Abstract
Evidence from several study techniques has provided substantial support to suggest that the hippocampus (HPP) plays an important role in learning and memory, which has been generally accepted by the scientific community. Dorsoventral lesion studies of the HPP, along with electrophysiological and other methods, have indicated that the dorsal axis of the HPP plays an important role in spatial processing and the ventral axis is important for anxiety as well as olfactory learning and memory. For example, evidence indicates that the hippocampal CA1 subregion is important in temporal learning and memory processes for spatial (dorsal) as well as olfactory (ventral) information. Studies have shown that the same dorsoventral relationship may hold for the CA3 subregion in pattern completion processes for odor information. Recent evidence has indicated parallel processing fidelity across the dorsoventral axis of the dentate gyrus (DG) for spatial and olfactory pattern separation. While there have been extensive investigations of spatial pattern completion, pattern separation, and temporal learning and an ever-increasing consensus on those processes, there have been far fewer reports and thus a lack of consensus for definitions of these parallel processes in regard to olfaction, with subregional anxiety processes being least understood. Further studies are necessary to understand how ventral subregions of the HPP contribute to learning and memory. Such research may yield increasing understanding of processes such as “odor pattern completion” and “anxiety-based pattern separation.”
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References
Amaral, D. G., & Witter, M. P. (1995). Hippocampal formation. In G. Paxinos (Ed.), The rat nervous system (pp. 443–493). San Diego: Academic.
Bakker, A., Kirwan, C. B., Miller, M., & Stark, C. E. L. (2008). Pattern separation in the human hippocampal CA3 and dentate gyrus. Science (New York, N.Y.), 319(5870), 1640–1642. doi:10.1126/science.1152882.
Bannerman, D. M., Yee, B. K., Good, M. A., Heupel, M. J., Iversen, S. D., & Rawlins, J. N. (1999). Double dissociation of function within the hippocampus: A comparison of dorsal, ventral, and complete hippocampal cytotoxic lesions. Behavioral Neuroscience, 113(6), 1170–1188.
Bannerman, D. M., Grubb, M., Deacon, R. M. J., Yee, B. K., Feldon, J., & Rawlins, J. N. P. (2003). ScienceDirect.com—behavioural brain research—ventral hippocampal lesions affect anxiety but not spatial learning. Behavioural Brain Research, 139(1–2), 197–213.
Bannerman, D. M., Rawlins, J. N. P., McHugh, S. B., Deacon, R. M. J., Yee, B. K., Bast, T., et al. (2004). Regional dissociations within the hippocampus—memory and anxiety. Neuroscience & Biobehavioral Reviews, 28(3), 273–283. doi:10.1016/j.neubiorev.2004.03.004.
Baron-Cohen, S., Ring, H. A., Bullmore, E. T., Wheelwright, S., Ashwin, C., & Williams, S. C. (2000). The amygdala theory of autism. Neuroscience & Biobehavioral Reviews, 24(3), 355–364.
Bowers, D., Verfaellie, M., Valenstein, E., & Heilman, K. M. (1988). Impaired acquisition of temporal information in retrosplenial amnesia. Brain and Cognition, 8(1), 47–66. doi:10.1016/0278-2626(88)90038-3.
Bramham, C. R., Southard, T., Ahlers, S. T., & Sarvey, J. M. (1998). Acute cold stress leading to elevated corticosterone neither enhances synaptic efficacy nor impairs LTP in the dentate gyrus of freely moving rats. Brain Research, 789(2), 245–255.
Chiba, A. A., Kesner, R. P., & Reynolds, A. M. (1994). Memory for spatial location as a function of temporal lag in rats: Role of hippocampus and medial prefrontal cortex. Behavioral and Neural Biology, 61(2), 123–131.
Christie, B. R., & Cameron, H. A. (2006). Neurogenesis in the adult hippocampus. Hippocampus, 16(3), 199–207. doi:10.1002/hipo.20151.
Cleland, T. A., Morse, A., Yue, E. L., & Linster, C. (2002). Behavioral models of odor similarity. Behavioral Neuroscience, 116(2), 222–231. doi:10.1037//0735-7044.116.2.222.
