even intensely studied phenomena such as the shaping of place cell activity or the function of hippocampal firing patterns during sleep remain incompletely understood. Interestingly, while the hippocampus may be a ‘higher order' area linked to a complex cortical hierarchy in mammals, it is an old cortical structure in evolutionary terms. The reptilian cortex, structurally much simpler than the mammalian cortex and hippocampus, therefore presents a good alternative model for exploring hippocampal function. Here, we trace common patterns in the evolution of the hippocampus of reptiles and mammals and ask which parts can be profitably compared to understand functional principles. In addition, we describe a selection of the highly diverse repertoire of reptilian behaviors to illustrate the value of a comparative approach towards understanding hippocampal function.

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Section: The Hippocampus In Pieces and Patchesmentioning

confidence: 99%

Section: The Hippocampus In Pieces and Patchesmentioning

confidence: 99%

On the Value of Reptilian Brains to Map the Evolution of the Hippocampal Formation

Reiter

Liaw²,

Yamawaki³

et al. 2017

Brain Behav Evol

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“…Given the considerable variation in tetrapod hippocampal neural organization ( Fig. 1 ) [Bingman et al, , 2017Herold et al, 2015;Striedter, 2016], this unifying functional descriptor is perhaps somewhat surprising. The question raised then is, during the course of evolution, what differences in the functional profile of the hippocampus may have accumulated as divergent evolutionary lineages acquired their unique hippocampal features ( Fig.…”

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

confidence: 99%

“…The binding functional descriptor of the tetrapod hippocampus, as well as its presumptive homologue in teleost fish [Rodríguez et al, 2002], is some role in the maplike representation of space used to guide navigation and provide a spatial context to support memory [Bingman et al, , 2017Herold et al, 2015]. Given the considerable variation in tetrapod hippocampal neural organization ( Fig.…”

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

confidence: 99%

“…The functional characterization of HF in nonmammalian tetrapods naturally led to anatomical interest in drawing finer-scale homologies between subdivisions of the hippocampus, i.e., dentate gyrus, CA subfields of Ammon's horn, subiculum, and neighboring entorhinal cortex, with distinct anatomical subdivisions of the HF of birds as well as other nonmammalian tetrapods. In our opinion, this search for strict subdivisional homologies has been a dissatisfying distraction from more fundamental and interesting questions of hippocampal evolution and how variation in hippocampal organization relates to variation in natural history, selective pressure, and function [Bingman et al, 2017]. It is noteworthy that the search for mammalian subdivisions in the avian HF was done without anyone ever really considering nuances in how the term "homology" should be understood.…”

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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

Brain Behav Evol

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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.

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The avian hippocampus and the hypothetical maps used by navigating migratory birds (with some reflection on compasses and migratory restlessness)

Bingman

MacDougall‐Shackleton

2017

J Comp Physiol A

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The homology between the avian hippocampal formation (HF) and mammalian hippocampus nurtures the expectation that HF plays a fundamental role in navigation by migratory birds. Indeed, HF of migratory birds displays anatomical properties that differ from non-migratory species. Using a hypothetical framework of multiple maps of differing spatial resolution and range, homing pigeon data suggest that HF is important for navigating by landscape features near familiar breeding, over-wintering, and stop-over sites. By contrast, HF would be unimportant for an olfactory navigational map, which could be operational over unfamiliar space farther away from a goal location, nor is there any evidence for HF involvement in the sun or geomagnetic compass. The most intriguing question that remains open is what role HF may play in navigation when a migrant is thousands kms away from a familiar area, where homing pigeon data are uninformative and a geomagnetic map may be operational. Beyond navigation, successful migration depends on seasonal timing and often becoming nocturnally active. There is little evidence that HF plays a role in the timing of circannual and circadian cycles. Rather, circadian pacemakers including the pineal gland may control circadian timing of nocturnal restlessness and photoperiodic seasonal pacemakers likely control circannual expression.

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The Hippocampus of Nonmammalian Vertebrates

Cited by 13 publications

References 95 publications

On the Value of Reptilian Brains to Map the Evolution of the Hippocampal Formation

On the Value of Reptilian Brains to Map the Evolution of the Hippocampal Formation

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

The avian hippocampus and the hypothetical maps used by navigating migratory birds (with some reflection on compasses and migratory restlessness)

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