Somatosensory response properties of excitatory and inhibitory neurons in rat motor cortex

Journal of Neurophysiology

Volumn 106, Issue 3, 2011, Pages 1355-1362

  Murray, Peter D ^a   Keller, Asaf ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

Fast spiking; Feedforward inhibition; Network; Receptive field; Regularspiking

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; FEMALE; MOTONEURON; MOTOR CORTEX; NERVE CELL EXCITABILITY; NERVE CELL INHIBITION; NONHUMAN; PRIORITY JOURNAL; RAT; RECEPTIVE FIELD; SENSORY STIMULATION; SOMATOSENSORY SYSTEM; TACTILE STIMULATION;

ANIMALS; EVOKED POTENTIALS, SOMATOSENSORY; FEMALE; MOTOR CORTEX; NEURAL INHIBITION; RATS; RATS, SPRAGUE-DAWLEY; SENSORY RECEPTOR CELLS; SOMATOSENSORY CORTEX;

EID: 80052572944     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.01089.2010     Document Type: Article

References (61)

1. Aflalo TN, Graziano MS. Possible origins of the complex topographic organization of motor cortex: reduction of a multidimensional space onto a two-dimensional array. J Neurosci 26: 6288-6297, 2006.
2. Agmon A, Connors BW. Correlation between intrinsic firing patterns and thalamocortical synaptic responses of neurons in mouse barrel cortex. J Neurosci 12: 319-329, 1992.
3. Aizawa H, Tanji J. Corticocortical and thalamocortical responses of neurons in the monkey primary motor cortex and their relation to a trained motor task. J Neurophysiol 71: 550-560, 1994.
4. Armstrong-James M, Welker E, Callahan CA. The contribution of NMDA and non-NMDA receptors to fast and slow transmission of sensory information in the rat Sl barrel cortex. J Neurosci 13: 2149-2160, 1993.
5. Atencio CA, Schreiner CE. Spectrotemporal processing differences between auditory cortical fast-spiking and regular-spiking neurons. J Neurosci 28: 3897-3910, 2008.
6. Beierlein M, Gibson JR, Connors BW. A network of electrically coupled interneurons drives synchronized inhibition in neocortex. Nat Neurosci 3: 904-910, 2000.
7. Beierlein M, Gibson JR, Connors BW. Two dynamically distinct inhibitory networks in layer 4 of the neocortex. J Neurophysiol 90: 2987-3000, 2003.
8. Benevento LA, Creutzfeldt OD, Kuhnt U. Significance of intracortical inhibition in the visual cortex. Nat New Biol 238: 124-126, 1972.
9. Blakemore C, Tobin EA. Lateral inhibition between orientation detectors in the cat's visual cortex. Exp Brain Res 15: 439-440, 1972.
10. Brumberg JC, Pinto DJ, Simons DJ. Spatial gradients and inhibitory summation in the rat whisker barrel system. J Neurophysiol 76: 130-140, 1996.
11. Bruno RM, Simons DJ. Feedforward mechanisms of excitatory and inhibitory cortical receptive fields. J Neurosci 22: 10966-10975, 2002.
12. Burke D, Hagbarth KE, Lofstedt L, Wallin BG. The responses of human muscle spindle endings to vibration of non-contracting muscles. J Physiol 261: 673-693, 1976.
13. Chapin JK. Laminar differences in sizes, shapes, and response profiles of cutaneous receptive fields in the rat SI cortex. Exp Brain Res 62: 549-559, 1986.
14. Constantinidis C, Goldman-Rakic PS. Correlated discharges among putative pyramidal neurons and interneurons in the primate prefrontal cortex. J Neurophysiol 88: 3487-3497, 2002.
15. Cruikshank SJ, Lewis TJ, Connors BW. Synaptic basis for intense thalamocortical activation of feedforward inhibitory cells in neocortex. Nat Neurosci 10: 462-468, 2007.
16. Cruikshank SJ, Urabe H, Nurmikko AV, Connors BW. Pathway-specific feedforward circuits between thalamus and neocortex revealed by selective optical stimulation of axons. Neuron 65: 230-245, 2010.
17. DeFelipe J, Elston GN, Fujita I, Fuster J, Harrison KH, Hof PR, Kawaguchi Y, Martin KA, Rockland KS, Thomson AM, Wang SS, White EL, Yuste R. Neocortical circuits: evolutionary aspects and specificity versus non-specificity of synaptic connections. Remarks, main conclusions and general comments and discussion. J Neurocytol 31: 387-416, 2002.
