Interdependence Between Dorsal and Ventral Hippocampus During Spatial Navigation

Overview

Journal Brain Behav

Specialty Psychology

Date 2019 Oct 2

PMID 31571397

Citations 11

Authors

Shang Lin Tommy Lee

Dana Lew

Victoria Wickenheisser

Etan J Markus

Affiliations

Soon will be listed here.

Abstract

Introduction: The hippocampus is linked to the formation and retrieval of episodic memories and spatial navigation. In rats, it is an elongated structure divided into dorsal (septal) and ventral (temporal) regions paralleling the respective division in the posterior and anterior hippocampus in humans. The dorsal hippocampus has been suggested to be more important for spatial processing and the ventral to processing anxiety-based behaviors. Far less is known regarding the degree to which these different regions interact during information processing. The anatomical connectivity suggests a flow of information between the dorsal and ventral regions; conversely, there are also commissural connections to the contralateral hippocampus. The current study examined the extent to which information from the dorsal hippocampus interacts with processing in the ipsilateral and contralateral ventral hippocampus following the acquisition of a spatial task.

Methods: Rats were well-trained on a spatial reference version of the water maze, followed by muscimol inactivation of different hippocampal subregions in a within-animal repeated design. Various combinations of bilateral, ipsilateral, and contralateral infusions were used.

Results: Combined dorsal and ventral inactivation produced a severe impairment in spatial performance. Inactivation of only the dorsal or ventral regions resulted in intermediate impairment with performance levels falling between controls and combined inactivation. Performance was impaired during contralateral inactivation and was almost equivalent to bilateral dorsal and ventral hippocampus inactivation, while ipsilateral inactivation resulted in little impairment.

Conclusions: Taken together, results indicate that for spatial processing, the hippocampus functions as a single integrated structure along the longitudinal axis.

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References

Fenton A, Arolfo M, Nerad L, Bures J . Interhippocampal synthesis of lateralized place navigation engrams. Hippocampus. 1995; 5(1):16-24. DOI: 10.1002/hipo.450050104. View

Chrobak J, Stackman R, Walsh T . Intraseptal administration of muscimol produces dose-dependent memory impairments in the rat. Behav Neural Biol. 1989; 52(3):357-69. DOI: 10.1016/s0163-1047(89)90472-x. View

Witter M, Naber P, van Haeften T, Machielsen W, Rombouts S, Barkhof F . Cortico-hippocampal communication by way of parallel parahippocampal-subicular pathways. Hippocampus. 2000; 10(4):398-410. DOI: 10.1002/1098-1063(2000)10:4<398::AID-HIPO6>3.0.CO;2-K. View

Li X, Somogyi P, Ylinen A, Buzsaki G . The hippocampal CA3 network: an in vivo intracellular labeling study. J Comp Neurol. 1994; 339(2):181-208. DOI: 10.1002/cne.903390204. View

Zou L, Yamada K, Sasa M, Nabeshima T . Two phases of behavioral plasticity in rats following unilateral excitotoxic lesion of the hippocampus. Neuroscience. 1999; 92(3):819-26. DOI: 10.1016/s0306-4522(99)00029-9. View

Kjelstrup K, Solstad T, Brun V, Hafting T, Leutgeb S, Witter M . Finite scale of spatial representation in the hippocampus. Science. 2008; 321(5885):140-3. DOI: 10.1126/science.1157086. View

Swanson L, Sawchenko P, Cowan W . Evidence that the commissural, associational and septal projections of the regio inferior of the hippocampus arise from the same neurons. Brain Res. 1980; 197(1):207-12. DOI: 10.1016/0006-8993(80)90446-1. View

de Hoz L, Martin S . Double dissociation between the contributions of the septal and temporal hippocampus to spatial learning: the role of prior experience. Hippocampus. 2014; 24(8):990-1005. DOI: 10.1002/hipo.22285. View

McEown K, Treit D . Inactivation of the dorsal or ventral hippocampus with muscimol differentially affects fear and memory. Brain Res. 2010; 1353:145-51. DOI: 10.1016/j.brainres.2010.07.030. View

10.

Gottlieb D, Cowan W . Autoradiographic studies of the commissural and ipsilateral association connection of the hippocampus and detentate gyrus of the rat. I. The commissural connections. J Comp Neurol. 1973; 149(4):393-422. DOI: 10.1002/cne.901490402. View

11.

van Groen T, Wyss J . Extrinsic projections from area CA1 of the rat hippocampus: olfactory, cortical, subcortical, and bilateral hippocampal formation projections. J Comp Neurol. 1990; 302(3):515-28. DOI: 10.1002/cne.903020308. View

12.

Witter M, Groenewegen H . Laminar origin and septotemporal distribution of entorhinal and perirhinal projections to the hippocampus in the cat. J Comp Neurol. 1984; 224(3):371-85. DOI: 10.1002/cne.902240305. View

13.

Turner D, Li X, Pyapali G, Ylinen A, Buzsaki G . Morphometric and electrical properties of reconstructed hippocampal CA3 neurons recorded in vivo. J Comp Neurol. 1995; 356(4):580-94. DOI: 10.1002/cne.903560408. View

14.

Ishizuka N, Weber J, Amaral D . Organization of intrahippocampal projections originating from CA3 pyramidal cells in the rat. J Comp Neurol. 1990; 295(4):580-623. DOI: 10.1002/cne.902950407. View

15.

Fanselow M, Dong H . Are the dorsal and ventral hippocampus functionally distinct structures?. Neuron. 2010; 65(1):7-19. PMC: 2822727. DOI: 10.1016/j.neuron.2009.11.031. View

16.

Floresco S, Seamans J, Phillips A . Differential effects of lidocaine infusions into the ventral CA1/subiculum or the nucleus accumbens on the acquisition and retention of spatial information. Behav Brain Res. 1996; 81(1-2):163-71. DOI: 10.1016/s0166-4328(96)00058-7. View

17.

Witter M . Intrinsic and extrinsic wiring of CA3: indications for connectional heterogeneity. Learn Mem. 2007; 14(11):705-13. DOI: 10.1101/lm.725207. View

18.

Groenewegen H, te Kortschot A, Witter M . Organization of the projections from the subiculum to the ventral striatum in the rat. A study using anterograde transport of Phaseolus vulgaris leucoagglutinin. Neuroscience. 1987; 23(1):103-20. DOI: 10.1016/0306-4522(87)90275-2. View

19.

Kesner R, Hunsaker M, Ziegler W . The role of the dorsal and ventral hippocampus in olfactory working memory. Neurobiol Learn Mem. 2011; 96(2):361-6. DOI: 10.1016/j.nlm.2011.06.011. View

20.

Vorhees C, Williams M . Morris water maze: procedures for assessing spatial and related forms of learning and memory. Nat Protoc. 2007; 1(2):848-58. PMC: 2895266. DOI: 10.1038/nprot.2006.116. View