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The Hippocampus Via Subiculum Upon Exposure to Desiccation

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The Hippocampus Via Subiculum Upon Exposure to Desiccation Current Biology Magazine Where next for the study of Primer anhydrobiosis? Studies have largely Direct and relied on detecting gene upregulation The hippocampus via subiculum upon exposure to desiccation. CA1 This approach will fail to identify constitutively expresssed genes that James J. Knierim DG CA2 are important for anhydrobiotic survival but whose expression does not change The hippocampus is one of the most EC CA3 during desiccation and rehydration. thoroughly investigated structures in axons We still do not understand why some the brain. Ever since the 1957 report nematodes, for example, do not of the case study H.M., who famously survive desiccation, while others can lost the ability to form new, declarative Current Biology survive immediate exposure to extreme memories after surgical removal of the desiccation, and yet others require hippocampus and nearby temporal Figure 1. Coronal slice through the trans- verse axis of the hippocampus. preconditioning at a high relative lobe structures to treat intractable The black lines trace the classic ‘trisynaptic humidity. A comparative approach epilepsy, the hippocampus has been loop’. The red lines depict other important is likely to be informative, as has at the forefront of research into the pathways in the hippocampus, including the recently been published comparing neurobiological bases of memory. direct projections from entorhinal cortex (EC) to the genomes of P. vanderplanki and its This research led to the discovery all three CA fi elds, the feedback to the EC via desiccation-intolerant relative P. nubifer. in the hippocampus of long-term the subiculum, the recurrent collateral circuitry of CA3, and the feedback projection from CA3 potentiation, the pre-eminent model to DG. For simplicity, many other details of the Where can I fi nd out more? of the cellular basis of memory. connectivity of the hippocampus are omitted. Barrett, J. (1982). Metabolic responses to Furthermore, the discovery of place anabiosis in the fourth stage juveniles of Ditylenchus dipsaci (Nematoda). Proc. R. Soc. cells, head direction cells, and grid within the medial temporal lobe. Its Lond. B. 216, 159–177. cells in the rodent hippocampal resemblance in gross dissection to a Boschetti, C., Pouchkina-Stantcheva, N., formation established a fi rm seahorse inspired its naming after this Hoffmann, P., and Tunnacliffe, A. (2011). Foreign genes and novel hydrophilic protein foundation for the notion that the sea creature (genus Hippocampus). genes participate in the desiccation response hippocampus plays a critical role in In rodents, the hippocampus is a of the bdelloid rotifer Adineta ricciae. J. Exp. Biol. 214, 59–68. memory formation by providing the relatively large, cashew-shaped Crowe, J.H. (2014). Anhydrobiosis: an unsolved brain with a spatiotemporal framework structure lying just beneath the problem. Plant Cell Environ. 37, 1491–1493. within which the various sensory, neocortex. A cross-section of its long Erkut, C., and Kurzchalia, T.V. (2015). The C. elegans dauer larva as a paradigm to study emotional, and cognitive components axis reveals the classic, textbook metabolic suppression and desiccation of an experience are bound together. depiction of the hippocampal tolerance. Planta 242, 389–396. This framework allows the experience anatomical connectivity, the so-called Gusev, O., Suetsugu, Y., Cornette, R., Kawashima, T., Logacheva, M.D., Kondrashov, to be stored in such a way that it ‘trisynaptic loop’ (Figure 1). The A.S., Penin, A.A., Hatanaka, R., Kikuta, can be later retrieved as a conscious entorhinal cortex provides the major S., Shimura, S., et al. (2014). Comparative recollection of that experience. cortical input to the hippocampus, genome sequencing reveals genomic signature of extreme desiccation tolerance in the In this primer, I will fi rst review the with its strongest projections via the anhydrobiotic midge. Nat. Commun. 5, 4784. basic anatomy of the hippocampus, perforant path to the dentate gyrus Perry, R.N., and Wharton, D.A. (2011). Molecular and Physiological Basis of Nematode Survival giving a historical overview of early (DG) region (Synapse 1). The DG (CABI Publishing, Wallingford). conceptions of hippocampal circuitry projects to the CA3 region via the Potts, M., Slaughter, S.M., Hunneke, F.U., Garst, and describing modern fi ndings that mossy fi ber pathway (Synapse 2). J.F., and Helm, R.F. (2005). Desiccation tolerance of prokaryotes: Application of are the inspiration of much current CA3 projects to the CA1 region via the principles to human cells. Integr. Comp. Biol. work on hippocampal physiology Schaffer Collateral pathway (Synapse 45, 800–809. and