Activation of a cortical column by a thalamocortical impulse

Abstract

Thalamocortical (TC) impulses potently influence the sensory neocortex, but the functional impact of individual TC neurons throughout the layers of the cortex has proved difficult to assess. Here we examine, in awake rabbits, the vertical distribution of monosynaptic currents generated in a somatosensory cortical "barrel" column by spontaneous impulses of single, topographically aligned TC neurons. We show that closely neighboring TC neurons generate widely differing patterns of monosynaptic activation within layers 4 and 6 of their aligned column. Moreover, synaptic currents generated by TC impulses with long preceding interspike intervals are greatly enhanced in both of these layers. The degree of this enhancement differs reliably among neighboring TC neurons but, for a given neuron, is very similar in layers 4 and 6. Our results indicate that in the awake state, TC synapses throughout the depth of the cortex serve as powerful filters of sensory information that reflect individual characteristics of their parent TC neuron.

Fig. 1.

A, An illustrative case. Two independent microelectrodes in a thalamic barreloid are shown. During two recording sessions, three TC neurons were studied via each electrode (N1–N6). The cortical probe is in the aligned barrel, with deeper sites within layer 6. An example of CSD traces showing the axon-terminal potential and the postsynaptic current sink (arrows) and the synaptic delay (time between the onset of these two potentials) is shown on the right. Thevertical dashed line indicates the time of the TC spike.B, N1 and N2 show spike-triggered field and CSD profiles generated by two TC neurons (N1 and N2 in A) recorded simultaneously via one of the microelectrodes. The vertical dashed lines indicate the time of the TC spike. Colorized CSDs are shown below (color intensities reflect source and sink amplitudes).Bottom right, CSD profile generated by an air puff (200 presentations, note the long time base). Horizontal arrows in colorized CSDs here and in Figure 2 denote sites known to be within layer 6 (see Materials and Methods). Gains for N1 and N2 are identical and are 20 times higher than those used for the air-puff stimulus.

Fig. 2.

CSD profiles for six TC neurons projecting to a single column (same as in Fig. 1A). N1–N3 were recorded on one microelectrode, and N4–N6 were recorded on the second electrode. The profile generated by the air puff is shown for reference. Gain (and color) settings for all TC profiles are identical and are 20 times higher than those used for the air-puff stimulus. Thevertical dashed lines indicate the time of the TC action potential.

Fig. 3.

A, CSD profiles for another TC neuron. The control profile is shown on the left(n = ∼120,000 TC spikes), with an amplified view (gain is 3.5 times greater) of the responses in layer 4 (top horizontal arrows) and layer 6 (bottom horizontal arrows). Oblique arrows indicate axon-terminal responses. The colorized CSD profile is shown below.Middle profiles were generated by TC spikes with preceding interspike intervals of 250–500 msec (n= 2290). Profiles on the right were generated by initial spikes of TC bursts (n = 2427). Gain settings and color intensities for all CSDs are identical. The vertical dashed lines indicate the time of the TC action potential.B, The amplitude (peak–peak) of the axon-terminal response (left) and the magnitude of the initial 1 msec of the postsynaptic current sink (right) were plotted at different CSD sites as a function of preceding interspike interval. Control response and the response to the initial spike in a TC burst are also plotted.

Fig. 4.

A, For 11 TC neurons, the magnitude of postsynaptic current sinks generated in layer 4 by spikes with various preceding interspike intervals. B, For these same 11 neurons, the correlation between the response to TC spikes with preceding intervals of 250–500 msec and with preceding interspike intervals of >500 msec. C, The relationship for five TC neurons between the magnitude of the response in layers 4 and 6 at three preceding interspike intervals.