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Department of Neurobiology, Pharmacology and Physiology, University of Chicago, Chicago, Illinois
Submitted 25 February 2005; accepted in final form 1 June 2005
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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; Sherman and Guillery 2001). The issue addressed here concerns the functional nature of the topography between the thalamic reticular nucleus and the ventral posterior lateral nucleus, the latter being a first-order relay for somatosensory information (see Sherman and Guillery 2001).
The issue of topography is important, because it helps establish aspects of the function of the thalamic reticular nucleus. Earlier reports have suggested that the thalamic reticular nucleus has rather diffuse connections with the relay nuclei (e.g., Jones 1975; Scheibel and Scheibel 1966; Steriade et al. 1993), but more recent evidence suggests that topography does exist, at least for parts of thalamus related to first-order relays (reviewed in Guillery and Harting 2003; Guillery et al. 1998). Evidence for topography has been anatomical, mostly using pathway tracing techniques (Guillery and Harting 2003; Guillery et al. 1998). In the ventral posterior lateral and medial nuclei of the rat, the axons of reticular neurons usually terminate in a compact arbor within a compact sphere, or more often, a short rod of tissue having its long axis oriented rostrocaudally. The diameters of these short rods were 100–150 µm and their length ranged between 250 and 300 µm (Cox et al. 1996; Pinault et al. 1995a,b). Cox et al. (1996) could differentiate two other termination patterns of reticular axons in younger animals: an intermediate arborization where the dimension of the branching structure was larger (585 by 359 µm) and a diffuse arborization with multiple arbors.
Evidence for topography in this projection to date has been anatomical, mostly using pathway tracing techniques (Guillery and Harting 2003; Guillery et al. 1998). The description for the topography between the thalamic reticular nucleus and the ventral posterior lateral nucleus is fairly typical in this regard (Crabtree 1992a,b, 1996). Here, the clearest evidence involves thin disks of reticular cells, oriented parallel to the border between the thalamic reticular and ventral posterior lateral nuclei. These disks and sites with which they connect were organized topographically in the direction perpendicular to the border in the horizontal sections of the brain; the topography in the direction parallel to the border is less well defined.
Our goal was to provide a mapping of the functional topography between the thalamic reticular and ventral posterior lateral nuclei to extend and clarify the mapping gleaned from pathway tracing studies. We did this using the technique of laser scanning photostimulation (Callaway and Katz 1993; Roerig and Chen 2002; Schubert et al. 2001; Shepherd et al. 2003) of in vitro slices through thalamus of the rat. We found a precise topography both parallel and perpendicular to the border between the thalamic reticular and ventral posterior lateral nuclei.
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METHODS |
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Preparation of thalamic slices
To obtain the slices, each animal was deeply anesthetized by inhalation of isoflurane, and its brain was quickly removed and chilled in ice-cold artificial cerebrospinal fluid (ACSF), which contained (in mM) 125 NaCl, 3 KCl, 1.25 NaH2PO4, 1 MgCl2, 2 CaCl2, 25 NaHCO3, and 25 glucose. Tissue slices were cut at 400 µm in the horizontal plane using a vibrating tissue slicer, transferred to a holding chamber containing oxygenated physiological saline maintained at 30°C, and incubated for 
1 h before recording. Horizontal slices were used in our study because pathway tracing experiments (unpublished data) indicate that this plane of sectioning preserves most of the connections in both directions between the thalamic reticular and ventral posterior lateral nuclei.
Physiological recording
Whole cell recordings were performed using a visualized slice preparation as described previously (Lam et al. 2005). Recording pipettes were pulled from borosilicate glass capillaries and had tip resistances of 4–8 M
when filled with the appropriate solution. For most cells, this solution contained (in mM) 117 Cs-gluconate, 13 CsCl, 2 MgCl2, 10 HEPES, 2 Na2-ATP, 0.3 Na-GTP, and 0.4% biocytin. In these cases, the K+ channel blocker, Cs+, was included in the recording pipette to suppress IK-leak and help maintain the holding voltage at 0 mV. In some cells, we replaced the Cs+ with K+ or Na+ (final concentration in mM: 135 K-gluconate, 7 NaCl, 2 MgCl2, 10 HEPES, 2 Na2-ATP, 0.3 Na-GTP, and 0.4% biocytin) to test for the possibility of GABAB responses, which require participation of K+ channel activity. The pH of the intracellular solution was adjusted to 7.3 with CsOH (or KOH in cases where we avoided Cs+) or gluconic acid, and the osmolality was 280–290 mOsm.
