The Influence of Single VB Thalamocortical Impulses on Barrel Columns of Rabbit Somatosensory Cortex

Abstract

Extracellular recordings were obtained from single neurons in ventrobasal (VB) thalamus of awake rabbits while field potentials were recorded at various depths within topographically aligned and nonaligned barrel columns of somatosensory cortex (S1). Spike-triggered averages of cortical field potentials were obtained following action potentials in thalamic neurons. Action potentials in a VB neuron elicited a cortical response within layer 4 with three distinct components. 1) A biphasic, initially positive response (latency <1 ms) was interpreted to reflect activation of the VB axon terminals (the AxTP). This response was not affected by infusion of an alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA)/kainate receptor antagonist within the barrel. In contrast, later components of the response were completely eliminated and were interpreted to reflect focal synaptic potentials. 2) A negative potential [focal synaptic negativity (FSN)] occurred at a mean latency of 1.65 ms and lasted approximately 4 ms. This response had a rapid rise time ( approximately 0.7 ms) and was interpreted to reflect monosynaptic excitation. 3) The third component was a positive potential (the FSP), with a slow rise time and a half-amplitude duration of approximately 30 ms. The FSP showed a weak reversal in superficial cortical layers and was interpreted to reflect di/polysynaptic inhibition. The amplitudes of the AxTP, the FSN, and the FSP reached a peak near layer 4 and were highly attenuated in both superficial and deep cortical layers. All components were attenuated or absent when the cortical electrode was missaligned from the thalamic electrode by a single cortical barrel. Deconvolution procedures revealed that the autocorrelogram of the presynaptic VB neuron had very little influence on either the amplitude or duration of the AxTP or the FSN, and only a minor influence (mean, 11%) on the amplitude of the FSP. We conclude that individual VB thalamic impulses entering a cortical barrel engage both monosynaptic excitatory and di/polysynaptic inhibitory mechanisms. Putative inhibitory interneurons of an S1 barrel receive a highly divergent/convergent monosynaptic input from the topographically aligned VB barreloid, and this results in sharp synchrony among these interneurons. We suggest that single-fiber access to disynaptic inhibition is facilitated by this sharp synchrony, and that the FSP reflects a consequent synchronous wave of feed-forward inhibition within the S1 barrel.

Selective, State-Dependent Activation of Somatostatin-Expressing Inhibitory Interneurons in Mouse Neocortex

“…Thus they seem to be ideal for responding to sudden, brief changes in cortical activity such as incoming sensory information (Simons 1978;Simons and Carvell 1989;Swadlow and Gusev 2000;Swadlow et al 1998), but not to slow changes in ongoing activity. In this respect, they act as a sort of filter of incoming excitatory activity, faithfully transmitting abrupt increases in input, but not persistent firing (Abbott and Regehr 2004).…”

“…Inhibition plays important roles in the feedforward control of sensory information (Cruikshank et al 2007;Simons 1978;Simons and Carvell 1989 ;Swadlow and Gusev 2000;Swadlow et al 1998), the overall control of cortical tone (ChagnacAmitai and Connors 1989), the generation of oscillatory activity at a range of frequencies (Beierlein et al 2000;Blatow et al 2003;Whittington et al 1995), and synchronization of spiking in excitatory pyramidal neurons (Cobb et al 1995;Long et al 2005). However, it has been very difficult to assign particular cortical functions to specific interneuron types.…”

Balanced Excitation and Inhibition Determine Spike Timing during Frequency Adaptation

“…In the rodent whisker system, ascending thalamic input engages neuronal circuits in cortical layer 4 (L4), consisting of excitatory spiny stellate and pyramidal cells as well as aspiny interneurons (White and Rock, 1981;Beierlein et al, 2002Beierlein et al, , 2003Bruno and Simons, 2002) that provide feedforward and feedback inhibition to the local network (Agmon and Connors, 1991;Swadlow and Gusev, 2000;Porter et al, 2001;Swadlow, 2003;Staiger et al, 2004). This functional architecture leads to a precise sequence of excitation followed by inhibition in response to whisker deflection that may serve to sharpen the spike timing of suprathreshold responses and limit the time for integration of excitatory inputs (Pinto et al, 2000(Pinto et al, , 2003Pouille and Scanziani, 2001;Wehr and Zador, 2003;Wilent and Contreras, 2004;Blitz and Regehr, 2005;Mittmann et al, 2005).…”

Diverse Types of Interneurons Generate Thalamus-Evoked Feedforward Inhibition in the Mouse Barrel Cortex

“…The short latency of the inhibitory response indicates that the inhibitory interneurons eliciting it must be excited directly by the thalamocortical afferents, consistent with anatomical data (White, 1978;Fairén and Valverde, 1979;Freund et al, 1985;Keller and White, 1987), and in turn inhibit other cortical neurons disynaptically. This feedforward inhibition is a highly robust feature that can be engaged by even a single thalamocortical action potential (Swadlow and Gusev, 2000), can influence the spread of thalamocortically evoked excitation, and can shape the cortical representation of the sensory environment (Sillito, 1975;Tsumoto et al, 1979;Sillito et al, 1980;Hicks and Dykes, 1983;Dykes et al, 1984;Kyriazi et al, 1996;Kyriazi et al, 1998).…”