Complex metabolically demanding sensory processing in the olfactory system: Implications for epilepsy

Epilepsy and Behavior

Volumn 38, Issue , 2014, Pages 37-42

  Restrepo, Diego ^a,b   Hellier, Jennifer L ^a   Salcedo, Ernesto ^a  

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

^b UNIVERSITY OF COLORADO   (United States)

Author keywords

Epilepsy; Olfaction; Olfactory bulb; Piriform

Indexed keywords

CELL ACTIVITY; DISEASE ASSOCIATION; EPILEPSY; EPILEPTOGENESIS; EXPERIMENTAL MODEL; GABAERGIC SYSTEM; HUMAN; INHIBITION KINETICS; INTERNEURON; NONHUMAN; OLFACTORY SYSTEM; PREPIRIFORM CORTEX; PYRIFORM CORTEX; REVIEW; SEIZURE; SENSORY ANALYSIS; SENSORY NERVE CELL; SMELLING; ANIMAL; METABOLISM; OLFACTORY BULB; PATHOPHYSIOLOGY; PHYSIOLOGY;

4 AMINOBUTYRIC ACID RECEPTOR;

ANIMALS; EPILEPSY; GABAERGIC NEURONS; OLFACTORY BULB; OLFACTORY PERCEPTION; PIRIFORM CORTEX;

EID: 84910600202     PISSN: 15255050     EISSN: 15255069     Source Type: Journal    
DOI: 10.1016/j.yebeh.2013.08.036     Document Type: Review

References (70)

