Synaptic Responses to Whisker Deflections in Rat Barrel Cortex as a Function of Cortical Layer and Stimulus Intensity

Abstract

To study the synaptic and spike responses of barrel cortex neurons as a function of cortical layer and stimulus intensity, we recorded intracellularly in vivo from barbiturate anesthetized rats while increasing the velocity-acceleration of the whisker deflection. Granular (Gr; layer 4) cells had the EPSP with the shortest peak and onset latency, whereas supragranular (SGr; layers 2-3) cells had the EPSP with longest duration and slowest rate of rise. Infragranular (Igr; layers 5-6) cells had intermediate values, and thus each layer was unique. The spike response peak of Gr cells was followed by IGr and then by SGr cells. In all cells, depolarization reduced the duration and amplitude of the response, but only in Gr cells did it reveal an early IPSP that cut short the EPSP. This early IPSP was associated with a large decrease in input resistance and an apparent reversal potential below spike threshold; consequently, synaptic integration in Gr cells was limited to the initial 5-7 msec of the response. In contrast, in SGr and IGr cells, results suggest an overlap in time of the EPSP and IPSP, with a small drop in input resistance and an apparent reversal potential above spike threshold, facilitating input integration for up to 20 msec. Decreasing stimulus intensity (velocity-acceleration) reduced the amplitude and increased the peak latency of the response without altering its synaptic composition. We propose that layer 4 circuits are better suited to perform coincidence detection, whereas supra and infragranular circuits are better designed for input integration.

Stimulus-Dependent Changes in Spike Threshold Enhance Feature Selectivity in Rat Barrel Cortex Neurons

“…Similar to what is reported in other intracellular studies performed in this system (Moore and Nelson, 1998;Brecht and Sakmann, 2002;Higley and Contreras, 2003;Wilent and Contreras, 2004), a small number of spikes per stimulus (0.28 spikes per stimulus) was evoked by the PD at the resting V m (Ϫ72 Ϯ 5 mV). Therefore, we measured the spike responses while cells were slightly depolarized (7-12 mV above rest; average V m ϭ Ϫ63 Ϯ 3 mV) with square current pulses (ϩ0.1 to ϩ0.3 nA) of 0.6 s duration and starting 0.2 s before each whisker deflection.…”

“…Other factors determining the rate of rise of the synaptic response include concomitant inhibitory input (Wehr and Zador, 2003;Wilent and Contreras, 2004), the degree of synchronization of the excitatory input, and the location of synapses on the somatodendritic membrane. Inhibitory input may simply add linearly to the excitatory input and decrease the slope of the synaptic response, or it may shunt excitatory input by increasing membrane conductance without necessarily causing hyperpolarization (Borg-Graham et al, 1998;Hirsch et al, 1998).…”

“…Inhibitory input may simply add linearly to the excitatory input and decrease the slope of the synaptic response, or it may shunt excitatory input by increasing membrane conductance without necessarily causing hyperpolarization (Borg-Graham et al, 1998;Hirsch et al, 1998). The degree of synchronization of thalamocortical input has been shown previously to play a key role for the encoding of velocity/acceleration in layer 4 of barrel cortex (Pinto et al, 2000(Pinto et al, , 2003, which results in an increase in dV m /dt of the synaptic response (Wilent and Contreras, 2004). A similar role for thalamocortical input synchronization in the encoding of direction has been suggested by the increase in the amplitude of local field potentials recorded in thalamic barreloids to preferred versus nonpreferred directions (Temereanca and Simons, 2003) and by the dependence of angular tuning on deflection velocity (Lee and Simons, 2004).…”

“…Before recording, whiskers were trimmed to a length of ϳ12 mm. Individual whiskers were deflected mechanically using ceramic piezoelectric bimorphs (Simons, 1983;Wilent and Contreras, 2004). Once a stable recording was obtained, the cell was depolarized moderately to facilitate whisker-evoked suprathreshold responses.…”

Layer-specific network oscillation and spatiotemporal receptive field in the visual cortex

“…This observation is consistent with previous findings in cortical slices that L5 inputs are located more proximally than L2/3 inputs (16,35), giving the L5 inputs greater control of postsynaptic responses. In the somatosensory cortex, the sensory response is also found to be more transient in L5 than in L2/3 (36,37), perhaps due to the same mechanism.…”