Colombo, M., Fernandez, T., Nakamura, K., & Gross, C. G. (1998). Functional differentiation along the anterior-posterior axis of the hippocampus in monkeys. Journal of Neurophysiology, 80(2), 1002–1005.
Decker, M. W., Curzon, P., & Brioni, J. D. (1995). Influence of separate and combined septal and amygdala lesions on memory, acoustic startle, anxiety, and locomotor activity in rats. Neurobiology of Learning and Memory, 64(2), 156–168. doi:10.1006/nlme.1995.1055.
Dedovic, K., Duchesne, A., Andrews, J., Engert, V., & Pruessner, J. C. (2009). The brain and the stress axis: The neural correlates of cortisol regulation in response to stress. NeuroImage, 47(3), 864–871. doi:10.1016/j.neuroimage.2009.05.074.
Dong, H.-W., Swanson, L. W., Chen, L., Fanselow, M. S., & Toga, A. W. (2009). Genomic-anatomic evidence for distinct functional domains in hippocampal field CA1. Proceedings of the National Academy of Sciences of the United States of America, 106(28), 11794–11799. doi:10.1073/pnas.0812608106.
Eadie, B. D., Zhang, W. N., Boehme, F., Gil-Mohapel, J., Kainer, L., Simpson, J. M., et al. (2009). Fmr1 knockout mice show reduced anxiety and alterations in neurogenesis that are specific to the ventral dentate gyrus. Neurobiology of Disease, 36(2), 361–373. doi:10.1016/j.nbd.2009.08.001.
Eichenbaum, H., Mathews, P., & Cohen, N. J. (1989). Further studies of hippocampal representation during odor discrimination learning. Behavioral Neuroscience, 103(6), 1207–1216.
Everitt, B. J., & Robbins, T. W. (2005). Neural systems of reinforcement for drug addiction: From actions to habits to compulsion. Nature Neuroscience, 8(11), 1481–1489. doi:10.1038/nn1579.
Fanselow, M. S. (1984). What is conditioned fear? Trends in Neurosciences, 7(12), 460–462.
Fanselow, M. S., & Dong, H.-W. (2010). Are the dorsal and ventral hippocampus functionally distinct structures? Neuron, 65(1), 7–19. doi:10.1016/j.neuron.2009.11.031.
Gage, F. H., & Thompson, R. G. (1980). Differential distribution of norepinephrine and serotonin along the dorsal-ventral axis of the hippocampal formation. Brain Research Bulletin, 5(6), 771–773. http://pdn.sciencedirect.com/science?_ob=MiamiImageURL&_cid=271056&_user=10843&_pii=0361923080902208&_check=y&_origin=article&_zone=toolbar&_coverDate=31-Dec-1980&view=c&originContentFamily=serial&wchp=dGLbVlk-zSkzk&md5=2857224f44d72adfdf9ea3facaa8bbee&pid=1-s2.0-0361923080902208-main.pdf&sqtrkid=0.21771737933158875. Accessed 12 June 2013.
Gilbert, M., Racine, R. J., & Smith, G. K. (1985). Epileptiform burst responses in ventral vs dorsal hippocampal slices. Brain Research, 361(1–2), 389–391.
Gilbert, P. E., Kesner, R. P., & Lee, I. (2001). Dissociating hippocampal subregions: A double dissociation between dentate gyrus and CA1. Hippocampus, 11(6), 626–636. doi:10.1002/hipo.1077.
Gold, A. E., & Kesner, R. P. (2005). The role of the CA3 subregion of the dorsal hippocampus in spatial pattern completion in the rat. Hippocampus, 15(6), 808–814. doi:10.1002/hipo.20103.
Goodrich-Hunsaker, N. J., Hunsaker, M. R., & Kesner, R. P. (2008). The interactions and dissociations of the dorsal hippocampus subregions: How the dentate gyrus, CA3, and CA1 process spatial information. Behavioral Neuroscience, 122(1), 16–26. doi:10.1037/0735-7044.122.1.16.