Recordings were obtained, often in pairs (see RESULTS), using an Axoclamp 2A amplifier in continuous single electrode voltage-clamp mode and an Axopatch 200B in voltage-clamp mode (Axon Instruments, Foster City, CA). The amplitudes of inhibitory postsynaptic currents (IPSCs) were maximized by holding the cells at 0 mV (Lam et al. 2005). The access resistance of the cells was constantly monitored throughout the recordings (>1 h each), and recordings were limited to neurons with a stable access of <30 M throughout the whole experiment. Spontaneous IPSCs were usually not frequent enough to interfere with the experiments; in rare cases that they were, the recording was delayed until these spontaneous events subsided.
The GABA antagonists SR 95531 and CGP 46381 were purchased from Tocris (Ellisville, MO). All the other chemicals were purchased from Sigma-Aldrich (St. Louis, MO).
Photostimulation
Data acquisition and photostimulation were controlled by a program in Matlab (MathWorks, Natlick, MA) developed in the laboratory of Karel Svoboda (Shepherd et al. 2003), who generously shared this with us. Nitroindolinyl (NI)-caged glutamate (Sigma-RBI; Canepari et al. 2001) was added to recirculating ACSF to a concentration of 0.39 mM during recording. Focal photolysis of the caged glutamate was accomplished by a pulsed UV laser (355 nm wavelength, frequency-tripled Nd:YVO4, 100-kHz pulse repetition rate; DPSS Lasers, San Jose, CA). Figure 1A is a schematic illustration of the optics: the laser beam was directed into the side port of an Olympus microscope (BX50WI) using UV-enhanced aluminum mirrors (Thorlabs, Newton, NJ) and a pair of mirror galvanometers (Cambridge Technology, Cambridge, MA) and focused onto the brain slice with a low-magnification objective (4x0.1 Plan, Olympus). Angles of the galvanometers were computer controlled and determined the position stimulated by the laser. The optics were designed to generate a nearly cylindrical beam in the slice so as to keep the mapping two dimensional (Shepherd et al. 2003). The Q-switch of the laser and a shutter (LS3-ZM2, Vincent Associate, Rochester, NY) controlled the timing of the laser. A variable neutral density wheel (Edmund, Barrington, NJ) attenuated the intensity of the laser to enable us to control the power of the laser at different levels during experiments. A thin microscope coverslip in the laser path reflected a small portion of the laser onto a photodiode. The current from this photodiode was amplified, acquired by the computer, and used to monitor the laser intensity throughout the experiment. During the setup and calibration of the optics, the laser powers corresponding to several levels of current output from the diodes were measured by a power meter (Thorlabs) at the back focal plane of the objectives. These data were used to plot a calibration curve, which in turn was used to provide the laser power estimates in this paper. Because the microscope objective blocks part of the laser path, we estimate that the power at the specimen is about 40% of that of the back focal plane.
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In related experiments, the pathway from relay cells of the ventral posterior lateral nucleus to the thalamic reticular nucleus and back to the relay cells was studied by photostimulation of regions containing the recorded relay cell, using the same stimulation protocol as described above.
Data analysis
Responses were analyzed using programs written in Matlab. Pearson’s correlations were calculated with Origin (Microcal, Northampton, MA). IPSCs evoked directly from the thalamic reticular nucleus were quantified by the total area under the traces (after being smoothed by1-ms moving average) within 100 ms after laser stimulation. This was not appropriate for the disynaptic IPSCs evoked from photostimulation in the ventral posterior lateral nucleus, because this typically evoked a depolarization/IPSC sequence. Thus for these experiments, we measured the peak values of the evoked IPSCs. An equation similar to the calculation of the center of mass of a two-dimensional object was used to locate the centroid of the area of the thalamic reticular nucleus within which photostimulation elicited IPSCs.
