The Journal of Neurophysiology Vol. 80 No. 6 December 1998, pp. 3261-3271
Copyright ©1998 The American Physiological Society

Contribution of Supragranular Layers to Sensory Processing and Plasticity in Adult Rat Barrel Cortex

Wei Huang¹, Michael Armstrong-James², V. Rema¹, Mathew E. Diamond³, and Ford F. Ebner¹

¹ Department of Psychology, Vanderbilt University, 37240; and Institute for Developmental Neuroscience, Vanderbilt University, Nashville, Tennessee 37203; ² Department of Physiology, Queen Mary & Westfield College, London University, London E1 4NS, United Kingdom; and ³ Cognitive Neuroscience Sector, International School for Advanced Studies, 34014 Trieste; and University of Udine, Department of Biomedical Sciences and Technologies, 33100 Udine, Italy

Huang, Wei, Michael Armstrong-James, V. Rema, Mathew E. Diamond, and Ford F. Ebner. Contribution of supragranular layers to sensory processing and plasticity in adult rat barrel cortex. J. Neurophysiol. 80: 3261-3271, 1998. In mature rat primary somatic sensory cortical area (SI) barrel field cortex, the thalamic-recipient granular layer IV neurons project especially densely to layers I, II, III, and IV. A prior study showed that cells in the supragranular layers are the fastest to change their response properties to novel changes in sensory inputs. Here we examine the effect of removing supragranular circuitry on the responsiveness and synaptic plasticity of cells in the remaining layers. To remove the layer II + III (supragranular) neurons from the circuitry of barrel field cortex, N-methyl-D-aspartate (NMDA) was applied to the exposed dura over the barrel cortex, which destroys those neurons by excitotoxicity without detectable damage to blood vessels or axons of passage. Fifteen days after NMDA treatment, the first responsive cells encountered were 400-430 µm below the pial surface. In separate cases triphenyltetrazolium chloride (TTC), a vital dye taken up by living cells, was absent from the lesion area. Cytochrome oxidase (CO) activity was absent in the first few tangential sections through the barrel field in all cases before arriving at the CO-dense barrel domains. These findings indicate that the lesions were quite consistent from animal to animal. Controls consisted of applying vehicle without NMDA under similar conditions. Responses of D2 barrel cells were assessed for spontaneous activity and level of response to stimulation of the principal D2 whisker and four surround whiskers D1, D3, C2, and E2. In two additional groups of animals treated in the same way, sensory plasticity was assessed by trimming all whiskers except D2 and either D1 or D3 (called Dpaired) for 7 days before recording cortical responses. Such whisker pairing normally potentiates D2 barrel cell responses to stimulation of the two intact whiskers (D2 + Dpaired). After NMDA lesions, cortical cells still responded to all whiskers tested. Cells in lesioned cortex showed reduced response amplitude compared with sham-operated controls to all D-row whiskers. In-arc surround whisker (C2 or E2) responses were normal. Spontaneous activity did not change significantly in any remaining layer at the time tested. Modal latencies to stimulation of principal D2 or surround D1 or D3 whiskers showed no significant change after lesioning. These findings indicate that there is a reasonable preservation of the response properties of layer IV, V, VI neurons after removal of layer II-III neurons in this way. Whisker pairing plasticity in layer IV-VI D2 barrel column neurons occurred in both lesioned and sham animals but was reduced significantly in lesioned animals compared with controls. The response bias generated by whisker trimming (Dpaired/Dcut + Dpaired ratio) was less pronounced in NMDA-lesioned than sham-lesioned animals. Proportionately fewer neurons in layer IV (52 vs. 64%) and in the infragranular layers (55 vs. 68%) exhibited a clear response bias to paired whiskers. We conclude that receptive-field plasticity can occur in layers IV-VI of barrel cortex in the absence of the supragranular layer circuitry. However, layer I-III circuitry does play a role in normal receptive-field generation and is required for the full expression of whisker pairing plasticity in granular and infragranular layer cells.

