Received September 17, 2001
Accepted after revision December 8, 2001

Different temporal processing of sensory inputs in the rat whisker thalamus during quiescent and information processing states in vivo

¹ Montreal Neurological Institute, 3801 University St, Room WB210, Montreal, Quebec H3A 2B4, Canada

^* To whom correspondence should be addressed.

Sensory inputs from the whiskers reach the primary somatosensory thalamus through the medial lemniscus tract. The main role of the thalamus is to relay these sensory inputs to the neocortex according to the regulations dictated by behavioural state. Intracellular recordings in urethane-anaesthetized rats show that whisker stimulation evokes EPSP-IPSP sequences in thalamic neurons. Both EPSPs and IPSPs depress with repetitive whisker stimulation at frequencies above 2 Hz. Single-unit recordings reveal that during quiescent states thalamic responses to repetitive whisker stimulation are suppressed at frequencies above 2 Hz, so that only low-frequency sensory stimulation is relayed to the neocortex. In contrast, during activated states, induced by stimulation of the brainstem reticular formation or application of acetylcholine in the thalamus, high-frequency whisker stimulation at up to 40 Hz is relayed to the neocortex. Sensory suppression is caused by the depression of lemniscal EPSPs in relatively hyperpolarized thalamocortical neurons. Sensory suppression is abolished during activated states because thalamocortical neurons depolarize and the depressed lemniscal EPSPs are able to reach firing threshold. Strong IPSPs may also contribute to sensory suppression by hyperpolarizing thalamocortical neurons, but during activated states IPSPs are strongly reduced altogether. The results indicate that the synaptic depression of lemniscal EPSPs and the level of depolarization of thalamocortical neurons work together in thalamic primary sensory pathways to suppress high-frequency sensory inputs during non-activated (quiescent) states while permitting the faithful relay of high-frequency sensory information during activated (processing) states.

This article has been cited by other articles:

				J. D. Cohen and M. A. Castro-Alamancos Early Sensory Pathways for Detection of Fearful Conditioned Stimuli: Tectal and Thalamic Relays J. Neurosci., July 18, 2007; 27(29): 7762 - 7776. [Abstract] [Full Text] [PDF]

				M. J. Higley and D. Contreras Frequency Adaptation Modulates Spatial Integration of Sensory Responses in the Rat Whisker System J Neurophysiol, May 1, 2007; 97(5): 3819 - 3824. [Abstract] [Full Text] [PDF]

				P. Rigas and M. A. Castro-Alamancos Thalamocortical Up States: Differential Effects of Intrinsic and Extrinsic Cortical Inputs on Persistent Activity J. Neurosci., April 18, 2007; 27(16): 4261 - 4272. [Abstract] [Full Text] [PDF]

				M. J. Higley and D. Contreras Cellular Mechanisms of Suppressive Interactions Between Somatosensory Responses In Vivo J Neurophysiol, January 1, 2007; 97(1): 647 - 658. [Abstract] [Full Text] [PDF]

				R. Reig, R. Gallego, L. G. Nowak, and M. V. Sanchez-Vives Impact of Cortical Network Activity on Short-term Synaptic Depression Cereb Cortex, May 1, 2006; 16(5): 688 - 695. [Abstract] [Full Text] [PDF]

				A. Hirata, J. Aguilar, and M. A. Castro-Alamancos Noradrenergic activation amplifies bottom-up and top-down signal-to-noise ratios in sensory thalamus. J. Neurosci., April 19, 2006; 26(16): 4426 - 4436. [Abstract] [Full Text] [PDF]

				A. Hirata and M. A. Castro-Alamancos Relief of Synaptic Depression Produces Long-Term Enhancement in Thalamocortical Networks J Neurophysiol, April 1, 2006; 95(4): 2479 - 2491. [Abstract] [Full Text] [PDF]

				D. Golomb, E. Ahissar, and D. Kleinfeld Coding of Stimulus Frequency by Latency in Thalamic Networks Through the Interplay of GABAB-Mediated Feedback and Stimulus Shape J Neurophysiol, March 1, 2006; 95(3): 1735 - 1750. [Abstract] [Full Text] [PDF]

				J. R. Aguilar and M. A. Castro-Alamancos Spatiotemporal Gating of Sensory Inputs in Thalamus during Quiescent and Activated States J. Neurosci., November 23, 2005; 25(47): 10990 - 11002. [Abstract] [Full Text] [PDF]