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and 
i are the coordinates of the centroid and stimulation positions, respectively, in vector form. Ri is the size of the IPSC response measured by the area under the curve or peak value of the smoothed traces. In nonvector form, the equation becomes
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For presentation of the reticular input maps, traces of 150 ms recording immediately after the photostimulation were overlaid on top of a photomicrograph of the slice and pipettes (see RESULTS). Some of the photomicrographs were taken without using differential infrared-contrast (DIC) and brain regions including an extensive fiber representation, such as the internal capsule or ventral posterior lateral nucleus, thus appeared dark because of the high contrast settings of the video camera (e.g., Figs. 1, 6, and 7). The above-mentioned traces were arranged into a 24 x 8 array and placed where the laser was focused during the stimulation, so that the reticular area that projected to the recorded neuron could be visualized as that with a large upward current (IPSCs) in these traces. We refer to these afferent areas as "footprints." The centroid of the footprint is indicated in the figures with a red, blue, or black dot. Areas where the responses were >20% of the peak were interpolated using programs written in Matlab and surrounded by a red, blue, or black line. The reported areas of the resultant polygons were also calculated using Matlab. In cases where the polygons were too large and cut off, only the area inside the field of view was included. Differences in data (e.g., between the long and short axes of reticular footprints, areas of these footprints, and regions in which disynaptic relay cell-to-reticular-to-relay cell responses were elicited) were compared using a Student’s t-test. The topographical arrangement of the reticular input was tested by calculating the Pearson correlation between the coordinates of the recording pipette and the centroid of the reticular footprint.
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RESULTS |
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Direct activation of neurons of the thalamic reticular nucleus
An example of the response of a reticular neuron to the direct photostimulation of the thalamic reticular nucleus, seen as an immediate inward current, is shown in Fig. 2. At the laser power used, the response to the photostimulation was evoked only from a small area around the soma, and this was seen in all four reticular cells studied. In two of these cells, in addition to this direct response to stimulation near the soma (Fig. 2B, red, top trace), we also were able to evoke an additional outward current (or IPSC; Fig. 2B, green, bottom trace), but again, only from photostimulation near the soma. In none of the four reticular cells did we see any evidence of long-ranged synaptic or electrical connections that could compromise the spatial specificity of photostimulation.
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Photostimulation in the thalamic reticular nucleus elicited large outward currents, or IPSCs, in recorded relay cells. Figure 3 shows that the evoked IPSCs are GABAergic, because they are blocked by the GABAA antagonist SR95531, and this control was seen in five other cells tested for the direct reticulothalamic pathway. Finally, six cells were recorded without Cs+ in the electrode (see METHODS) to detect the possible presence of a GABAB component to the IPSCs evoked by reticular photostimulation. As exemplified by Fig. 4, in each of these cells, we found evidence for such a response, because in the presence of the GABAA antagonist SR95531, reticular photostimulation evoked long, slow IPSCs, with peaks of 25.1 ± 28.5 (SD) and a range of 2–80 pA that were reversibly blocked by the GABAB antagonist, CGP46381.
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The only exception to the single elliptical footprint consisted of one neuron for which we saw two nearby footprints (see Fig. 6B). This result is included in our analyses and is shown separately as red circles in Figs. 7D and 9, B and C. In any case, exclusion of this pair of cells from the data set had no affect on the statistical evaluations.
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The topographical relationship of the reticular inputs to the ventral posterior lateral relay cells was studied using simultaneous recordings of pairs of relays cells while photostimulation was applied to the thalamic reticular nucleus. These pairs were recorded in either a "horizontal" configuration, in which both cells were approximately equally distant from the border with the thalamic reticular nucleus (Fig. 7), or a "vertical" one, in which they were located along an axis perpendicular to this border (Fig. 8).
