Novel and Distinct Operational Principles of Intralaminar Thalamic Neurons and Their Striatal Projections

Neurons of the intralaminar thalamus, including central lateral (CL) and parafascicular (Pf) nuclei, innervate the cortex and striatum and are important for cognitive, sensory, and motor processes. We tested the hypothesis that CL and Pf neurons provide functionally distinct inputs to the striatum. We performed recordings of single CL and Pf neurons in anesthetized rats and, after juxtacellularly labeling the neurons, their somatodendritic features and synaptic connections were characterized. All CL neurons (n = 31) discharged classic low-threshold Ca2+ spike bursts during cortical slow-wave activity in vivo. In contrast, Pf neurons (n = 52) rarely fired such bursts, but instead discharged groups of spikes at relatively low frequencies. The activity of CL and Pf neurons was often temporally coupled to cortical slow oscillations. Identified CL neurons possessed archetypal “bushy” dendrites and preferentially established synapses with dendritic spines (91% of synapses) of striatal projection neurons. Pf neurons possessed “reticular-like” dendrites, and, on average, preferentially established synapses with dendritic shafts (63%) in striatum, although connectivity was markedly heterogeneous across neurons. Two of the six Pf neurons studied exclusively targeted dendritic shafts, whereas another neuron almost exclusively (97%) targeted spines. The remaining three neurons preferentially targeted dendritic shafts (53–70%). Thus, the fundamental properties of CL and Pf neurons differ (the latter do not express the typical operational principles of thalamic relay neurons), and they provide different temporally patterned inputs to distinct striatal targets. This mechanistic diversity likely underpins the transmission of specific and discrete information from intralaminar thalamic nuclei to striatal and cortical targets.

[1]  A. Morel,et al.  Low-threshold calcium spike bursts in the human thalamus. Common physiopathology for sensory, motor and limbic positive symptoms. , 1996, Brain : a journal of neurology.

[2]  R. Llinás,et al.  Bursting of thalamic neurons and states of vigilance. , 2006, Journal of neurophysiology.

[3]  R. Llinás,et al.  The neuronal basis for consciousness. , 1998, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[4]  Y. Smith,et al.  Microcircuitry of the direct and indirect pathways of the basal ganglia. , 1998, Neuroscience.

[5]  S. Sherman Tonic and burst firing: dual modes of thalamocortical relay , 2001, Trends in Neurosciences.

[6]  M. Kimura,et al.  Monitoring and switching of cortico-basal ganglia loop functions by the thalamo-striatal system , 2004, Neuroscience Research.

[7]  M. Deschenes,et al.  A Single‐cell Study of the Axonal Projections Arising from the Posterior Intralaminar Thalamic Nuclei in the Rat , 1996, The European journal of neuroscience.

[8]  S. Sherman,et al.  Effects of membrane voltage on receptive field properties of lateral geniculate neurons in the cat: contributions of the low-threshold Ca2+ conductance. , 1992, Journal of neurophysiology.

[9]  J. Lisman Bursts as a unit of neural information: making unreliable synapses reliable , 1997, Trends in Neurosciences.

[10]  A. Destexhe,et al.  Dendritic Low-Threshold Calcium Currents in Thalamic Relay Cells , 1998, The Journal of Neuroscience.

[11]  R.,et al.  Low-Threshold Calcium Currents in Central Nervous System Neurons , 2003 .

[12]  Brendon O. Watson,et al.  Internal Dynamics Determine the Cortical Response to Thalamic Stimulation , 2005, Neuron.

[13]  G. Stuart,et al.  Action Potential Backpropagation and Somato-dendritic Distribution of Ion Channels in Thalamocortical Neurons , 2000, The Journal of Neuroscience.

[14]  M. Steriade Corticothalamic resonance, states of vigilance and mentation , 2000, Neuroscience.

[15]  P. Barthó,et al.  Selective GABAergic innervation of thalamic nuclei from zona incerta , 2002, The European journal of neuroscience.

[16]  A M Amjad,et al.  A framework for the analysis of mixed time series/point process data--theory and application to the study of physiological tremor, single motor unit discharges and electromyograms. , 1995, Progress in biophysics and molecular biology.

[17]  A. D. Smith,et al.  Identification of synaptic terminals of thalamic or cortical origin in contact with distinct medium‐size spiny neurons in the rat neostriatum , 1988, The Journal of comparative neurology.

[18]  A. Parent,et al.  Single‐axon tracing and three‐dimensional reconstruction of centre médian‐parafascicular thalamic neurons in primates , 2005, The Journal of comparative neurology.

[19]  P. Emson,et al.  Restoration of thalamostriatal projections in rat neostriatal grafts: An electron microscopic analysis , 1991, The Journal of comparative neurology.

[20]  Richard T. Marrocco,et al.  Arousal systems , 1994, Current Opinion in Neurobiology.

[21]  N. Ichinohe,et al.  Intrastriatal targets of projection fibers from the central lateral nucleus of the rat thalamus , 2001, Neuroscience Letters.

