Anatomical and physiological considerations in thalamic rhythm generation

The thalamus, known as the pacemaker for spindle rhythms in sleep, has several enabling features that promote such pacemaking. These include a circuitry that interconnects large groups of excitatory and inhibitory neurons, all of which are essentially capable of firing high‐frequency ‘bursts’ of discharges. Bursts in thalamic reticular neurons produce powerful inhibition in thalamic relay neurons, which leads to rebound excitation. The timing properties of the inhibition regulate the network activity by controlling rebound burst latency. Anatomical features within thalamus such as convergence and divergence determine the spread and synchronization of pacemaking activity. The anatomical basis of divergence, i.e. the degree of axonal arborization of elements within the thalamic circuit, can be functionally modified in a dynamic fashion by biochemical pathways that regulate the properties of synaptic release. These data suggest that it will be possible to therapeutically regulate the thalamus to modify not only the propensity to sleep but also forms of epilepsy that rely on similar thalamic circuitry.

[1]  G Oakson,et al.  Thalamic burst patterns in the naturally sleeping cat: a comparison between cortically projecting and reticularis neurones. , 1986, The Journal of physiology.

[2]  D. Prince,et al.  Heterogeneous axonal arborizations of rat thalamic reticular neurons in the ventrobasal nucleus , 1996, The Journal of comparative neurology.

[3]  R. Llinás,et al.  Electrophysiological properties of guinea‐pig thalamic neurones: an in vitro study. , 1984, The Journal of physiology.

[4]  D. McCormick,et al.  Sleep and arousal: thalamocortical mechanisms. , 1997, Annual review of neuroscience.

[5]  A. Scheibel,et al.  The organization of the nucleus reticularis thalami: a Golgi study. , 1966, Brain research.

[6]  D. Prince,et al.  Printed in Great Britain , 2005 .

[7]  P. Gloor,et al.  A study of the transition from spindles to spike and wave discharge in feline generalized penicillin epilepsy: EEG features , 1981, Experimental Neurology.

[8]  P. Golshani,et al.  GABA(B)-receptor-mediated inhibition in developing mouse ventral posterior thalamic nucleus. , 1997, Journal of neurophysiology.

[9]  T. Sejnowski,et al.  Ionic mechanisms underlying synchronized oscillations and propagating waves in a model of ferret thalamic slices. , 1996, Journal of neurophysiology.

[10]  Maria V. Sanchez-Vives,et al.  Inhibitory Interactions between Perigeniculate GABAergic Neurons , 1997, The Journal of Neuroscience.

[11]  D. Prince,et al.  Clonazepam suppresses GABAB-mediated inhibition in thalamic relay neurons through effects in nucleus reticularis. , 1994, Journal of neurophysiology.

[12]  A. Thomson Inhibitory postsynaptic potentials evoked in thalamic neurons by stimulation of the reticularis nucleus evoke slow spikes in isolated rat brain slices—I , 1988, Neuroscience.

[13]  D. Ulrich,et al.  Purinergic inhibition of GABA and glutamate release in the thalamus: Implications for thalamic network activity , 1995, Neuron.

[14]  M. Deschenes,et al.  The thalamus as a neuronal oscillator , 1984, Brain Research Reviews.

[15]  V. Crunelli,et al.  A T‐type Ca2+ current underlies low‐threshold Ca2+ potentials in cells of the cat and rat lateral geniculate nucleus. , 1989, The Journal of physiology.

[16]  J R Huguenard,et al.  GABA(A)-receptor-mediated rebound burst firing and burst shunting in thalamus. , 1997, Journal of neurophysiology.

[17]  J R Huguenard,et al.  Gamma-aminobutyric acid type B receptor-dependent burst-firing in thalamic neurons: a dynamic clamp study. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[18]  J. Bourassa,et al.  Thalamic reticular input to the rat visual thalamus: a single fiber study using biocytin as an anterograde tracer , 1995, Brain Research.

[19]  D. Prince,et al.  GABAA receptor-mediated Cl- currents in rat thalamic reticular and relay neurons. , 1997, Journal of neurophysiology.