Gourevitch, B., Kay, L. M., & Martin, C. (2010). Directional coupling from the olfactory bulb to the hippocampus during a go/no-go odor discrimination task. Journal of Neurophysiology, 103(5), 2633–2641. doi:10.1152/jn.01075.2009.
Gray, J. A., & McNaughton, N. (2000). The Neuropsychology of Anxiety (2nd ed.). USA: Oxford University Press.
Gulyás, A. I., Tóth, K., McBain, C. J., & Freund, T. F. (1998). Stratum radiatum giant cells: A type of principal cell in the rat hippocampus. The European journal of neuroscience, 10(12), 3813–3822.
Hafting, T., Fyhn, M., Molden, S., Moser, M.-B., & Moser, E. I. (2005). Microstructure of a spatial map in the entorhinal cortex. Nature, 436(7052), 801–806. doi:10.1038/nature03721.
Heale, V. R., & Vanderwolf, C. H. (1999). Odor-induced fast waves in the dentate gyrus depend on a pathway through posterior cerebral cortex: Effects of limbic lesions and trimethyltin. Brain Research Bulletin, 50(4), 291–299.
Hughes, K. C., & Shin, L. M. (2011). Functional neuroimaging studies of post-traumatic stress disorder. Expert Review of Neurotherapeutics, 11(2), 275–285. doi:10.1586/ern.10.198.
Hunsaker, M. R., & Kesner, R. P. (2012). The operation of pattern separation and pattern completion processes associated with different attributes or domains of memory. Neuroscience & Biobehavioral Reviews. doi:10.1016/j.neubiorev.2012.09.014.
Hunsaker, M. R., Fieldsted, P. M., Rosenberg, J. S., & Kesner, R. P. (2008). Dissociating the roles of dorsal and ventral CA1 for the temporal processing of spatial locations, visual objects, and odors. Behavioral Neuroscience, 122(3), 643–650. doi:10.1037/0735-7044.122.3.643.
Jayatissa, M. N., Bisgaard, C., Tingström, A., Papp, M., & Wiborg, O. (2006). Hippocampal cytogenesis correlates to escitalopram-mediated recovery in a chronic mild stress rat model of depression. Neuropsychopharmacology: Official Publication of the American College of Neuropsychopharmacology, 31(11), 2395–2404. doi:10.1038/sj.npp.1301041.
Jung, M. W., Wiener, S. I., & McNaughton, B. L. (1994). Comparison of spatial firing characteristics of units in dorsal and ventral hippocampus of the rat. The Journal of neuroscience: the official journal of the Society for Neuroscience, 14(12), 7347–7356.
Kavushansky, A., Vouimba, R.-M., Cohen, H., & Richter-Levin, G. (2006). Activity and plasticity in the CA1, the dentate gyrus, and the amygdala following controllable vs. uncontrollable water stress. Hippocampus, 16(1), 35–42. doi:10.1002/hipo.20130.
Kent, K., Hess, K., Tonegawa, S., & Small, S. A. (2007). CA3 NMDA receptors are required for experience-dependent shifts in hippocampal activity. Hippocampus, 17(10), 1003–1011. doi:10.1002/hipo.20332.
Kesner, R. P. (2009). Tapestry of memory. Behavioral Neuroscience, 123(1), 1–13. doi:10.1037/a0014004.
Kesner, R. P., & Hunsaker, M. R. (2010). The temporal attributes of episodic memory. Behavioural Brain Research, 215(2), 299–309. doi:10.1016/j.bbr.2009.12.029.
Kesner, R. P., Gilbert, P. E., & Barua, L. A. (2002). The role of the hippocampus in memory for the temporal order of a sequence of odors. Behavioral Neuroscience, 116(2), 286–290.
Kesner, R. P., Hunsaker, M. R., & Ziegler, W. (2010). The role of the dorsal CA1 and ventral CA1 in memory for the temporal order of a sequence of odors. Neurobiology of Learning and Memory, 93(1), 111–116. doi:10.1016/j.nlm.2009.08.010.
Kesner, R. P., Hunsaker, M. R., & Ziegler, W. (2011). The role of the dorsal and ventral hippocampus in olfactory working memory. Neurobiology of Learning and Memory, 96(2), 361–366. doi:10.1016/j.nlm.2011.06.011.
