A New Thalamic Pathway of Vibrissal Information Modulated by the Motor Cortex

Three ascending pathways of information processing have been identified so far in the vibrissal system of rodents. In the ventral posterior medial nucleus of the thalamus, two of these pathways convey information through the core and tail of barrel-associated structures, called barreloids. The other pathway transits through the posterior group nucleus. The present study provides anatomical and electrophysiological evidence for the existence of an additional pathway that passes through the head of the barreloids. This pathway arises from multiwhisker-responsive cells in the principal trigeminal nucleus and differs from the classic lemniscal pathway, in that constituent thalamic cells have multiwhisker receptive field and receive corticothalamic input from lamina 6 of the vibrissa motor cortex. It is suggested that this pathway might be involved in relaying signals encoding phase of whisker motion during free whisking.

[1]  Martin Deschênes,et al.  Feedforward Inhibitory Control of Sensory Information in Higher-Order Thalamic Nuclei , 2005, The Journal of Neuroscience.

[2]  M. Deschenes,et al.  Parallel Streams for the Relay of Vibrissal Information through Thalamic Barreloids , 2000, The Journal of Neuroscience.

[3]  Martin Deschênes,et al.  Electrophysiology and Pharmacology of the Corticothalamic Input to Lateral Thalamic Nuclei: an Intracellular Study in the Cat , 1990, The European journal of neuroscience.

[4]  KF Jensen,et al.  Terminal arbors of axons projecting to the somatosensory cortex of the adult rat. I. The normal morphology of specific thalamocortical afferents , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[5]  E Ahissar,et al.  Size gradients of barreloids in the rat thalamus , 2001, The Journal of comparative neurology.

[6]  M. Deschenes,et al.  The Relay of High-Frequency Sensory Signals in the Whisker-to-Barreloid Pathway , 2003, The Journal of Neuroscience.

[7]  M. Sugitani,et al.  Somatotopic organization and columnar structure of vibrissae representation in the rat ventrobasal complex , 2004, Experimental Brain Research.

[8]  M. Deschenes,et al.  Substrate for Cross-Talk Inhibition between Thalamic Barreloids , 2002, The Journal of Neuroscience.

[9]  M. Deschenes,et al.  Corticothalamic Projections from the Cortical Barrel Field to the Somatosensory Thalamus in Rats: A Single‐fibre Study Using Biocytin as an Anterograde Tracer , 1995, The European journal of neuroscience.

[10]  Leonard K. Kaczmarek,et al.  Protein Kinase Modulation of a Neuronal Cation Channel Requires Protein–Protein Interactions Mediated by an Src homology 3 Domain , 2002, The Journal of Neuroscience.

[11]  Daniel J Simons,et al.  Response properties of whisker-associated trigeminothalamic neurons in rat nucleus principalis. , 2003, Journal of neurophysiology.

[12]  F. Ebner,et al.  Somatic sensory responses in the rostral sector of the posterior group (POm) and in the ventral posterior medial nucleus (VPM) of the rat thalamus: Dependence on the barrel field cortex , 1992, The Journal of comparative neurology.

[13]  Haruhide Hayashi,et al.  Distributions of vibrissae afferent fiber collaterals in the trigeminal nuclei as revealed by intra-axonal injection of horseradish peroxidase , 1980, Brain Research.

[14]  M. Deschenes,et al.  Single- and Multi-Whisker Channels in the Ascending Projections from the Principal Trigeminal Nucleus in the Rat , 1999, The Journal of Neuroscience.

[15]  David Kleinfeld,et al.  Seeing What the Mouse Sees with Its Vibrissae: A Matter of Behavioral State , 2006, Neuron.

[16]  E. Ahissar,et al.  Parallel Thalamic Pathways for Whisking and Touch Signals in the Rat , 2006, PLoS biology.

[17]  Asaf Keller,et al.  Reducing the Uncertainty: Gating of Peripheral Inputs by Zona Incerta , 2004, The Journal of Neuroscience.

[18]  Riitta Hari,et al.  Neuromagnetic Responses to Frequency-Tagged Sounds: A New Method to Follow Inputs from Each Ear to the Human Auditory Cortex during Binaural Hearing , 2002, The Journal of Neuroscience.

[19]  C. Petersen,et al.  Correlating whisker behavior with membrane potential in barrel cortex of awake mice , 2006, Nature Neuroscience.

[20]  M. Castro-Alamancos,et al.  Spatiotemporal Gating of Sensory Inputs in Thalamus during Quiescent and Activated States , 2005, The Journal of Neuroscience.

[21]  R. S. Waters,et al.  Thalamocortical arbors extend beyond single cortical barrels: an in vivo intracellular tracing study in rat , 2000, Experimental Brain Research.

[22]  S. Buffer,et al.  Barreloids in adult rat thalamus: Three‐dimensional architecture and relationship to somatosensory cortical barrels , 1995, The Journal of comparative neurology.

[23]  D. McCormick,et al.  Corticothalamic activation modulates thalamic firing through glutamate "metabotropic" receptors. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[24]  H. Killackey,et al.  Receptive-field properties of rat ventral posterior medial neurons before and after selective kainic acid lesions of the trigeminal brain stem complex. , 1987, Journal of neurophysiology.

[25]  M. Ito,et al.  Response properties and topography of vibrissa-sensitive VPM neurons in the rat. , 1988, Journal of neurophysiology.

[26]  D Kleinfeld,et al.  Central versus peripheral determinants of patterned spike activity in rat vibrissa cortex during whisking. , 1997, Journal of neurophysiology.

[27]  M. Deschenes,et al.  Dendroarchitecture of Relay Cells in Thalamic Barreloids: A Substrate for Cross-Whisker Modulation , 2002, The Journal of Neuroscience.

[28]  M. Castro-Alamancos,et al.  Properties of primary sensory (lemniscal) synapses in the ventrobasal thalamus and the relay of high-frequency sensory inputs. , 2002, Journal of neurophysiology.

[29]  M. Calcagnotto,et al.  Presynaptic Long-Term Potentiation in Corticothalamic Synapses , 1999, The Journal of Neuroscience.

[30]  M. Deschenes,et al.  Dendroarchitecture and Lateral Inhibition in Thalamic Barreloids , 2004, The Journal of Neuroscience.

[31]  F. Ebner,et al.  Modulation of receptive field properties of thalamic somatosensory neurons by the depth of anesthesia. , 1999, Journal of neurophysiology.

[32]  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.

[33]  Martin Deschênes,et al.  The organization of corticothalamic projections: reciprocity versus parity , 1998, Brain Research Reviews.

[34]  Rune W. Berg,et al.  Coherent electrical activity between vibrissa sensory areas of cerebellum and neocortex is enhanced during free whisking. , 2002, Journal of neurophysiology.

[35]  M. Deschenes,et al.  Thalamic projections from the whisker‐sensitive regions of the spinal trigeminal complex in the rat , 2000, The Journal of comparative neurology.

[36]  M F Jacquin,et al.  Differential Foci and Synaptic Organization of the Principal and Spinal Trigeminal Projections to the Thalamus in the Rat , 1994, The European journal of neuroscience.

[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 .