[20]  J. Gotman,et al.  A study of the transition from spindles to spike and wave discharge in feline generalized penicillin epilepsy: Microphysiological features , 1981, Experimental Neurology.

[21]  D. McCormick,et al.  What Stops Synchronized Thalamocortical Oscillations? , 1996, Neuron.

[22]  Maria V. Sanchez-Vives,et al.  Functional dynamics of GABAergic inhibition in the thalamus. , 1997, Science.

[23]  M. Rogawski,et al.  T-type calcium channels mediate the transition between tonic and phasic firing in thalamic neurons. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[24]  A. Hernández-Cruz,et al.  Identification of two calcium currents in acutely dissociated neurons from the rat lateral geniculate nucleus. , 1989, Journal of neurophysiology.

[25]  J R Huguenard,et al.  Nucleus-Specific Chloride Homeostasis in Rat Thalamus , 1997, The Journal of Neuroscience.

[26]  D. Prince,et al.  Nucleus reticularis neurons mediate diverse inhibitory effects in thalamus. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[27]  E. G. Jones,et al.  The morphology of physiologically identified GABAergic neurons in the somatic sensory part of the thalamic reticular nucleus in the cat , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[28]  T. Sejnowski,et al.  G protein activation kinetics and spillover of gamma-aminobutyric acid may account for differences between inhibitory responses in the hippocampus and thalamus. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[29]  A. Agmon,et al.  Oscillatory synaptic interactions between ventroposterior and reticular neurons in mouse thalamus in vitro. , 1994, Journal of neurophysiology.

[30]  D. L. Bassett,et al.  ELECTRICAL ACTIVITY OF THE THALAMUS AND BASAL GANGLIA IN DECORTICATE CATS , 1946 .

[31]  D. Prince,et al.  A novel T-type current underlies prolonged Ca(2+)-dependent burst firing in GABAergic neurons of rat thalamic reticular nucleus , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[32]  I. Módy,et al.  Characterization of synaptically elicited GABAB responses using patch‐clamp recordings in rat hippocampal slices. , 1993, The Journal of physiology.

[33]  Mircea Steriade,et al.  Dendrodendritic synapses in the cat reticularis thalami nucleus: a structural basis for thalamic spindle synchronization , 1985, Brain Research.

[34]  J. Rinzel,et al.  Propagation of spindle waves in a thalamic slice model. , 1996, Journal of neurophysiology.

[35]  G Mann,et al.  ON THE THALAMUS * , 1905, British medical journal.

[36]  Maria V. Sanchez-Vives,et al.  Functional Properties of Perigeniculate Inhibition of Dorsal Lateral Geniculate Nucleus Thalamocortical Neurons In Vitro , 1997, The Journal of Neuroscience.

[37]  M. Deschenes,et al.  Electrophysiology of neurons of lateral thalamic nuclei in cat: resting properties and burst discharges. , 1984, Journal of neurophysiology.

[38]  J R Huguenard,et al.  GABAB receptor‐mediated responses in GABAergic projection neurones of rat nucleus reticularis thalami in vitro. , 1996, The Journal of physiology.

[39]  B D Burns,et al.  Some properties of the cat's isolated cerebral cortex , 1950, The Journal of physiology.

[40]  T. Sejnowski,et al.  Control of Spatiotemporal Coherence of a Thalamic Oscillation by Corticothalamic Feedback , 1996, Science.

[41]  M. Scanziani,et al.  Presynaptic inhibition in the hippocampus , 1993, Trends in Neurosciences.

[42]  D. Prince,et al.  Intrathalamic rhythmicity studied in vitro: nominal T-current modulation causes robust antioscillatory effects , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[43]  D. Prince,et al.  Peptidergic Modulation of Intrathalamic Circuit Activity In Vitro: Actions of Cholecystokinin , 1997, The Journal of Neuroscience.

[44]  D. McCormick,et al.  Cellular mechanisms of a synchronized oscillation in the thalamus. , 1993, Science.