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Synaptic Properties of the Mammillary and Cortical Afferents to the Anterodorsal Thalamic Nucleus in the Mouse

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Synaptic Properties of the Mammillary and Cortical Afferents to the Anterodorsal Thalamic Nucleus in the Mouse The Journal of Neuroscience, June 17, 2009 • 29(24):7815–7819 • 7815 Brief Communications Synaptic Properties of the Mammillary and Cortical Afferents to the Anterodorsal Thalamic Nucleus in the Mouse Iraklis Petrof and S. Murray Sherman Department of Neurobiology, University of Chicago, Chicago, Illinois 60637 Input to sensory thalamic nuclei can be classified as either driver or modulator, based on whether or not the information conveyed determines basic postsynaptic receptive field properties. Here we demonstrate that this distinction can also be applied to inputs received by nonsensory thalamic areas. Using flavoprotein autofluorescence imaging, we developed two slice preparations that contain the afferents to the anterodorsal thalamic nucleus (AD) from the lateral mammillary body and the cortical afferents arriving through the internal capsule, respectively. We examined the synaptic properties of these inputs and found that the mammillothalamic pathway exhibits paired-pulse depression, lack of a metabotropic glutamate component, and an all-or-none response pattern, which are all signatures of a driver pathway. On the other hand, the cortical input exhibits graded paired-pulse facilitation and the capacity to activate metabotropic glutamatergic responses, all features of a modulatory pathway. Our results extend the notion of driving and modulating inputs to the AD, indicating that it is a first-order relay nucleus and suggesting that these criteria may be general to the whole of thalamus. Introduction and Sherman, 2004; Van Horn and Sherman, 2007; Lee and Sher- The thalamus receives input from a multitude of cortical and man, 2008), this is not the case for other nuclei. It needs to be subcortical areas and relays this to cortex, representing the sole noted that the distinction between “traditional sensory” and source of information flow to the latter. Afferents to the main “other” thalamic nuclei is primarily a semantic one. By “tradi- sensory thalamic nuclei can be divided into drivers, which deter- tional sensory nuclei,” we mean nuclei such as the lateral genic- mine the main postsynaptic receptive field properties and carry ulate or ventral posterior medial nuclei, which have been the the main information to be relayed to cortex, and modulators, main experimental models to study thalamus. One of the “other” which affect the way driver information is relayed (Sherman and nuclei is the anterodorsal nucleus (AD), perhaps the most prom- Guillery, 1998, 2006). Driver inputs exhibit such synaptic fea- inent of the anterior thalamic nuclei. Its subcortical afferents tures as a strong, all-or-none response pattern, paired-pulse de- arrive from lateral mammillary body (LM) of the hypothalamus pression, and the capacity to activate only ionotropic glutamate (Watanabe and Kawana, 1980; Hayakawa and Zyo, 1989; Shibata, receptors. Modulators, on the other hand, produce relatively 1992), whereas cortical afferents arrive primarily from the para- weak, graded responses with paired-pulse facilitation and can subiculum, postsubiculum, and the parts of the retrosplenial cor- activate both ionotropic and metabotropic receptors (Sherman tex (van Groen and Wyss, 1990a,b; Shibata and Naito, 2005), the and Guillery, 2006). Individual thalamic nuclei, on the basis of latter two also being the major target of AD efferents (Shibata, whether they relay driving information from subcortical areas to 1993; Van Groen and Wyss, 1995, 2003). In addition to their the cortex or from one cortical area to another, have been cate- involvement in some limbic functions (Sziklas and Petrides, gorized as first-order (FO) or higher-order (HO) nuclei, respec- 1999; Ce´le´rier et al., 2000; Wolff et al., 2008), AD cells have been tively (Guillery, 1995; Sherman and Guillery, 1998, 2006). found to respond to head direction activity, similarly to cells in Whereas a great deal is known about the origin of driver and cortical areas associated with AD (Sharp, 1996; Goodridge and modulating input in most traditional sensory thalamic nuclei Taube, 1997; Hargreaves et al., 2007). We wished to determine (Guillery et al., 2001; Wang et al., 2002; Li et al., 2003; Reichova whether the synaptic properties of various inputs to AD con- formed to the driver/modulator model developed for the tradi- tional sensory thalamic relays, thereby extending this concept to Received April 1, 2009; revised May 7, 2009; accepted May 22, 2009. thalamus more generally, or whether some other pattern might Funding was obtained from National Institutes of Health (NIH)/National Eye Institute Grant EY03038 and NIH/ National Institute on Deafness and Other Communication Disorders Grant DC008794 to S.M.S. We thank the follow- exist. To do so, we developed two new slice preparations in the ingpeoplefortheirinvaluablehelpandtechnicaladviceincarryingoutallexperimentalprocedures(inalphabetical mouse: one that contains the pathway between