Experience-dependent increase in spine calcium evoked by backpropagating action potentials in layer 2/3 pyramidal neurons in rat somatosensory cortex

Rats rhythmically sweep their whiskers over object features, generating sequential deflections of whisker arcs. Such moving wavefronts of whisker deflection are likely to be fundamental elements of natural somatosensory input. To determine how moving wavefronts are represented in somatosensory cortex (S1), we measured single- and multiunit neural responses in S1 of anesthetized rats to moving wavefronts applied through a piezoelectric whisker deflector array. Wavefronts consisted of sequential deflections of individual whisker arcs, which moved progressively across the whisker array. Starting position (starting arc), direction, and velocity of wavefronts were varied. Neurons responded strongly only when wavefront starting position included their principal whisker (PW). When wavefronts started at neighboring positions and swept through the PW, responses to the PW arc were suppressed by ≤95%, and responses over the entire wavefront duration were suppressed by ≤60% compared with wavefronts that initiated with the PW. Suppression occurred with interarc deflection delays of ≥5 ms, was maximal at 20 ms, and recovered within 100–200 ms. Suppression of PW arc responses during wavefronts was largely independent of wavefront direction. However, layer 2/3 neurons showed direction selectivity for responses to the entire wavefront (the entire sequence of SW and PW arc deflection). Wavefront direction selectivity was correlated with receptive field somatotopy and reflected differential responses to the specific SWs that were deflected first in a wavefront. These results indicate that suppressive interwhisker interactions shape responses to wavefronts, resulting in increased salience of wavefront starting position, and, in some neurons, preference for wavefront direction.

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Lack of Depolarization-Induced Suppression of Inhibition (DSI) in Layer 2/3 Interneurons That Receive Cannabinoid-Sensitive Inhibitory Inputs

Journal of Neurophysiology ◽

10.1152/jn.00817.2007 ◽

2007 ◽

Vol 98 (5) ◽

pp. 2517-2524 ◽

Cited By ~ 9

Author(s):

Fouad Lemtiri-Chlieh ◽

Eric S. Levine

Keyword(s):

Action Potentials ◽

Pyramidal Neurons ◽

Cannabinoid Receptor ◽

Brain Slices ◽

Gaba Release ◽

Synaptic Activity ◽

Layer 2 ◽

Fast Spiking ◽

Whole Cell Recordings

In layer 2/3 of neocortex, brief trains of action potentials in pyramidal neurons (PNs) induce the mobilization of endogenous cannabinoids (eCBs), resulting in a depression of GABA release from the terminals of inhibitory interneurons (INs). This depolarization-induced suppression of inhibition (DSI) is mediated by activation of the type 1 cannabinoid receptor (CB1) on presynaptic terminals of a subset of INs. However, it is not clear whether CB1 receptors are also expressed at synapses between INs, and whether INs can release eCBs in response to depolarization. In the present studies, brain slices containing somatosensory cortex were prepared from 14- to 21-day-old CD-1 mice. Whole cell recordings were obtained from layer 2/3 PNs and from INs classified as regular spiking nonpyramidal, irregular spiking, or fast spiking. For all three classes of INs, the cannabinoid agonist WIN55,212-2 suppressed inhibitory synaptic activity, similar to the effect seen in PNs. In addition, trains of action potentials in PNs resulted in significant DSI. In INs, however, DSI was not seen in any cell type, even with prolonged high-frequency spike trains that produced calcium increases comparable to that seen with DSI induction in PNs. In addition, blocking eCB reuptake with AM404, which enhanced DSI in PNs, failed to unmask any DSI in INs. Thus the lack of DSI in INs does not appear to be due to an insufficient increase in intracellular calcium or enhanced reuptake. These results suggest that layer 2/3 INs receive CB1-expressing inhibitory inputs, but that eCBs are not released by these INs.

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