1. Annegers J.F. The epidemiology of epilepsy. The treatment of epilepsy: principles and practice 2001, 131-138. Lippincott Williams & Wilkins, Philadelphia. E. Wyllie (Ed.).
2. Benbadis S.R. Epileptic seizures and syndromes. Neurol Clin 2001, 19:251-270.
3. Chang B.S., Lowenstein D.H. Epilepsy. N Engl J Med 2003, 349:1257-1266.
4. Engel J. Surgery for seizures. N Engl J Med 1996, 334:647-652.
5. Williamson P.D., French J.A., Thadani V.M., Kim J.H., Novelly R.A., Spencer S.S., et al. Characteristics of medial temporal lobe epilepsy: II. interictal and ictal scalp electroencephalography, neuropsychological testing, neuroimaging, surgical results, and pathology. Ann Neurol 1993, 34:781-787.
6. Brodie M.J. Diagnosing and predicting refractory epilepsy. Acta Neurol Scand Suppl 2005, 181:36-39.
7. Kwan P., Brodie M.J. Early identification of refractory epilepsy. N Engl J Med 2000, 342:314-319.
8. Stables J.P., Bertram E., Dudek F.E., Holmes G., Mathern G., Pitkanen A., et al. Therapy discovery for pharmacoresistant epilepsy and for disease-modifying therapeutics: summary of the NIH/NINDS/AES models II workshop. Epilepsia 2003, 44:1472-1478.
9. Devinsky O. Patients with refractory seizures. N Engl J Med 1999, 340:1565-1570.
10. de Lanerolle N.C., Brines M., Williamson A., Kim J.H., Spencer D.D. Neurotransmitters and their receptors in human temporal lobe epilepsy. Epilepsy Res Suppl 1992, 7:235-250.
11. Malmgren K., Thom M. Hippocampal sclerosis-origins and imaging. Epilepsia 2012, 53(Suppl. 4):19-33.
12. Cohen A.S., Lin D.D., Quirk G.L., Coulter D.A. Dentate granule cell GABA(A) receptors in epileptic hippocampus: enhanced synaptic efficacy and altered pharmacology. Eur J Neurosci 2003, 17:1607-1616.
13. Lund I.V., Hu Y., Raol Y.H., Benham R.S., Faris R., Russek S.J., et al. BDNF selectively regulates GABAA receptor transcription by activation of the JAK/STAT pathway. Sci Signal 2008, 1:ra9.
14. Sayin U., Osting S., Hagen J., Rutecki P., Sutula T. Spontaneous seizures and loss of axo-axonic and axo-somatic inhibition induced by repeated brief seizures in kindled rats. J Neurosci 2003, 23:2759-2768.
15. Zhang N., Wei W., Mody I., Houser C.R. Altered localization of GABA(A) receptor subunits on dentate granule cell dendrites influences tonic and phasic inhibition in a mouse model of epilepsy. J Neurosci 2007, 27:7520-7531.
16. Kinoshita M., Ikeda A., Matsuhashi M., Matsumoto R., Hitomi T., Begum T., et al. Electric cortical stimulation suppresses epileptic and background activities in neocortical epilepsy and mesial temporal lobe epilepsy. Clin Neurophysiol 2005, 116:1291-1299.
17. Bender R.A., Soleymani S.V., Brewster A.L., Nguyen S.T., Beck H., Mathern G.W., et al. Enhanced expression of a specific hyperpolarization-activated cyclic nucleotide-gated cation channel (HCN) in surviving dentate gyrus granule cells of human and experimental epileptic hippocampus. J Neurosci 2003, 23:6826-6836.
18. Diao L., Hellier J.L., Uskert-Newsom J., Williams P.A., Staley K.J., Yee A.S. Diphenytoin, riluzole and lidocaine: three sodium channel blockers, with different mechanisms of action, decrease hippocampal epileptiform activity. Neuropharmacology 2013, 73C:48-55.
19. Grabenstatter H.L., Dudek F.E. A new potential AED, carisbamate, substantially reduces spontaneous motor seizures in rats with kainate-induced epilepsy. Epilepsia 2008, 49:1787-1794.
20. Grabenstatter H.L., Clark S., Dudek F.E. Anticonvulsant effects of carbamazepine on spontaneous seizures in rats with kainate-induced epilepsy: comparison of intraperitoneal injections with drug-in-food protocols. Epilepsia 2007, 48:2287-2295.
21. Grabenstatter H.L., Ferraro D.J., Williams P.A., Chapman P.L., Dudek F.E. Use of chronic epilepsy models in antiepileptic drug discovery: the effect of topiramate on spontaneous motor seizures in rats with kainate-induced epilepsy. Epilepsia 2005, 46:8-14.
22. Hellier J.L., White A., Williams P.A., Edward Dudek F., Staley K.J. NMDA receptor-mediated long-term alterations in epileptiform activity in experimental chronic epilepsy. Neuropharmacology 2009, 56:414-421.
23. Bertram E. The relevance of kindling for human epilepsy. Epilepsia 2007, 48(Suppl. 2):65-74.
24. Staley K., Hellier J.L., Dudek F.E. Do interictal spikes drive epileptogenesis?. Neuroscientist 2005, 11:272-276.
25. Muller C.J., Bankstahl M., Groticke I., Loscher W. Pilocarpine vs. lithium-pilocarpine for induction of status epilepticus in mice: development of spontaneous seizures, behavioral alterations and neuronal damage. Eur J Pharmacol 2009, 619:15-24.
26. Hong S.C., Holbrook E.H., Leopold D.A., Hummel T. Distorted olfactory perception: a systematic review. Acta Otolaryngol 2012, 132(Suppl. 1):S27-S31.
27. Acharya V., Acharya J., Luders H. Olfactory epileptic auras. Neurology 1998, 51:56-61.
28. Chen C., Shih Y.H., Yen D.J., Lirng J.F., Guo Y.C., Yu H.Y., et al. Olfactory auras in patients with temporal lobe epilepsy. Epilepsia 2003, 44:257-260.
29. Nagayama S., Enerva A., Fletcher M.L., Masurkar A.V., Igarashi K.M., Mori K., et al. Differential axonal projection of mitral and tufted cells in the mouse main olfactory system. Front Neural Circuits 2010, 4.
30. Shepherd G.M., Chen W.R., Greer C.A. Olfactory bulb. The synaptic organization of the brain 2004, 159-204. Oxford University Press, New York. G.M. Shepherd (Ed.).
31. Neville K.R., Haberly L.B. Olfactory cortex. The synaptic organization of the brain 2004, 415-454. Oxford UP, New York. 5th ed. G.M. Shepherd, C.A. Greer (Eds.).
32. Bertram E.H. Temporal lobe epilepsy: where do the seizures really begin?. Epilepsy Behav 2009, 14(Suppl. 1):32-37.
33. Thom M., Mathern G.W., Cross J.H., Bertram E.H. Mesial temporal lobe epilepsy: how do we improve surgical outcome?. Ann Neurol 2010, 68:424-434.