function. Next, I will consider 3). Finally, CA1 projects back to the Tyson, T., O’Mahony Zamora, G., Wong, S., Skelton, M., Daly, B., Jones, J.T., human and animal lesion studies, the entorhinal cortex, completing the loop. Mulvihill, E.D., Elsworth, B., Phillips, M., results of which underlie our basic An important addition to the classic Blaxter, M., et al. (2012). A molecular analysis understanding that the hippocampus trisynaptic circuitry is that CA3 axons, of desiccation tolerance mechanisms in the anhydrobiotic nematode Panagrolaimus performs a critical function in the in addition to their projections to CA1, superbus using expressed sequence tags. brain’s ability to store and retrieve send collaterals that make synapses BMC Res. Notes 5, 68. Wang, C., Grohme, M.A., Mali, B., Schill, R.O., memories (particularly episodic onto other CA3 neurons. This and Frohme, M. (2014). Towards decrypting memories in humans). Finally, I will recurrent collateral pathway inspired a cryptobiosis - analyzing anhydrobiosis in review key aspects of hippocampal number of infl uential theories of CA3 the tardigrade Milnesium tardigradum using transcriptome sequencing. PLoS One 9, http:// behavioral neurophysiology and as an autoassociative memory system, dx.doi.org/10.1371/journal.pone.0092663. relate them to current theories of displaying attractor dynamics that are Wharton, D.A. (2002). Life at the Limits: Organisms hippocampal function. critical for supporting a distributed in Extreme Environments (Cambridge University Press, Cambridge). memory. Anatomy The unidirectional circuitry of Department of Zoology, University of Otago, Intrinsic circuitry the trisynaptic loop was originally P.O. Box 56, Dunedin, New Zealand. In humans, the hippocampus is an believed to be mainly contained *E-mail: [email protected] elongated structure buried deep within a cross-sectional slice (or R1116 Current Biology 25, R1107–R1125, December 7, 2015 ©2015 Elsevier Ltd All rights reserved Current Biology Magazine lamella) of the hippocampus. The input from LEC and the part of CA1 posterior orientation. The anterior ‘lamellar hypothesis’ proposed that close to CA2 receives input from hippocampus of primates corresponds the hippocampus was structured as MEC. The superfi cial layers of MEC to the ventral hippocampus of rodents, a stack of these lamellae, organized and LEC project to the hippocampus and the posterior hippocampus of as independent, functional modules (in general, layer II projects to DG primates corresponds to the dorsal along the longitudinal axis of the and CA3, whereas layer III projects hippocampus of rodents. In rodents, hippocampus. Modern anatomical to CA1 and subiculum). The deep the dorsal hippocampus and ventral tracing studies, however, have layers receive feedback from the hippocampus are differentially revealed widespread connectivity hippocampus. Connections from deep involved in spatial versus emotional along the longitudinal axis, showing to superfi cial layers, as well as the memory and cognition. Because most that transverse slices (cross- presence of basal dendrites of layer single unit recording studies and sections, as in Figure 1) through the II/III neurons in deep layers, form a many lesion studies in rodents are hippocampus are not functionally critical anatomical feedback loop that performed on dorsal hippocampus, independent. The connectivity within allows the hippocampal output to and many primate studies concentrate the transverse axis is also more directly affect the neural processing of on the anterior hippocampus (the complex, with multiple, parallel the hippocampal inputs. homolog of ventral hippocampus in processing circuits and feedback rodents), data that appear to show circuits. The entorhinal cortex projects Other cortical and subcortical species differences between rodents not only to DG, but also directly to the connections and primates may actually refl ect CA3 and CA1 regions. CA3 provides In addition to the major inputs differences between the computational a feedback projection to the DG, from the entorhinal cortex, the processes of dorsal (posterior) via the excitatory mossy cells of the hippocampus receives direct inputs hippocampus versus ventral (anterior) dentate hilus, thus violating the earlier from the perirhinal cortex and hippocampus. notion that hippocampal processing postrhinal cortex. It also receives is exclusively unidirectional. Finally, major subcortical inputs from the Hippocampal lesions recent experiments have fostered medial septum (related to the strong Human studies a new appreciation of the CA2 theta rhythm in the hippocampus), There is a rich literature on the region, which has traditionally been locus coeruleus, raphe nucleus, amnesic effects of hippocampal considered a transition zone between nucleus reuniens, and amygdala. damage in humans. The hippocampus
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