Whole-cell voltage recordings were made in vivo from subsequently reconstructed pyramidal neurons (n = 30) in layer 3 (L3) and layer 2 (L2) of the barrel cortex of urethane-anaesthetised rats. Average resting membrane potentials were well below (15-40 mV) action potential (AP) initiation threshold. The average spontaneous AP activity (0.068 +/- 0.22 APs s-1) was low. Principal whisker (PW) deflections evoked postsynaptic potentials (PSPs) in almost all cells of a PW column but evoked AP activity (0.031 +/- 0.056 APs per PW stimulus 6 deg deflection) was low indicating 'sparse' coding by APs. Barrel-related cells (n = 16) have their soma located above a barrel and project their main axon through the barrel whereas septum-related cells (n = 8) are located above and project their main axon through the septum between barrels. Both classes of cell had broad subthreshold receptive fields (RFs) which comprised a PW and several (> 8) surround whiskers (SuW). Barrel-related cells had shorter PSP onset latencies (9.6 +/- 4.6 ms) and larger amplitude PW stimulus responses (9.1 +/- 4.5 mV) than septum-related cells (23.3 +/- 16.5 ms and 5.0 +/- 2.8 mV, respectively). The dendritic fields of barrel-related cells were restricted, in the horizontal plane, to the PW column width. Their axonal arbors projected horizontally into several SuW columns, preferentially those representing whiskers of the same row, suggesting that they are the major anatomical substrate for the broad subthreshold RFs. In barrel-related cells the response time course varied with whisker position and subthreshold RFs were highly dynamic, expanding in size from narrow single-whisker to broad multi-whisker RFs, elongated along rows within 10-150 ms following a deflection. The response time course in septum-related cells was much longer and almost independent of whisker position. Their broad subthreshold RF suggests that L2/3 cells integrate PSPs from several barrel columns. We conclude that the lemniscal (barrel-related) and paralemniscal (septum-related) afferent inputs remain anatomically and functionally segregated in L2/3.

Whole-cell voltage recordings were made in vivo from excitatory neurons (n = 23) in layer 4 of the barrel cortex in urethane-anaesthetised rats. Their receptive fields (RFs) for a brief whisker deflection were mapped, the position of the cell soma relative to barrel borders was determined for 15 cells and dendritic and axonal arbors were reconstructed for all cells. Three classes of neurons were identified: spiny stellate cells and pyramidal cells located in barrels and pyramidal cells located in septa. Dendritic and, with some exceptions, axonal arborisations of barrel cells were mostly restricted to the borders of a column with a cross sectional area of a barrel, defining a cytoarchitectonic barrel-column. Dendrites and axons of septum cells, in contrast, mostly extended across barrel borders. The subthreshold RFs measured by evoked postsynaptic potentials (PSPs) comprised a principal whisker (PW) and several surround whiskers (SuWs) indicating that deflection of a single whisker is represented in multiple barrels and septa. Barrel cells responded with larger depolarisation to stimulation of the PW (13.7 +/- 4.6 mV (mean +/- S.D.), n = 10) than septum cells (5.7 +/- 2.4 mV, n = 5), the gradient between peak responses to PW and SuW deflection was steeper and the latency of depolarisation onset was shorter (8 +/- 1.4 ms vs. 11 +/- 2 ms). In barrel cells the response onset and the peak to SuW deflection was delayed depending on the distance to the PW thus indicating that the spatial representation of a single whisker deflection in the barrel map is dynamic and varies on the scale of milliseconds to tens of milliseconds. Septum cells responded later and with comparable latencies to PW and SuW stimulation. Spontaneous (0.053 +/- 0.12 action potentials (APs) s(-1)) and evoked APs (0.14 +/- 0.29 APs per principal whisker (PW) stimulus) were sparse. We conclude that PSPs in ensembles of barrel cells represent dynamically the deflection of a single whisker with high temporal and spatial acuity, initially by the excitation in a single PW-barrel followed by multi-barrel excitation. This presumably reflects the divergence of thalamocortical projections to different barrels. Septum cell PSPs preferably represent multiple whisker deflections, but less dynamically and with less spatial acuity.

Whole-cell voltage recordings were made in vivo in the ventral posterior medial nucleus (VPM) of the thalamus in urethane-anaesthetised young (postnatal day 16-24) rats. Receptive fields (RFs) on the whisker pad were mapped for 31 neurones, and 10 cells were recovered for morphological reconstruction of their dendritic arbors. Most VPM neurones had antagonistic subthreshold RFs that could be divided into excitatory and inhibitory whiskers. VPM cells comprised different classes, the most frequently occurring being single-whisker excitation (SWE) and multi-whisker excitation (MWE) cells. In SWE cells (36 % of VPM neurones), only principal whisker (PW) deflection evoked an EPSP and was followed by a single action potential (AP) or remained subthreshold. The depolarisation was terminated by a large, delayed IPSP. A stimulus evoked on average 0.74 +/- 0.46 APs (mean +/- S.D.) with short latency (8.1 +/- 1.0 ms) and small temporal scatter (0.31 +/- 0.23 ms dispersion of 50 % of the first APs). In MWE cells (29 % of VPM neurones), deflection of several whiskers evoked EPSPs. PW responses were either subthreshold EPSPs or consisted of an EPSP followed by one or several APs (0.96 +/- 0.99 APs per stimulus). AP responses were often associated with putative low-threshold calcium-dependent regenerative potentials and were followed by a small delayed IPSP. AP responses had a longer latency (12.3 +/- 2.6 ms) and larger temporal scatter (2.5 +/- 1.6 ms) than responses of SWE cells. MWE cells had a lower input resistance than SWE cells. The elongation of dendritic arbors along the representation fields of rows and arcs in VPM barreloids was weakly correlated with the subthreshold RF elongation along whisker rows and arcs, respectively. Evoked EPSP-AP responses exhibited a sharper directional tuning than subthreshold EPSPs, which in turn exhibited a sharper directional tuning than IPSPs. In conclusion, we document two main classes of VPM neurones. SWE cells responded with a precisely timed single AP to the deflection of the PW. In contrast, MWE cell RFs were more broadly tuned and the temporally dispersed multiple AP responses of these cells represented the degree of collective deflection of the PW and several adjacent whiskers.