34. Traub R.D., Wong R.K., Miles R., Michelson H. A model of a CA3 hippocampal pyramidal neuron incorporating voltage-clamp data on intrinsic conductances. J Neurophysiol 1991, 66:635-650.
35. Bains J.S., Longacher J.M., Staley K.J. Reciprocal interactions between CA3 network activity and strength of recurrent collateral synapses. Nat Neurosci 1999, 2:720-726.
36. CO2 to cortical excitability via pH. Neuron 2005, 48:1011-1023.
37. Dulla C.G., Frenguelli B.G., Staley K.J., Masino S.A. Intracellular acidification causes adenosine release during states of hyperexcitability in the hippocampus. J Neurophysiol 2009, 102:1984-1993.
38. Hellier J.L., Grosshans D.R., Coultrap S.J., Jones J.P., Dobelis P., Browning M.D., et al. NMDA receptor trafficking at recurrent synapses stabilizes the state of the CA3 network. J Neurophysiol 2007, 98:2818-2826.
39. Miles R., Wong R.K. Single neurones can initiate synchronized population discharge in the hippocampus. Nature 1983, 306:371-373.
40. Stasheff S.F., Bragdon A.C., Wilson W.A. Induction of epileptiform activity in hippocampal slices by trains of electrical stimuli. Brain Res 1985, 344:296-302.
41. Yee A.S., Longacher J.M., Staley K.J. Convulsant and anticonvulsant effects on spontaneous CA3 population bursts. J Neurophysiol 2003, 89:427-441.
42. Hellier J.L., Dudek F.E. Chemoconvulsant model of chronic spontaneous seizures. Curr Protoc Neurosci 2005, [Chapter 9: Unit 9 19]. 10.1002/0471142301.ns0919s31.
43. Cavazos J.E., Das I., Sutula T.P. Neuronal loss induced in limbic pathways by kindling: evidence for induction of hippocampal sclerosis by repeated brief seizures. J Neurosci 1994, 14:3106-3121.
44. McNamara J.O. Kindling: an animal model of complex partial epilepsy. Ann Neurol 1984, 16:S72-S76. [Suppl.].
45. Loscher W. Animal models of intractable epilepsy. Prog Neurobiol 1997, 53:239-258.
46. Goddard G.V., McIntyre D.C., Leech C.K. A permanent change in brain function resulting from daily electrical stimulation. Exp Neurol 1969, 25:295-330.
47. Racine R.J. Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr Clin Neurophysiol 1972, 32:281-294.
48. Zhang X., Firestein S. The olfactory receptor gene superfamily of the mouse. Nat Neurosci 2002, 5:124-133.
49. Buck L.B. Unraveling the sense of smell (Nobel lecture). Angew Chem Int Ed Engl 2005, 44:6128-6140.
50. Axel R. Scents and sensibility: a molecular logic of olfactory perception (Nobel lecture). Angew Chem Int Ed Engl 2005, 44:6110-6127.
51. Gire D.H., Restrepo D., Sejnowski T.J., Greer C., De Carlos J.A., Lopez-Mascaraque L. Temporal processing in the olfactory system: can we see a smell?. Neuron 2013, 78:416-432.
52. Wachowiak M., Shipley M.T. Coding and synaptic processing of sensory information in the glomerular layer of the olfactory bulb. Semin Cell Dev Biol 2006, 17:411-423.
53. Bekkers J.M., Suzuki N. Neurons and circuits for odor processing in the piriform cortex. Trends Neurosci 2013, 36:429-438.
54. Gottfried J.A., Wilson D.A. Smell. Neurobiology of sensation and reward 2011, CRC Press, Boca Raton (FL). J.A. Gottfried (Ed.).
55. Luna V.M., Schoppa N.E. GABAergic circuits control input-spike coupling in the piriform cortex. J Neurosci 2008, 28:8851-8859.
56. Franks K.M., Isaacson J.S. Strong single-fiber sensory inputs to olfactory cortex: implications for olfactory coding. Neuron 2006, 49:357-363.
57. Luna V.M., Pettit D.L. Asymmetric rostro-caudal inhibition in the primary olfactory cortex. Nat Neurosci 2010, 13:533-535.
58. Igarashi K.M., Ieki N., An M., Yamaguchi Y., Nagayama S., Kobayakawa K., et al. Parallel mitral and tufted cell pathways route distinct odor information to different targets in the olfactory cortex. J Neurosci 2012, 32:7970-7985.
59. Gire D.H., Whitesell J.D., Doucette W., Restrepo D. Information for decision-making and stimulus identification is multiplexed in sensory cortex. Nat Neurosci 2013, 16:991-993.
60. Zelano C., Bensafi M., Porter J., Mainland J., Johnson B., Bremner E., et al. Attentional modulation in human primary olfactory cortex. Nat Neurosci 2005, 8:114-120.
61. Gottfried J.A. Central mechanisms of odour object perception. Nat Rev Neurosci 2010, 11:628-641.
62. Balu R., Pressler R.T., Strowbridge B.W. Multiple modes of synaptic excitation of olfactory bulb granule cells. J Neurosci 2007, 27:5621-5632.
63. Boyd A.M., Sturgill J.F., Poo C., Isaacson J.S. Cortical feedback control of olfactory bulb circuits. Neuron 2012, 76:1161-1174.
64. Markopoulos F., Rokni D., Gire D.H., Murthy V.N. Functional properties of cortical feedback projections to the olfactory bulb. Neuron 2012, 76:1175-1188.
65. Panuccio G., Sanchez G., Levesque M., Salami P., de Curtis M., Avoli M. On the ictogenic properties of the piriform cortex in vitro. Epilepsia 2012, 53:459-468.
66. Schwabe K., Ebert U., Loscher W. The central piriform cortex: anatomical connections and anticonvulsant effect of GABA elevation in the kindling model. Neuroscience 2004, 126:727-741.
67. Uva L., Trombin F., Carriero G., Avoli M., de Curtis M. Seizure-like discharges induced by 4-aminopyridine in the olfactory system of the in vitro isolated guinea pig brain. Epilepsia 2013, 54:605-615.
68. Nguyen M.Q., Ryba N.J. A smell that causes seizure. PLoS One 2012, 7:e41899.
69. Kass M.D., Moberly A.H., Rosenthal M.C., Guang S.A., McGann J.P. Odor-specific, olfactory marker protein-mediated sparsening of primary olfactory input to the brain after odor exposure. J Neurosci 2013, 33:6594-6602.
70. Johnson D.M., Illig K.R., Behan M., Haberly L.B. New features of connectivity in piriform cortex visualized by intracellular injection of pyramidal cells suggest that "primary" olfactory cortex functions like "association" cortex in other sensory systems. J Neurosci 2000, 20:6974-6982.