				C. E. Boudreau and D. Ferster Short-Term Depression in Thalamocortical Synapses of Cat Primary Visual Cortex J. Neurosci., August 3, 2005; 25(31): 7179 - 7190. [Abstract] [Full Text] [PDF]

				L. A. Grande and W. J. Spain Synaptic Depression as a Timing Device Physiology, June 1, 2005; 20(3): 201 - 210. [Abstract] [Full Text] [PDF]

				J. D. Cohen and M. A. Castro-Alamancos Skilled Motor Learning Does Not Enhance Long-Term Depression in the Motor Cortex In Vivo J Neurophysiol, March 1, 2005; 93(3): 1486 - 1497. [Abstract] [Full Text] [PDF]

				C. I. Moore Frequency-Dependent Processing in the Vibrissa Sensory System J Neurophysiol, June 1, 2004; 91(6): 2390 - 2399. [Abstract] [Full Text] [PDF]

				R. M. Webber and G. B. Stanley Nonlinear Encoding of Tactile Patterns in the Barrel Cortex J Neurophysiol, May 1, 2004; 91(5): 2010 - 2022. [Abstract] [Full Text] [PDF]

				J. A. Cardin and M. F. Schmidt Auditory Responses in Multiple Sensorimotor Song System Nuclei Are Co-Modulated by Behavioral State J Neurophysiol, May 1, 2004; 91(5): 2148 - 2163. [Abstract] [Full Text] [PDF]

				D. M. Mooney, L. Zhang, C. Basile, V. V. Senatorov, J. Ngsee, A. Omar, and B. Hu Distinct forms of cholinergic modulation in parallel thalamic sensory pathways PNAS, January 6, 2004; 101(1): 320 - 324. [Abstract] [Full Text] [PDF]

				J. A. Hartings, S. Temereanca, and D. J. Simons Processing of Periodic Whisker Deflections By Neurons in the Ventroposterior Medial and Thalamic Reticular Nuclei J Neurophysiol, November 1, 2003; 90(5): 3087 - 3094. [Abstract] [Full Text] [PDF]

				J. A. Cardin and M. F. Schmidt Song System Auditory Responses Are Stable and Highly Tuned During Sedation, Rapidly Modulated and Unselective During Wakefulness, and Suppressed By Arousal J Neurophysiol, November 1, 2003; 90(5): 2884 - 2899. [Abstract] [Full Text] [PDF]

				R. W. Berg and D. Kleinfeld Vibrissa Movement Elicited by Rhythmic Electrical Microstimulation to Motor Cortex in the Aroused Rat Mimics Exploratory Whisking J Neurophysiol, November 1, 2003; 90(5): 2950 - 2963. [Abstract] [Full Text] [PDF]

				C. E. Garabedian, S. R. Jones, M. M. Merzenich, A. Dale, and C. I. Moore Band-Pass Response Properties of Rat SI Neurons J Neurophysiol, September 1, 2003; 90(3): 1379 - 1391. [Abstract] [Full Text] [PDF]

				B. S. Minnery, R. M. Bruno, and D. J. Simons Response Transformation and Receptive-Field Synthesis in the Lemniscal Trigeminothalamic Circuit J Neurophysiol, September 1, 2003; 90(3): 1556 - 1570. [Abstract] [Full Text] [PDF]

				M. Deschenes, E. Timofeeva, and P. Lavallee The Relay of High-Frequency Sensory Signals in the Whisker-to-Barreloid Pathway J. Neurosci., July 30, 2003; 23(17): 6778 - 6787. [Abstract] [Full Text] [PDF]

				M. J. Hartmann, N. J. Johnson, R. B. Towal, and C. Assad Mechanical Characteristics of Rat Vibrissae: Resonant Frequencies and Damping in Isolated Whiskers and in the Awake Behaving Animal J. Neurosci., July 23, 2003; 23(16): 6510 - 6519. [Abstract] [Full Text] [PDF]

				S. Temereanca and D. J. Simons Local Field Potentials and the Encoding of Whisker Deflections by Population Firing Synchrony in Thalamic Barreloids J Neurophysiol, April 1, 2003; 89(4): 2137 - 2145. [Abstract] [Full Text] [PDF]

				M. A. Castro-Alamancos Role of Thalamocortical Sensory Suppression during Arousal: Focusing Sensory Inputs in Neocortex J. Neurosci., November 15, 2002; 22(22): 9651 - 9655. [Abstract] [Full Text] [PDF]