18. Fetz EE, Gustafsson B. Relation between shapes of post-synaptic potentials and changes in firing probability of cat motoneurones. J Physiol 341: 387-410, 1983.
19. Fetz EE, Toyama K, Smith W. Synaptic interactions between cortical neurons. In: Cerebral Cortex, Vol. IX: Altered Cortical States, edited by Peters A and Jones EG. New York: Plenum Press, 1991, p. 1-47.
20. Gabernet L, Jadhav SP, Feldman DE, Carandini M, Scanziani M. Somatosensory integration controlled by dynamic thalamocortical feed-forward inhibition. Neuron 48: 315-327, 2005.
21. Galarreta M, Hestrin S. A network of fast-spiking cells in the neocortex connected by electrical synapses. Nature 402: 72-75, 1999.
22. Gibson JR, Beierlein M, Connors BW. Two networks of electrically coupled inhibitory neurons in neocortex. Nature 402: 75-79, 1999.
23. Gil Z, Amitai Y. Properties of convergent thalamocortical and intracortical synaptic potentials in single neurons of neocortex. J Neurosci 16: 6567-6578, 1996.
24. Godschalk M, Lemon RN, Kuypers HG, Ronday HK. Cortical afferents and efferents of monkey postarcuate area: an anatomical and electrophysiological study. Exp Brain Res 56: 410-424, 1984.
25. Inoue T, Imoto K. Feedforward inhibitory connections from multiple thalamic cells to multiple regular-spiking cells in layer 4 of the somatosensory cortex. J Neurophysiol 96: 1746-1754, 2006.
26. Kawaguchi Y. Physiological subgroups of nonpyramidal cells with specific morphological characteristics in layer II/III of rat frontal cortex. J Neurosci 15: 2638-2655, 1995.
27. Kawaguchi Y, Kubota Y. Correlation of physiological subgroupings of nonpyramidal cells with parvalbumin-and calbindinD28k-immunoreactive neurons in layer V of rat frontal cortex. J Neurophysiol 70: 387-396, 1993.
28. Kawaguchi Y, Kubota Y. Physiological and morphological identification of somatostatin-or vasoactive intestinal polypeptide-containing cells among GABAergic cell subtypes in rat frontal cortex. J Neurosci 16: 2701-2715, 1996.
29. Keller A. Intrinsic synaptic interactions in the barrel cortex. Proceedings of the Fourth Meeting of the German Neuroscience Society. Göttingen, Germany, 2001, p. 138.
30. Keller A. The role of intrinsic circuitry in motor cortex plasticity. In: The Changing Nervous System: Neurobehavioral Consequences of Early Brain Disorders, edited by Broman SA and Fletcher JM. New York: Oxford Univ. Press, 1999, p. 428.
31. Khatri V, Hartings JA, Simons DJ. Adaptation in thalamic barreloid and cortical barrel neurons to periodic whisker deflections varying in frequency and velocity. J Neurophysiol 92: 3244-3254, 2004.
32. Levy SC, Law AJ, Davidson AG, Schieber MH. Fast-spiking to regularspiking contnuum among primate motor cortex neurons (Online). Program no. 494.16.2010 Neuroscience Meeting Planner. San Diego, CA: Society for Neuroscience, 2010.
33. McCormick DA, Connors BW, Lighthall JW, Prince DA. Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. J Neurophysiol 54: 782-806, 1985.
34. Miller KD, Pinto DJ, Simons DJ. Processing in layer 4 of the neocortical circuit: new insights from visual and somatosensory cortex. Curr Opin Neurobiol 11: 488-497, 2001.
35. Mountcastle VB, Talbot WH, Sakata H, Hyvarinen J. Cortical neuronal mechanisms in flutter-vibration studied in unanesthetized monkeys. Neuronal periodicity and frequency discrimination. J Neurophysiol 32: 452-484, 1969.
36. Neafsey EJ, Bold EL, Haas G, Hurley-Gius KM, Quirk G, Sievert CF, Terreberry RR. The organization of the rat motor cortex: a microstimulation mapping study. Brain Res 396: 77-96, 1986.
37. Nudo RJ. Mechanisms for recovery of motor function following cortical damage. Curr Opin Neurobiol 16: 638-644, 2006.
38. Ozeki H, Finn IM, Schaffer ES, Miller KD, Ferster D. Inhibitory stabilization of the cortical network underlies visual surround suppression. Neuron 62: 578-592, 2009.