LM and AD, and order): Dr. Joseph A. Beatty, Elise N. Covic, Dr. Y. W. Lam, Dr. Charles C. Lee, Dr. Dan A. Llano, Brian B. Theyel, and Dr. another that contains the severed corticothalamic axons termi- Carmen Varela. nating into AD through the internal capsule. We thus examined CorrespondenceshouldbeaddressedtoS.MurraySherman,DepartmentofNeurobiology,UniversityofChicago, the synaptic responses of AD cells following the stimulation of Abbott J-117, 947 East 58th Street, Chicago, IL 60637. E-mail: [email protected]. DOI:10.1523/JNEUROSCI.1564-09.2009 their subcortical and cortical afferent pathways. Our data show Copyright © 2009 Society for Neuroscience 0270-6474/09/297815-05$15.00/0 that the mammillary input to AD possesses the profile character- 7816 • J. Neurosci., June 17, 2009 • 29(24):7815–7819 Petrof and Sherman • Driver and Modulatory Afferents of the Anterodorsal Nucleus ulation consisted of a current injection train (50–250 ␮A, 20 Hz) over 1 s. FA activity was monitored over that period of time in addition to 1 s before stimulation and 12 s following stimulation. Fluorescence images were acquired at 2.5–10 frames per second (integration time of 150–300 ms). The optical image was generated as a function of the ⌬f/f ratio of the baseline autofluorescence of the slice before stimulation subtracted from the autofluorescence of the slice over the period of stimulation (⌬f) divided by baseline ( f). In some FA experiments, LM was stimulated through the photo- uncaging of caged glutamate. For these experiments, nitroindolinyl- caged glutamate (Sigma-Aldrich) was added to the recirculating ACSF (0.4 mM), and a UV laser beam (DPSS Laser) was used to locally photo- lyse the caged compound (Shepherd et al., 2003; Lam and Sherman, 2005, 2007; Lam et al., 2006). The laser beam had an intensity of 20–80 mW and gave off a 10 ms, 20-pulse light stimulus (355 nm wavelength, frequency-tripled Nd:YVO4, 100 kHz pulse repetition rate). For photo- uncaging FA experiments, the ⌬f/f ratio was calculated by subtracting Figure 1. Schematic illustration of the blocking angles used to generate the two slice prep- baseline autofluorescence from autofluorescence immediately after the arations. The mammillothalamic slice was prepared as follows: taking the midline as a refer- last laser pulse (⌬f) and by then dividing the result by baseline ( f). FA ence, a 12° cut was made to parallel the route of the mammillothalamic tract and a single analyses for both electrical and glutamate photo-uncaging stimulation 500-␮m-thickslicewasvibratomed.TheslicecontainingtheseveredcorticalaxonsintoADwas were performed using a custom-made software written in Matlab prepared by blocking the brain at a 70° angle and by cutting a single 500-␮m-thick slice. C, (MathWorks). Caudal; L, lateral; M, medial; R, rostral. Electrophysiology. Whole-cell patch-clamp recordings in current- clamp mode were performed using a visualized slice setup under a dif- ferential interference contrast-equipped Axioscop 2FS microscope (Carl istics of a driving pathway, whereas cortical input arriving Zeiss Instruments) and with a Multiclamp 700B amplifier and pCLAMP through the internal capsule appears to be of an exclusively mod- software (Molecular Devices). The pipettes used for the recordings were ulatory nature, a pattern seen in the traditional sensory thalamic pulled from 1.5 mm borosilicate glass capillaries and were filled with nuclei. intracellular solution containing the following (in mM): 117 K-gluconate, 13 KCl, 1 MgCl2, 0.07 CaCl2, 10 HEPES, 0.1 EGTA, 2 Na2-ATP, and 0.4 Materials and Methods Na-GTP, pH 7.3, 290 mOsm). Pipette input resistances varied between 4 Slice preparation. BALB/c mice (ages 14–18 d) were anesthetized with and8M⍀. Data were digitized on a Digidata 1200 board and stored on a isoflurane and decapitated. Brains were rapidly removed and placed in computer. Analyses of the acquired traces were performed in ClampFit chilled (0–4°C), oxygenated (95% O2,5%CO2) slicing solution contain- (Molecular Devices) software. To evoke synaptic responses in AD cells, ing the following (in mM): 2.5 KCl, 1.25 NaH2PO4, 10 MgCl2, 0.5 CaCl2, electric stimulation of their afferent pathways was delivered through the 26 NaHCO3, 11 glucose, and 206 sucrose. The mammillothalamic slice same bipolar electrodes as the ones used for FA. For the examination of preparation was prepared as follows: brains were blocked at a 12° angle short-term synaptic plasticity, we used a protocol that consisted of four from the midline over the right hemisphere (Fig. 1), and the blocked side 0.1-ms-long pulses at a frequency of 10 Hz. In doing so, we used the was glued onto a vibratome platform (Leica). Slices were cut at 500 ␮m minimal stimulation intensity required to elicit an EPSP. This was done off-parasagittal in that orientation, thus preserving most of the connec- to minimize the potential spread of current around the stimulation area, tivity between LM and AD (see Results). The trajectory of the corticofu- which could potentially result in the recruitment of other AD afferents, gal fibers terminating in AD is such that the inclusion of the whole thus contaminating the responses recorded from the nucleus.
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