The impact of corticothalamic feedback on the output dynamics of a thalamocortical neurone model: the role of synapse location and metabotropic glutamate receptors

Neuroscience. 2003;117(1):229-39. doi: 10.1016/s0306-4522(02)00759-5.

Abstract

The spatio-temporal integration of cortical excitatory postsynaptic potentials was investigated in a multi-compartment model of a thalamocortical neurone. Consistent with experimental data, cortical excitatory postsynaptic potentials contained a metabotropic glutamate receptor-mediated component and were generated by synapses located on distal dendrites. Within this framework, three synaptic distributions (each with equal maximal synaptic conductances) were compared: symmetric, with synapses distributed equally between all dendritic trees, single-dendrite, where synapses were allocated on all distal segments of one dendrite, and single-segment, which comprised one synapse on a single dendritic compartment. We addressed three main issues: (1) the propagation of cortical excitatory postsynaptic potentials to the soma, (2) the interaction of cortical excitatory postsynaptic potentials with proximally generated retinal excitatory postsynaptic potentials, and (3) the effectiveness of cortical excitatory postsynaptic potentials in entraining and perturbing the delta oscillation. The somatic and dendritic amplitudes of the cortical excitatory postsynaptic potentials depended on the distribution of the synapses, being largest and smallest, respectively, for the symmetric distribution, and smallest and largest, respectively, for the single-segment distribution. When a retinal excitatory postsynaptic potential followed a subthreshold cortical excitatory postsynaptic potential with a short (2-200 ms) delay, its ability to evoke action potentials was increased, with single-segment cortical excitatory postsynaptic potentials having the longest-lasting facilitatory effect. When a retinal excitatory postsynaptic potential arrived with a longer delay (210-400 ms), the effect of the cortical excitatory postsynaptic potential was to decrease the number of retinally evoked action potentials. These facilitatory and depressant effects of the cortical excitatory postsynaptic potentials were dependent on the presence of their metabotropic glutamate receptor, and were enhanced by increasing the strength of this glutamate receptor component. Axial resistivity and distal dendritic A-type current had little qualitative effect on these modulatory actions of the cortical excitatory postsynaptic potential. Cortical excitatory postsynaptic potentials were more effective than retinal excitatory postsynaptic potentials in perturbing the phase of the delta oscillation, indicating that they are ideally suited to entraining this form of rhythmic activity. Again, this effect was closely dependent on the presence of metabotropic glutamate receptor but was largely independent of synapse distribution. These results indicate that the distribution of activated synapses and the presence of metabotropic glutamate receptor are crucial factors in determining the effect of cortical feedback excitation on thalamocortical neurons. Moreover, the distinct postsynaptic receptor composition of cortical inputs renders them ideally suited to synchronising low-frequency oscillatory activity in thalamocortical neurons.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cerebral Cortex / physiology*
  • Excitatory Postsynaptic Potentials / physiology
  • Feedback, Physiological / physiology
  • Neural Networks, Computer*
  • Neural Pathways / physiology
  • Neurons / physiology
  • Receptors, Metabotropic Glutamate / physiology*
  • Retina / physiology
  • Synapses / physiology*
  • Thalamus / physiology*

Substances

  • Receptors, Metabotropic Glutamate