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Figure 8 is an example of the recordings from a pair of cells in the vertical configuration. Results from the two cells are shown in Fig. 8, A (blue star) and B (red star), respectively. Their reticular inputs are shown together in Fig. 8C for comparison. Figure 8D summarizes the correlation between the separation of the footprints and recorded cells for 13 pairs. The correlation is significant (r = +0.68, df = 12, P < 0.05, Fig. 8D), again indicating topography in the reticulothalamic pathway.
For comparison across experiments, the top left corner of the pattern of photostimulation in the thalamic reticular nucleus was assigned a coordinate (0,0; this is indicated by the gray open arrow in Fig. 1B and by the arrow and black star in Fig. 9A); the coordinates of the recorded ventral posterior lateral relay cells and the centroid of their reticular inputs were measured accordingly. These coordinates are plotted as connected circles in Fig. 9A; the exception in Fig. 6B is plotted as red triangles. A picture of one of the brain slices was overlaid in this relative plotting for reference; however, this is not precise because the dimensions and shapes varied from experiment to experiment. Figure 9B shows the correlation between the locations of the relay cells and their reticular inputs for the axis parallel to the reticular border, and Fig. 9C does the same for the axis perpendicular to this border. In both cases, the correlations are significant (r = +0.52, Fig. 9B; r = +0.58, Fig. 9C; df = 51, P < 0.0001 for both).
Pattern of relay cell-to-reticular-to-relay cell projections
As a supplement to the maps described above, we tried to establish the footprint of the inhibitory influence of ventral posterior lateral relay cells on their neighbors. Because there are virtually no interneurons in the rat ventral posterior lateral nucleus (Arcelli et al. 1997), we conclude that IPSCs evoked in recorded relay cells from photostimulation of their neighbors results from a relay cell-to-reticular-to-relay cell pathway. In this fashion, we recorded the evoked IPSCs to neighborhood photostimulation for 25 relay cells in the ventral posterior lateral nucleus. For these recorded cells, we also determined the footprint in the thalamic reticular nucleus by photostimulation there as described above. Figure 10 shows examples of the data obtained. Photostimulation elicited an inward, depolarizing current in the area 50–100 µm around the recorded cell (Fig. 10, B, and D, purple and green traces), presumably because of direct photostimulation of the dendritic arbor of the recorded cell (the reversal potential of the glutamatergic currents was slightly more depolarized than the holding potential, 0 mV, in our recording). However, more interestingly, in all but one case, we saw IPSCs with longer delays riding on top of such direct depolarization (Fig. 10, B and D, green and blue traces). Moreover, IPSCs were typically (24 of 25 cells) elicited in a larger area around the cell, where direct depolarization from the photostimulation could not be detected (Fig. 10, B and D, blue traces). This we regard as the area from which nearby relay cells inhibit the recorded cell through the thalamic reticular nucleus. Our interpretation that this reflects activation of a disynaptic pathway means that photostimulation of the relay cells activates them strongly enough to create action potentials, and not just excitatory postsynaptic potentials (EPSPs), in their postsynaptic reticular targets.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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; Guillery et al. 1998). We found that, in the horizontal slice, the topography was clear in both mediolateral and anteroposterior directions (Fig. 9). However, these footprints were oval with the long axis parallel to the border between the thalamic reticular and the ventral posterior lateral nuclei (Figs. 5, 7, and 8). This may reflect the fact that reticular cells have disk-shaped dendritic arbors, with the long axis running parallel to this border (Lübke 1993; Pinault et al. 1995a,b; Scheibel and Scheibel 1966; Yen et al. 1985), so that there may thus be more area in this dimension parallel to the border to photostimulate given reticular neurons.
Although there is anatomical evidence that some reticulothalamic axons form diffuse arbors (Cox et al. 1996), we found no such examples. Perhaps this is because any such diffusely projecting reticular cells form weak and unreliable connections (Cox et al. 1996) that are not readily detected with photostimulation. It has also been argued that such diffuse projections of reticular cells existed only transiently in developing animal (Pinault 2004). Our data add little to this controversy, but it does show that, functionally, the reticular projection to ventral posterior lateral relay cells in rat is already predominately topographical even at ages as young as 10 days old.
