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The Journal of Neuroscience, May 7, 2008, 28(19):5018-5028; doi:10.1523/JNEUROSCI.4726-07.2008

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

Carl R. Stoelzel, Yulia Bereshpolova, Alexander G. Gusev, and Harvey A. Swadlow

Department of Psychology, University of Connecticut, Storrs, Connecticut 06269

Correspondence should be addressed to Dr. Harvey A. Swadlow, Department of Psychology, University of Connecticut, 406 Babbidge Road, Box U-1020, Storrs, CT 06269. Email: Harvey.Swadlow{at}Uconn.edu

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 0.3 ms earlier and 100–200 µm 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 >750 ms. We interpret this to reflect interval-dependent recovery from chronic depression at the thalamocortical synapse, caused by significant spontaneous firing of LGNd cells (8 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.

Key words: thalamocortical; synaptic dynamics; synaptic depression; dorsal lateral geniculate nucleus (LGNd); striate cortex; synaptic plasticity; thalamus; visual

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Received Oct. 18, 2007; revised March 19, 2008; accepted March 24, 2008.

Correspondence should be addressed to Dr. Harvey A. Swadlow, Department of Psychology, University of Connecticut, 406 Babbidge Road, Box U-1020, Storrs, CT 06269. Email: Harvey.Swadlow{at}Uconn.edu

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