[22]  A. Morel,et al.  Single-unit analysis of the pallidum, thalamus and subthalamic nucleus in parkinsonian patients , 2000, Neuroscience.

[23]  G. Paxinos,et al.  The Rat Brain in Stereotaxic Coordinates , 1983 .

[24]  A. Scheibel,et al.  Structural organization of nonspecific thalamic nuclei and their projection toward cortex. , 1967, Brain research.

[25]  D. Contreras,et al.  Cellular basis of EEG slow rhythms: a study of dynamic corticothalamic relationships , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[26]  J. Vitek,et al.  Burst and oscillation as disparate neuronal properties , 1996, Journal of Neuroscience Methods.

[27]  M. Steriade,et al.  A novel slow (< 1 Hz) oscillation of neocortical neurons in vivo: depolarizing and hyperpolarizing components , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[28]  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.

[29]  E. Garcia-Rill,et al.  Postnatal maturational properties of rat parafascicular thalamic neurons recorded in vitro. , 2005, Thalamus & related systems.

[30]  Edward L. Bartlett,et al.  Unique combination of anatomy and physiology in cells of the rat paralaminar thalamic nuclei adjacent to the medial geniculate body , 2006, The Journal of comparative neurology.

[31]  D. Pinault,et al.  A novel single-cell staining procedure performed in vivo under electrophysiological control: morpho-functional features of juxtacellularly labeled thalamic cells and other central neurons with biocytin or Neurobiotin , 1996, Journal of Neuroscience Methods.

[32]  K. Svoboda,et al.  Structure and function of dendritic spines. , 2002, Annual review of physiology.

[33]  Y. Smith,et al.  The thalamostriatal system: a highly specific network of the basal ganglia circuitry , 2004, Trends in Neurosciences.

[34]  J. Bolam,et al.  Input from the frontal cortex and the parafascicular nucleus to cholinergic interneurons in the dorsal striatum of the rat , 1992, Neuroscience.

[35]  T. Stanford,et al.  Subcortical loops through the basal ganglia , 2005, Trends in Neurosciences.

[36]  D. Pinault,et al.  The thalamic reticular nucleus does not send commissural projection to the contralateral parafascicular nucleus in the rat , 1995, Brain Research.

[37]  L. Swanson The Rat Brain in Stereotaxic Coordinates, George Paxinos, Charles Watson (Eds.). Academic Press, San Diego, CA (1982), vii + 153, $35.00, ISBN: 0 125 47620 5 , 1984 .

[38]  T. Sejnowski,et al.  LETTERS TO NATURE , 1996 .

[39]  G. Govindaiah,et al.  Modulation of thalamic neuron excitability by orexins , 2006, Neuropharmacology.

[40]  M. Witter,et al.  The intralaminar and midline nuclei of the thalamus. Anatomical and functional evidence for participation in processes of arousal and awareness , 2002, Brain Research Reviews.

[41]  A. Parent,et al.  Efferent connections of the centromedian and parafascicular thalamic nuclei in the squirrel monkey: A light and electron microscopic study of the thalamostriatal projection in relation to striatal heterogeneity , 1992, The Journal of comparative neurology.

[42]  M. Steriade Grouping of brain rhythms in corticothalamic systems , 2006, Neuroscience.

[43]  D. Contreras,et al.  The slow (< 1 Hz) oscillation in reticular thalamic and thalamocortical neurons: scenario of sleep rhythm generation in interacting thalamic and neocortical networks , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[44]  M. Deschenes,et al.  Striatal and cortical projections of single neurons from the central lateral thalamic nucleus in the rat , 1996, Neuroscience.

[45]  Erika E. Fanselow,et al.  Thalamic bursting in rats during different awake behavioral states , 2001, Proceedings of the National Academy of Sciences of the United States of America.

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

[47]  J. Bolam,et al.  Relationship of Activity in the Subthalamic Nucleus–Globus Pallidus Network to Cortical Electroencephalogram , 2000, The Journal of Neuroscience.

[48]  H. Swadlow,et al.  The impact of 'bursting' thalamic impulses at a neocortical synapse , 2001, Nature Neuroscience.

[49]  H. Groenewegen,et al.  The specificity of the ‘nonspecific’ midline and intralaminar thalamic nuclei , 1994, Trends in Neurosciences.

[50]  Don H. Johnson,et al.  Point process models of single-neuron discharges , 1996, Journal of Computational Neuroscience.

[51]  Charles J. Wilson,et al.  Spontaneous subthreshold membrane potential fluctuations and action potential variability of rat corticostriatal and striatal neurons in vivo. , 1997, Journal of neurophysiology.

[52]  K. Uemura,et al.  Identification of nociceptive neurons in the medial thalamus: morphological studies of nociceptive neurons with intracellular injection of horseradish peroxidase , 1992, Brain Research.

[53]  J. Mitrofanis,et al.  Organisation of the reticular thalamic projection to the intralaminar and midline nuclei in rats , 1997, The Journal of comparative neurology.