We were also able, with photostimulation, to show both GABAA and GABAB components to the IPSCs evoked from reticular activation (Figs. 3 and 4), suggesting that the photostimulation strongly activates reticular cells. In general, photostimulation evokes responses that are quite similar to those evoked by electrical stimulation in paired recordings (e.g., Kim et al. 1997). We thus conclude that photostimulation can be a reliable method for specifically stimulating the soma and dendrites of a neuron without affecting axons en passage in complex brain regions.
In limited experiments, we were also able to show at least some local, inhibitory interconnections between reticular cells that appear to be synaptic, although we did not thoroughly study this feature. We did not find evidence of strong electrical coupling between reticular neurons (Landisman et al. 2002) perhaps because these synapses exist only between neurons within a limited distance (<40 µm; Long et al. 2004) that is below the resolution of our maps, and this suggests that such coupling that is present did not greatly affect our topographical results.
Functional significance
Our experiments testing the topography of the relay cell-to-reticular-to-relay cell pathway (e.g., Fig. 10) is interesting for at least two reasons beyond the simple demonstration of topography. First, as noted in the RESULTS, our data indicate that photostimulation of relay cells must activate them sufficiently that they produce firing in the postsynaptic reticular neurons. This is consistent with evidence both that EPSPs generated in reticular cells from relay cells of the ventral posterior lateral nucleus are relatively large with a low failure rate (Gentet and Ulrich 2003, 2004) and that terminals from these relay cells are relatively large and proximally located on reticular cell dendrites (Liu and Jones 1999; Ohara and Lieberman 1981, 1985). In the parlance of Sherman and Guillery (1998), these observations suggest that relay cell inputs to these reticular cells are drivers, rather than modulators, meaning that these inputs convey the main information that is represented by the receptive fields of reticular cells.
Second, the zones of the ventral posterior lateral nucleus within which photostimulation evokes disynaptic IPSCs in relay cells are clearly larger than the footprints for monosynaptic photostimulation in the thalamic reticular nucleus; they are also considerably larger than the extent of the dendritic arbors of the relay cells (identified by a direct depolarizing response to photostimulation as in Fig. 10, B and D; detailed analysis not shown). As just noted, relay cells tend to innervate reticular cells proximally. There are two connectivity patterns suggested by Fig. 12 that could account for this; note that a combination of these patterns is also possible. (Chemical and electrical synapses between reticular neurons will be not discussed in detail, because they are beyond the scope of the reported results, but they are suggested here by double-headed arrows.) One (Fig. 12A) is that there is more spatial spread among thalamoreticular axon arbors than among reticulothalamic ones. The other (Fig. 12B) is related to the fact that there are more relay than reticular cells: this proposes that a spread of relay cells converges onto each reticular cell. Note that both circuits require relatively little convergence in the reticulothalamic projection, which is suggested by the small reticulothalamic footprints seen with photostimulation. While there is substantial anatomical evidence for restricted reticulothalamic arbors (Cox et al. 1996; Pinault and Deschênes 1998; Uhlrich et al. 1991), thalamoreticular arbors, which typically emanate as very thin collaterals of the thalamocortical axons, tend to be difficult to label completely, and thus the anatomical correlate we suggest has not yet been adequately resolved.
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Our data also indicate local synaptic connections between reticular cells as well as a surprisingly strong pathway providing inhibition through the thalamic reticular nucleus from relay cells to neighboring relay cells. Thus the thalamic reticular nucleus could provide a mechanism of lateral inhibition between relay cells that serves to sharpen sensory processing through the thalamus.
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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ACKNOWLEDGMENTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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FOOTNOTES |
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Address for reprint requests and other correspondence: S. M. Sherman, Dept. of Neurobiology, Pharmacology and Physiology, Univ. of Chicago, Chicago, IL 60637 (E-mail: msherman{at}bsd.uchicago.edu)
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REFERENCES |
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