This article has been cited by other articles:

				A. Frick, D. Feldmeyer, M. Helmstaedter, and B. Sakmann Monosynaptic Connections between Pairs of L5A Pyramidal Neurons in Columns of Juvenile Rat Somatosensory Cortex Cereb Cortex, February 1, 2008; 18(2): 397 - 406. [Abstract] [Full Text] [PDF]

				A. Frick, D. Feldmeyer, and B. Sakmann Postnatal development of synaptic transmission in local networks of L5A pyramidal neurons in rat somatosensory cortex J. Physiol., November 15, 2007; 585(1): 103 - 116. [Abstract] [Full Text] [PDF]

				V. Jacob, D. J. Brasier, I. Erchova, D. Feldman, and D. E. Shulz Spike Timing-Dependent Synaptic Depression in the In Vivo Barrel Cortex of the Rat J. Neurosci., February 7, 2007; 27(6): 1271 - 1284. [Abstract] [Full Text] [PDF]

				A. Wolters, A. Schmidt, A. Schramm, D. Zeller, M. Naumann, E. Kunesch, R. Benecke, K. Reiners, and J. Classen Timing-dependent plasticity in human primary somatosensory cortex J. Physiol., June 15, 2005; 565(3): 1039 - 1052. [Abstract] [Full Text] [PDF]

				D. Feldmeyer, A. Roth, and B. Sakmann Monosynaptic Connections between Pairs of Spiny Stellate Cells in Layer 4 and Pyramidal Cells in Layer 5A Indicate That Lemniscal and Paralemniscal Afferent Pathways Converge in the Infragranular Somatosensory Cortex J. Neurosci., March 30, 2005; 25(13): 3423 - 3431. [Abstract] [Full Text] [PDF]

				C. P. Pluto, R. D. Lane, and R. W. Rhoades Local GABA Receptor Blockade Reveals Hindlimb Responses in the SI Forelimb-Stump Representation of Neonatally Amputated Rats J Neurophysiol, July 1, 2004; 92(1): 372 - 379. [Abstract] [Full Text] [PDF]

				I. D. Manns, B. Sakmann, and M. Brecht Sub- and suprathreshold receptive field properties of pyramidal neurones in layers 5A and 5B of rat somatosensory barrel cortex J. Physiol., April 15, 2004; 556(2): 601 - 622. [Abstract] [Full Text] [PDF]

				V. Rema and F. F. Ebner Lesions of Mature Barrel Field Cortex Interfere with Sensory Processing and Plasticity in Connected Areas of the Contralateral Hemisphere J. Neurosci., November 12, 2003; 23(32): 10378 - 10387. [Abstract] [Full Text] [PDF]

				C. P. Pluto, R. D. Lane, N. L. Chiaia, A. S. Stojic, and R. W. Rhoades Role of Development in Reorganization of the SI Forelimb-Stump Representation in Fetally, Neonatally, and Adult Amputated Rats J Neurophysiol, September 1, 2003; 90(3): 1842 - 1851. [Abstract] [Full Text] [PDF]

				V. Rema, M. Armstrong-James, and F. F. Ebner Experience-Dependent Plasticity Is Impaired in Adult Rat Barrel Cortex after Whiskers Are Unused in Early Postnatal Life J. Neurosci., January 1, 2003; 23(1): 358 - 366. [Abstract] [Full Text] [PDF]

				C. R L Simkus and C. Stricker Properties of mEPSCs recorded in layer II neurones of rat barrel cortex J. Physiol., December 1, 2002; 545(2): 509 - 520. [Abstract] [Full Text] [PDF]

				M. Brecht and B. Sakmann -Dynamic representation of whisker deflection by synaptic potentials in spiny stellate and pyramidal cells in the barrels and septa of layer 4 rat somatosensory cortex J. Physiol., August 15, 2002; 543(1): 49 - 70. [Abstract] [Full Text] [PDF]

				N. Laaris and A. Keller Functional Independence of Layer IV Barrels J Neurophysiol, February 1, 2002; 87(2): 1028 - 1034. [Abstract] [Full Text] [PDF]

				E. Ahissar, R. Sosnik, K. Bagdasarian, and S. Haidarliu Temporal Frequency of Whisker Movement. II. Laminar Organization of Cortical Representations J Neurophysiol, July 1, 2001; 86(1): 354 - 367. [Abstract] [Full Text] [PDF]

				J. A. Harris, R. S. Petersen, and M. E. Diamond Distribution of tactile learning and its neural basis PNAS, June 22, 1999; 96(13): 7587 - 7591. [Abstract] [Full Text] [PDF]