Differential Regulation of Synaptic Plasticity of the Hippocampal and the Hypothalamic Inputs to the Anterior Thalamus

Overview

Journal Hippocampus

Publisher Wiley

Date 2010 Jan 1

PMID 20043283

Citations 24

Authors

Marian Tsanov

Seralynne D Vann

Jonathan T Erichsen

Nick Wright

John P Aggleton

Shane M OMara

Affiliations

Soon will be listed here.

Abstract

The hippocampus projects to the anterior thalamic nuclei both directly and indirectly via the mammillary bodies, but little is known about the electrophysiological properties of these convergent pathways. Here we demonstrate, for the first time, the presence of long-term plasticity in anterior thalamic nuclei synapses in response to high- and low-frequency stimulation (LFS) in urethane-anesthetized rats. We compared the synaptic changes evoked via the direct vs. the indirect hippocampal pathways to the anterior thalamus, and found that long-term potentiation (LTP) of the thalamic field response is induced predominantly through the direct hippocampal projections. Furthermore, we have estimated that that long-term depression (LTD) can be induced only after stimulation of the indirect connections carried by the mammillothalamic tract. Interestingly, basal synaptic transmission mediated by the mammillothalamic tract undergoes use-dependent, BDNF-mediated potentiation, revealing a distinct form of plasticity specific to the diencephalic region. Our data indicate that the thalamus does not passively relay incoming information, but rather acts as a synaptic network, where the ability to integrate hippocampal and mammillary body inputs is dynamically modified as a result of previous activity in the circuit. The complementary properties of these two parallel pathways upon anterior thalamic activity reveal that they do not have duplicate functions.

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References

Ying S, Futter M, Rosenblum K, Webber M, Hunt S, Bliss T . Brain-derived neurotrophic factor induces long-term potentiation in intact adult hippocampus: requirement for ERK activation coupled to CREB and upregulation of Arc synthesis. J Neurosci. 2002; 22(5):1532-40. PMC: 6758896. View

Aggleton J, DeSimone R, Mishkin M . The origin, course, and termination of the hippocampothalamic projections in the macaque. J Comp Neurol. 1986; 243(3):409-21. DOI: 10.1002/cne.902430310. View

Aggleton J, Brown M . Episodic memory, amnesia, and the hippocampal-anterior thalamic axis. Behav Brain Sci. 2001; 22(3):425-44; discussion 444-89. View

Tsanov M, Manahan-Vaughan D . The adult visual cortex expresses dynamic synaptic plasticity that is driven by the light/dark cycle. J Neurosci. 2007; 27(31):8414-21. PMC: 6673052. DOI: 10.1523/JNEUROSCI.1101-07.2007. View

Thompson R . Rapid forgetting of a spatial habit in rats with hippocampal lesions. Science. 1981; 212(4497):959-60. DOI: 10.1126/science.6785882. View

Warburton E, Baird A, Morgan A, Muir J, Aggleton J . The conjoint importance of the hippocampus and anterior thalamic nuclei for allocentric spatial learning: evidence from a disconnection study in the rat. J Neurosci. 2001; 21(18):7323-30. PMC: 6762976. View

Rauschecker J . Cortical control of the thalamus: top-down processing and plasticity. Nat Neurosci. 1999; 1(3):179-80. DOI: 10.1038/625. View

Sharma S, Sherff C, Stough S, Hsuan V, Carew T . A tropomyosin-related kinase B ligand is required for ERK activation, long-term synaptic facilitation, and long-term memory in aplysia. Proc Natl Acad Sci U S A. 2006; 103(38):14206-10. PMC: 1599935. DOI: 10.1073/pnas.0603412103. View

Chance F, Nelson S, Abbott L . Synaptic depression and the temporal response characteristics of V1 cells. J Neurosci. 1998; 18(12):4785-99. PMC: 6792683. View

10.

Buzsaki G, Haas H, Anderson E . Long-term potentiation induced by physiologically relevant stimulus patterns. Brain Res. 1987; 435(1-2):331-3. DOI: 10.1016/0006-8993(87)91618-0. View

11.

van der Werf Y, Scheltens P, Lindeboom J, Witter M, Uylings H, Jolles J . Deficits of memory, executive functioning and attention following infarction in the thalamus; a study of 22 cases with localised lesions. Neuropsychologia. 2003; 41(10):1330-44. DOI: 10.1016/s0028-3932(03)00059-9. View

12.

Klausnitzer J, Manahan-Vaughan D . Frequency facilitation at mossy fiber-CA3 synapses of freely behaving rats is regulated by adenosine A1 receptors. J Neurosci. 2008; 28(18):4836-40. PMC: 6670436. DOI: 10.1523/JNEUROSCI.3729-07.2008. View

13.

Meibach R, Siegel A . The origin of fornix fibers which project to the mammillary bodies in the rat: a horseradish peroxidase study. Brain Res. 1975; 88(3):508-12. DOI: 10.1016/0006-8993(75)90662-9. View

14.

Gartner A, Polnau D, Staiger V, Sciarretta C, Minichiello L, Thoenen H . Hippocampal long-term potentiation is supported by presynaptic and postsynaptic tyrosine receptor kinase B-mediated phospholipase Cgamma signaling. J Neurosci. 2006; 26(13):3496-504. PMC: 6673845. DOI: 10.1523/JNEUROSCI.3792-05.2006. View

15.

Vann S, Aggleton J . The mammillary bodies: two memory systems in one?. Nat Rev Neurosci. 2004; 5(1):35-44. DOI: 10.1038/nrn1299. View

16.

von Cramon D, Hebel N, Schuri U . A contribution to the anatomical basis of thalamic amnesia. Brain. 1985; 108 ( Pt 4):993-1008. DOI: 10.1093/brain/108.4.993. View

17.

Lisman J . The CaM kinase II hypothesis for the storage of synaptic memory. Trends Neurosci. 1994; 17(10):406-12. DOI: 10.1016/0166-2236(94)90014-0. View

18.

Bienenstock E, Cooper L, Munro P . Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex. J Neurosci. 1982; 2(1):32-48. PMC: 6564292. View

19.

Salin P, Scanziani M, Malenka R, Nicoll R . Distinct short-term plasticity at two excitatory synapses in the hippocampus. Proc Natl Acad Sci U S A. 1996; 93(23):13304-9. PMC: 24088. DOI: 10.1073/pnas.93.23.13304. View

20.

Kosub K, Do V, Derrick B . NMDA receptor antagonists block heterosynaptic long-term depression (LTD) but not long-term potentiation (LTP) in the CA3 region following lateral perforant path stimulation. Neurosci Lett. 2005; 374(1):29-34. DOI: 10.1016/j.neulet.2004.10.028. View