Kjelstrup, K. G., Tuvnes, F. A., Steffenach, H.-A., Murison, R., Moser, E. I., & Moser, M.-B. (2002). Reduced fear expression after lesions of the ventral hippocampus. Proceedings of the National Academy of Sciences of the United States of America, 99(16), 10825–10830. doi:10.1073/pnas.152112399.
Lazar, R. M., & Mohr, J. P. (2011). Revisiting the contributions of Paul Broca to the study of aphasia. Neuropsychology Review, 21, 236–239. doi:10.1007/s11065-011-9176-8.
Lee, I., & Kesner, R. P. (2004). Differential contributions of dorsal hippocampal subregions to memory acquisition and retrieval in contextual fear-conditioning. Hippocampus, 14(3), 301–310. doi:10.1002/hipo.10177.
Levita, L., & Muzzio, I. A. (2010). Role of the hippocampus in goal-oriented tasks requiring retrieval of spatial versus non-spatial information. Neurobiology of Learning and Memory, 93(4), 581–588. doi:10.1016/j.nlm.2010.02.006.
Magariños, A. M., McEwen, B. S., Flügge, G., & Fuchs, E. (1996). Chronic psychosocial stress causes apical dendritic atrophy of hippocampal CA3 pyramidal neurons in subordinate tree shrews. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 16(10), 3534–3540.
Maguire, E. A., Gadian, D. G., Johnsrude, I. S., Good, C. D., Ashburner, J., Frackowiak, R. S., et al. (2000). Navigation-related structural change in the hippocampi of taxi drivers. Proceedings of the National Academy of Sciences of the United States of America, 97(8), 4398–4403. doi:10.1073/pnas.070039597.
McHugh, S. B., Deacon, R. M. J., Rawlins, J. N. P., & Bannerman, D. M. (2004). Amygdala and ventral hippocampus contribute differentially to mechanisms of fear and anxiety. Behavioral Neuroscience, 118(1), 63–78. doi:10.1037/0735-7044.118.1.63.
Moser, M. B., & Moser, E. I. (1998a). Distributed encoding and retrieval of spatial memory in the hippocampus. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 18(18), 7535–7542.
Moser, M. B., & Moser, E. I. (1998b). Functional differentiation in the hippocampus. Hippocampus, 8(6), 608–619. doi:10.1002/(SICI)1098-1063(1998)8:6<608::AID-HIPO3>3.0.CO;2-7.
Moser, E., Moser, M. B., & Andersen, P. (1993). Spatial learning impairment parallels the magnitude of dorsal hippocampal lesions, but is hardly present following ventral lesions. The Journal of Neuroscience: The Official journal of the Society for Neuroscience, 13(9), 3916–3925.
O’Keefe, J., & Nadel, L. (1978). The hippocampus as a cognitive map. Oxford: Clarendon Press.
Pandis, C., Sotiriou, E., Kouvaras, E., Asprodini, E., Papatheodoropoulos, C., & Angelatou, F. (2006). Differential expression of NMDA and AMPA receptor subunits in rat dorsal and ventral hippocampus. Neuroscience, 140(1), 163–175. doi:10.1016/j.neuroscience.2006.02.003.
Papatheodoropoulos, C., & Kostopoulos, G. (2000). Decreased ability of rat temporal hippocampal CA1 region to produce long-term potentiation. Neuroscience Letters, 279(3), 177–180.
Pentkowski, N. S., Blanchard, D. C., Lever, C., Litvin, Y., & Blanchard, R. J. (2006). Effects of lesions to the dorsal and ventral hippocampus on defensive behaviors in rats. European Journal of Neuroscience, 23(8), 2185–2196. doi:10.1111/j.1460-9568.2006.04754.x.
Rogers, J. L., Hunsaker, M. R., & Kesner, R. P. (2006). Effects of ventral and dorsal CA1 subregional lesions on trace fear conditioning. Neurobiology of Learning and Memory, 86(1), 72–81. doi:10.1016/j.nlm.2006.01.002.
