Vibrissal responses of thalamic cells that project to the septal columns of the barrel cortex and to the second somatosensory area

Abstract

The rodent somatosensory cortex contains barrel-related and septa-related circuits representing two separate streams of vibrissa information processing that differ in their response patterns and anatomical connections. Whereas barrel-related circuits process lemniscal inputs that transit through the thalamic barreloids, septa-related circuits process paralemniscal inputs and inputs that are relayed through the ventral lateral part of the ventral posterior medial nucleus (VPMvl). Septa-projecting thalamic afferents also target the secondary somatosensory cortical area. Although a number of studies have examined response properties in the lemniscal pathway, and demonstrated that barreloids receive feedback from specific sets of corticothalamic and reticular thalamic neurons, such information is currently lacking for the VPMvl. In the present study, we show that in sharp contrast to the relay cells of the barreloids VPMvl neurons exhibit large multiwhisker receptive fields that are independent of input from the principal trigeminal nucleus. Results also suggest that the topography of receptive fields and response properties in VPMvl rely on converging input from neurons of the interpolaris trigeminal nucleus. Tracer injection and single-cell labeling further reveal that the VPMvl receives input from specific populations of reticular thalamic and corticothalamic neurons. Together, these results confirm the status of the VPMvl as a thalamic relay of an independent parallel pathway of vibrissa information processing. They further indicate that a sensory pathway does not merely consist on a three-neuron chain that links the vibrissae to the cerebral cortex, but that it also involves specific sets of topographically related corticothalamic and reticular thalamic projections.

Figure 1.

Receptive field size of vibrissa-sensitive units in the somatosensory thalamus. A, Receptive field size of cells recorded along five vertical electrode tracks in the VPM in a rat (dark blue dots, monowhisker cells; light blue dots, multiwhisker cells in dorsal VPM; purple dots, multiwhisker cells in VPMvl; gray dots, cells that responded to stimulation of the forelimb). Vibrissae within the receptive field of each unit are identified next to each dot. B, VPMvl cell labeled with Neurobiotin (arrow). The location of this unit is indicated by an asterisk in A (tract 4), and the same cell is shown at higher magnification in B₁. C, Location of 10 labeled multiwhisker cells on a representative coronal section of the thalamus (∼3.8 mm behind the bregma) (drawing modified from Paxinos and Watson, 1998). Scale bars: B, 1 mm; B₁, 100 μm.

Figure 2.

Effect of PrV lesion on receptive field size of VPMvl units. A, Extent of an electrolytic lesion that severed ascending axons from the PrV. The frontal plane of each costained section is indicated below (Br, bregma). B, C, Population PSTHs of vibrissal responses in normal and lesioned rats, respectively (sum of all responses to all directions; 18 cells in B, 12 cells in C). The higher level of background activity in C was caused by juxtacellular current that was applied to assess the presence of inhibition in some cells. Prestimulus background activity in B and C was subtracted from the poststimulus counts to compare the magnitude and latency of responses. Scale bar, 3 mm.

Figure 3.

Response properties and directional tuning of multivibrissa VPMvl cells. A, B, Three-dimensional bar graphs of normalized response magnitudes within the receptive field of two VPMvl cells. For each vibrissa, response magnitudes were summed across all directions. Bars with zero magnitude (B1 and C1 in the bottom graph, for example) indicate vibrissae of a threshold too high to be tested with the piezo stimulator. Polar plots in A1 and A2 show normalized response magnitudes for the same two units after deflection of each vibrissa in four cardinal directions. C, Angular tuning preference of VPMvl cells. Each vector is the vector sum of all vibrissa-associated vectors within the receptive field of a cell (17 cells). Vector length corresponds to the normalized magnitude of angular preference among a population of 17 VPMvl cells.

Figure 4.

Axonal projections of multivibrissa RT cells. A, Population PSTH of vibrissal responses recorded in six multiwhisker units (sum of all responses to all directions). Dots in B indicate the location of five multiwhisker RT units labeled with Neurobiotin. The RT cell labeled in C was reconstructed from serial sections, and drawings in D–F show horizontal (D), coronal (E), and sagittal (F) views of the dendritic and axonal arbors. Note that the axonal arbor is mostly restricted to the VPMvl, with a few collaterals in Po. E₁, Axonal branches and boutons (arrowheads) within the framed area in E. Photomicrograph in E₂ show a cluster of corticothalamic boutons in the VPMvl (arrowheads). A, Anterior; D, dorsal; eml, external medullary lamina; M, medial. Scale bars: B, 1 mm; C–F, 200 μm; E₁, 10 μm; E₂, 25 μm.

Figure 5.

Retrograde labeling in the cerebral cortex after FluoroGold injection in the VPMvl. The injection site shown in A led to retrograde labeling of layer 6 cells in S1 and S2 (B). Clusters of labeled cells in S1 and S2 are shown at higher magnification in C and D, respectively. Asterisks indicate coreactive barrels. E, Distribution of retrogradely labeled cells in S1 and S2 on representative sections taken at different frontal planes (drawings adapted from Paxinos and Watson, 1998) [distance from the bregma (Br) as indicated; gray patches, barrels]. AuD; Dorsal auditory cortex; I, insular cortex; S1BF, barrel field of S1; S1DZ, dysgranular zone of S1; ZI, zona incerta. Scale bars: A, B, 1 mm; C, D, 500 μm.

Figure 6.

Corticothalamic cells in S2 project to the VPMvl. A–G, Distribution of corticothalamic terminals (white patches) in representative sections through the somatosensory thalamus after an injection of BDA in the infragranular layers of S2 (H; asterisks, barrels). Note that corticothalamic terminals form two separate clusters: one in Po and the other one in VPMvl (arrows in the photomicrograph in I). The terminal field in VPMvl is shown at higher magnification in J. K, Higher magnification of the framed area in J. Note the drumstick like boutons (arrows) given off en passant by the fine branches of corticothalamic axons. Ang, Angular thalamic nucleus; Br., bregma. Scale bars: A–I, 500 μm; H, 1 mm; J, 200 μm; K, 20 μm.