The Impact of an LGNd Impulse on the Awake Visual Cortex: Synaptic Dynamics and the Sustained/Transient Distinction

Abstract

We used spike-triggered current source-density analysis to examine axonal and postsynaptic currents generated in the visual cortex of awake rabbits by spontaneous spikes of individual sustained and transient dorsal lateral geniculate nucleus (LGNd) neurons. Using these data, we asked whether sustained/transient sensory responses are related to short-term synaptic dynamics at the thalamocortical synapse. Most sustained (34 of 40) and transient (24 of 25) neurons generated axonal and monosynaptic responses in layer 4 and/or 6 of the aligned cortical domain, with input from transient neurons arriving ϳ0.3 ms earlier and 100 -200 m deeper. Postsynaptic cortical responses generated by both thalamic cell classes were reduced in amplitude after a preceding impulse and slowly recovered over a period of Ͼ750 ms. We interpret this to reflect interval-dependent recovery from chronic depression at the thalamocortical synapse, caused by significant spontaneous firing of LGNd cells (ϳ8 Hz). Surprisingly, postsynaptic cortical responses generated by spontaneous spikes of sustained thalamic neurons were more depressed than those of transient neurons. This difference was seen both in layers 4 and 6. The depression saturated rapidly with multiple preceding impulses, and postsynaptic responses generated by sustained neurons during maintained visual stimulation remained sufficiently robust to allow a sustained flow of information to the cortex. Our results indicate a relationship between the sensory response properties of thalamic neurons and the short-term dynamics of their synapses, and suggest that cortical recipients of sustained and transient thalamic inputs will differ considerably in their response modulation by prior impulse activity.

Getting Drowsy? Alert/Nonalert Transitions and Visual Thalamocortical Network Dynamics

“…Consistent with our previous results for thalamocortical neurons (Swadlow and Gusev, 2001;Bezdudnaya et al, 2006;Stoelzel et al, 2008), LGNd neurons show abrupt reductions in spontaneous firing and increases in bursting when nonalert. Cortical layer 4 RS simple cells, the main recipients of the thalamic input, maintain constant rate of spontaneous spiking activity and ISI distributions throughout state transition.…”

“…We identified LGNd thalamocortical neurons using spike-triggered averages of axonal field potentials elicited in layers 4 and 6 of the retinotopically aligned region of V1 Jin et al, 2008;Stoelzel et al, 2008). Putative fast-spike interneurons (SINs) of layer 4 were identified by a high-frequency (Ͼ600 Hz) burst of three or more spikes elicited by electrical stimulation of afferent pathways.…”

“…Hippocampal EEG was monitored while neurons fired spontaneously. The EEG was segmented by visual inspection into alert versus nonalert states based on the presence of theta activity (5-7 Hz) or high-voltage, irregular activity, respectively (Swadlow and Gusev, 2001;Bezdudnaya et al, 2006;Stoelzel et al, 2008). This segmentation was aided and verified by fast Fourier transform (FFT) analysis.…”

“…First, thalamocortical synapses are depressing (Gil et al, 1997) and, in vivo, thalamocortical synapses are in a state of chronic synaptic depression because of the high rates of firing (Swadlow and Gusev, 2001;Castro-Alamancos, 2004;Stoelzel et al, 2008). Lower rates of thalamic firing in the nonalert state yield relief from this depression, which could compensate for changes in thalamocortical firing rates, adding to the stability of baseline rates in spiny cells.…”

“…We focused on the alert to nonalert transition (5 s before and after) to assure that the change was not elicited by uncontrolled sensory or motor events. This state transition is often rapid (Ͻ1 s) and, in thalamocortical neurons, is associated with sharply reduced firing rates and irregular and bursty spike trains (Swadlow and Gusev, 2001;Bezdudnaya et al, 2006;Stoelzel et al, 2008). We studied the effects of this state transition on spontaneous activity of neurons in the primary input layer of visual cortex, layer 4, and a primary output layer, layer 5.…”