Rolls, E. T., & Kesner, R. P. (2006). A computational theory of hippocampal function, and empirical tests of the theory. Progress in Neurobiology, 79(1), 1–48. doi:10.1016/j.pneurobio.2006.04.005.
Rolls, E. T., Treves, A., Foster, D., & Perez-Vicente, C. (1997). Simulation studies of the CA3 hippocampal subfield modelled as an attractor neural network. Neural Networks, 10(9), 1559–1569. doi:10.1016/S0893-6080(97)00092-0.
Royer, S., Sirota, A., Patel, J., & Buzsaki, G. (2010). Distinct representations and theta dynamics in dorsal and ventral hippocampus. Journal of Neuroscience, 30(5), 1777–1787. doi:10.1523/JNEUROSCI.4681-09.2010.
Sano, K. (1997). Hippocampus and epilepsy surgery. Epilepsia, 38(s6), 4–10. doi:10.1111/j.1528-1157.1997.tb00098.x
Scoville, W. B., & Milner, B. (1957). Loss of recent memory after bilateral hippocampal lesions. Journal of Neurology, Neurosurgery, and Psychiatry, 20(1), 11–21.
Squire, L. R., & Zola-Morgan, S. (1991). The medial temporal lobe memory system. Science (New York, N.Y.), 253(5026), 1380–1386.
Taube, J. S. (2007). The head direction signal: Origins and sensory-motor integration. Annual Review of Neuroscience, 30, 181–207. doi:10.1146/annurev.neuro.29.051605.112854.
Treit, D., Pesold, C., & Rotzinger, S. (1993). Noninteractive effects of diazepam and amygdaloid lesions in two animal models of anxiety. Behavioral Neuroscience, 107(6), 1099–1105.
Van Groen, T., & Wyss, J. M. (1990). Extrinsic projections from area CA1 of the rat hippocampus: Olfactory, cortical, subcortical, and bilateral hippocampal formation projections. The Journal of Comparative Neurology, 302(3), 515–528. doi:10.1002/cne.903020308.
Vanderwolf, C. H. (1992). Hippocampal activity, olfaction, and sniffing: An olfactory input to the dentate gyrus. Brain Research, 593(2), 197–208.
Vouimba, R.-M., Yaniv, D., Diamond, D., & Richter-Levin, G. (2004). Effects of inescapable stress on LTP in the amygdala versus the dentate gyrus of freely behaving rats. The European Journal of Neuroscience, 19(7), 1887–1894. doi:10.1111/j.1460-9568.2004.03294.x.
Walsh, R. N., & Cummins, R. A. (1976). The open-field test: A critical review. Psychological Bulletin, 83(3), 482–504.
Weeden, C. S. S., Hu, N. J., Ho, L. Y. N., & Kesner, R. P. (2012). The role of the ventral dentate gyrus in olfactory learning and memory. Presented at the Society for Neuroscience Abstracts, New Orleans.
Witter, M. P. (1993). Organization of the entorhinal-hippocampal system: A review of current anatomical data. Hippocampus, 3 (Spec No), 33–44.
Witter, M. P., Van Hoesen, G. W., & Amaral, D. G. (1989). Topographical organization of the entorhinal projection to the dentate gyrus of the monkey. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 9(1), 216–228..
Yassa, M. A., Stark, S. M., Bakker, A., Albert, M. S., Gallagher, M., & Stark, C. E. L. (2010). High-resolution structural and functional MRI of hippocampal CA3 and dentate gyrus in patients with amnestic mild cognitive impairment. NeuroImage, 51(3), 1242–1252. doi:10.1016/j.neuroimage.2010.03.040.
Yoon, T., & Otto, T. (2007). Differential contributions of dorsal vs. ventral hippocampus to auditory trace fear conditioning. Neurobiology of Learning and Memory, 87(4), 464–475. doi:10.1016/j.nlm.2006.12.006.
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Weeden, C. (2016). Dorsoventral Hippocampus: Subregional Importance in Anxiety and Olfactory Learning and Memory. In: Jackson, P., Chiba, A., Berman, R., Ragozzino, M. (eds) The Neurobiological Basis of Memory. Springer, Cham. https://doi.org/10.1007/978-3-319-15759-7_8
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