An Extrahippocampal Projection from the Dentate Gyrus to the Olfactory Tubercle

Overview

Journal BMC Neurosci

Publisher Biomed Central

Specialty Neurology

Date 2005 Jun 2

PMID 15927048

Citations 2

Authors

Heinz Kunzle

Affiliations

Soon will be listed here.

Abstract

Background: The dentate gyrus is well known for its mossy fiber projection to the hippocampal field 3 (CA3) and its extensive associational and commissural connections. The dentate gyrus, on the other hand, has only few projections to the CA1 and the subiculum, and none have clearly been shown to extrahippocampal target regions.

Results: Using anterograde and retrograde tracer techniques in the Madagascan lesser hedgehog tenrec (Afrosoricidae, Afrotheria) it was shown in this study that the dentate hilar region gave rise to a faint, but distinct, bilateral projection to the most rostromedial portion of the olfactory tubercle, particularly its molecular layer. Unlike the CA1 and the subiculum the dentate gyrus did not project to the accumbens nucleus. A control injection into the medial septum-diagonal band complex also retrogradely labeled cells in the dentate hilus, but these neurons were found immediately adjacent to the heavily labeled CA3, while the tracer injections into the rostromedial tubercle did not reveal any labeling in CA3.

Conclusion: The dentate hilar neurons projecting to the olfactory tubercle cannot be considered displaced cells of CA3 but represent true dentato-tubercular projection neurons. This projection supplements the subiculo-tubercular projection. Both terminal fields overlap among one another as well as with the fiber terminations arising in the anteromedial frontal cortex. The rostromedial olfactory tubercle might represent a distinct ventral striatal target area worth investigating in studies of the parallel processing of cortico-limbic information in tenrec as well as in cat and monkey.

Citing Articles

Sharp wave-associated synchronized inputs from the piriform cortex activate olfactory tubercle neurons during slow-wave sleep.

Narikiyo K, Manabe H, Mori K J Neurophysiol. 2013; 111(1):72-81.

PMID: 24108798 PMC: 3921374. DOI: 10.1152/jn.00535.2013.

Sniffing out the contributions of the olfactory tubercle to the sense of smell: hedonics, sensory integration, and more?.

Wesson D, Wilson D Neurosci Biobehav Rev. 2010; 35(3):655-68.

PMID: 20800615 PMC: 3005978. DOI: 10.1016/j.neubiorev.2010.08.004.

References

Groenewegen H, Room P, Witter M, Lohman A . Cortical afferents of the nucleus accumbens in the cat, studied with anterograde and retrograde transport techniques. Neuroscience. 1982; 7(4):977-96. DOI: 10.1016/0306-4522(82)90055-0. View

Christakou A, Robbins T, Everitt B . Prefrontal cortical-ventral striatal interactions involved in affective modulation of attentional performance: implications for corticostriatal circuit function. J Neurosci. 2004; 24(4):773-80. PMC: 6729820. DOI: 10.1523/JNEUROSCI.0949-03.2004. View

Room P, Russchen F, Groenewegen H, Lohman A . Efferent connections of the prelimbic (area 32) and the infralimbic (area 25) cortices: an anterograde tracing study in the cat. J Comp Neurol. 1985; 242(1):40-55. DOI: 10.1002/cne.902420104. View

Ferry A, Ongur D, An X, Price J . Prefrontal cortical projections to the striatum in macaque monkeys: evidence for an organization related to prefrontal networks. J Comp Neurol. 2000; 425(3):447-70. DOI: 10.1002/1096-9861(20000925)425:3<447::aid-cne9>3.0.co;2-v. View

Verwer R, Meijer R, Van Uum H, Witter M . Collateral projections from the rat hippocampal formation to the lateral and medial prefrontal cortex. Hippocampus. 1997; 7(4):397-402. DOI: 10.1002/(SICI)1098-1063(1997)7:4<397::AID-HIPO5>3.0.CO;2-G. View

Velayos J, Reinoso-Suarez F . Prosencephalic afferents to the mediodorsal thalamic nucleus. J Comp Neurol. 1985; 242(2):161-81. DOI: 10.1002/cne.902420203. View

Kunzle H . The striatum in the hedgehog tenrec: histochemical organization and cortical afferents. Brain Res. 2005; 1034(1-2):90-113. DOI: 10.1016/j.brainres.2004.11.047. View

Schwerdtfeger W, Buhl E . Various types of non-pyramidal hippocampal neurons project to the septum and contralateral hippocampus. Brain Res. 1986; 386(1-2):146-54. DOI: 10.1016/0006-8993(86)90151-4. View

Totterdell S, Hayes L . Non-pyramidal hippocampal projection neurons: a light and electron microscopic study. J Neurocytol. 1987; 16(4):477-85. DOI: 10.1007/BF01668502. View

10.

Witter M, Groenewegen H . Connections of the parahippocampal cortex in the cat. IV. Subcortical efferents. J Comp Neurol. 1986; 252(1):51-77. DOI: 10.1002/cne.902520104. View

11.

Berendse H, Galis-de Graaf Y, Groenewegen H . Topographical organization and relationship with ventral striatal compartments of prefrontal corticostriatal projections in the rat. J Comp Neurol. 1992; 316(3):314-47. DOI: 10.1002/cne.903160305. View

12.

Sesack S, Deutch A, Roth R, Bunney B . Topographical organization of the efferent projections of the medial prefrontal cortex in the rat: an anterograde tract-tracing study with Phaseolus vulgaris leucoagglutinin. J Comp Neurol. 1989; 290(2):213-42. DOI: 10.1002/cne.902900205. View

13.

Sorensen K . Projections of the entorhinal area to the striatum, nucleus accumbens, and cerebral cortex in the guinea pig. J Comp Neurol. 1985; 238(3):308-22. DOI: 10.1002/cne.902380306. View

14.

Deller T, Nitsch R, Frotscher M . Phaseolus vulgaris-leucoagglutinin tracing of commissural fibers to the rat dentate gyrus: evidence for a previously unknown commissural projection to the outer molecular layer. J Comp Neurol. 1995; 352(1):55-68. DOI: 10.1002/cne.903520105. View

15.

Forti M, Michelson H . Synaptic connectivity of distinct hilar interneuron subpopulations. J Neurophysiol. 1998; 79(6):3229-37. DOI: 10.1152/jn.1998.79.6.3229. View

16.

Chiba T, Kayahara T, Nakano K . Efferent projections of infralimbic and prelimbic areas of the medial prefrontal cortex in the Japanese monkey, Macaca fuscata. Brain Res. 2001; 888(1):83-101. DOI: 10.1016/s0006-8993(00)03013-4. View

17.

Jinno S, Kosaka T . Heterogeneous expression of the cholecystokinin-like immunoreactivity in the mouse hippocampus, with special reference to the dorsoventral difference. Neuroscience. 2003; 122(4):869-84. DOI: 10.1016/j.neuroscience.2003.08.039. View

18.

Zhou L, Furuta T, Kaneko T . Chemical organization of projection neurons in the rat accumbens nucleus and olfactory tubercle. Neuroscience. 2003; 120(3):783-98. DOI: 10.1016/s0306-4522(03)00326-9. View

19.

Haber S, Kunishio K, Mizobuchi M, Lynd-Balta E . The orbital and medial prefrontal circuit through the primate basal ganglia. J Neurosci. 1995; 15(7 Pt 1):4851-67. PMC: 6577885. View

20.

Patton P, McNaughton B . Connection matrix of the hippocampal formation: I. The dentate gyrus. Hippocampus. 1995; 5(4):245-86. DOI: 10.1002/hipo.450050402. View