39. Penfield W, Rasmussen T. The Cerebral Cortex of Man: A Clinical Study of Localization of Function. New York: MacMillan, 1950.
40. Porter JT, Johnson CK, Agmon A. Diverse types of interneurons generate thalamus-evoked feedforward inhibition in the mouse barrel cortex. J Neurosci 21: 2699-2710, 2001.
41. Porter LL. Patterns of projections from area 2 of the sensory cortex to area 3a and to the motor cortex in cats. Exp Brain Res 91: 85-93, 1992.
42. Roll JP, Vedel JP, Ribot E. Alteration of proprioceptive messages induced by tendon vibration in man: a microneurographic study. Exp Brain Res 76: 213-222, 1989.
43. Rosenkranz K, Rothwell JC. Differential effect of muscle vibration on intracortical inhibitory circuits in humans. J Physiol 551: 649-660, 2003.
44. Sanes JN, Donoghue JP. Plasticity and primary motor cortex. Annu Rev Neurosci 23: 393-415, 2000.
45. Sapienza S, Talbi B, Jacquemin J, Albe-Fessard D. Relationship between input and output of cells in motor and somatosensory cortices of the chronic awake rat. A study using glass micropipettes. Exp Brain Res 43: 47-56, 1981.
46. Schieber MH. Constraints on somatotopic organization in the primary motor cortex. J Neurophysiol 86: 2125-2143, 2001.
47. Simons DJ. Response properties of vibrissa units in rat SI somatosensory neocortex. J Neurophysiol 41: 798-820, 1978.
48. Simons DJ, Carvell GE. Thalamocortical response transformation in rat vibrissa/barrel system. J Neurophysiol 61: 311-330, 1989.
49. Sun QQ, Huguenard JR, Prince DA. Barrel cortex microcircuits: thalamocortical feedforward inhibition in spiny stellate cells is mediated by a small number of fast-spiking interneurons. J Neurosci 26: 1219-1230, 2006.
50. Swadlow HA. Efferent neurons and suspected interneurons in motor cortex of the awake rabbit: axonal properties, sensory receptive fields, and subthreshold synaptic inputs. J Neurophysiol 71: 437-453, 1994.
51. Swadlow HA. Fast-spike interneurons and feedforward inhibition in awake sensory neocortex. Cereb Cortex 13: 25-32, 2003.
52. Swadlow HA. Influence of VPM afferents on putative inhibitory interneurons in S1 of the awake rabbit: evidence from cross-correlation, microstimulation, and latencies to peripheral sensory stimulation. J Neurophysiol 73: 1584-1599, 1995.
53. Swadlow HA. Thalamocortical control of feed-forward inhibition in awake somatosensory 'barrel' cortex. Philos Trans R Soc Lond B Biol Sci 357: 1717-1727, 2002.
54. Swadlow HA, Beloozerova IN, Sirota MG. Sharp, local synchrony among putative feed-forward inhibitory interneurons of rabbit somatosensory cortex. J Neurophysiol 79: 567-582, 1998.
55. Swadlow HA, Gusev AG. Receptive-field construction in cortical inhibitory interneurons. Nat Neurosci 5: 403-404, 2002.
56. Swadlow HA, Weyand TG. Corticogeniculate neurons, corticotectal neurons, and suspected interneurons in visual cortex of awake rabbits: receptive-field properties, axonal properties, and effects of EEG arousal. J Neurophysiol 57: 977-1001, 1987.
57. Wehr M, Zador AM. Synaptic mechanisms of forward suppression in rat auditory cortex. Neuron 47: 437-445, 2005.
58. Wilent WB, Contreras D. Dynamics of excitation and inhibition underlying stimulus selectivity in rat somatosensory cortex. Nat Neurosci 8: 1364-1370, 2005.
59. Woolsey CN, Settlage PH, Meyer DR, Sencer W, Pinto Hamuy T, Travis AM. Patterns of localization in precentral and "supplementary" motor areas and their relation to the concept of a premotor area. Res Publ Assoc Res Nerv Ment Dis 30: 238-264, 1952.
60. Zarzecki P. The distribution of corticocortical, thalamocortical, and callosal inputs on identified motor cortex output neurons: mechanisms for their selective recruitment. Somatosens Mot Res 8: 313-325, 1991.
61. Zhu JJ, Connors BW. Intrinsic firing patterns and whisker-evoked synaptic responses of neurons in the rat barrel cortex. J Neurophysiol 81: 1171-1183, 1999.