Dynamic cortical lateralization during olfactory discrimination learning

Journal of Physiology

Volumn 593, Issue 7, 2015, Pages 1701-1714

  Cohen, Yaniv ^a,b   Putrino, David ^c,d   Wilson, Donald A ^a,b  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NATHAN S KLINE INSTITUTE FOR PSYCHIATRIC RESEARCH   (United States)

^c WEILL CORNELL MEDICAL COLLEGE   (United States)

^d BURKE MEDICAL RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; BRAIN ELECTROPHYSIOLOGY; BRAIN FUNCTION; COGNITION; DISCRIMINATION LEARNING; ELECTRIC POTENTIAL; HEMISPHERIC DOMINANCE; LEFT HEMISPHERE; MALE; MENTAL PERFORMANCE; NONHUMAN; ODOR; OLFACTORY DISCRIMINATION; PRIORITY JOURNAL; PYRIFORM CORTEX; RAT; STEADY STATE; ANIMAL; ANIMAL BEHAVIOR; LONG EVANS RAT; MEMORY; OLFACTORY CORTEX; PHYSIOLOGY;

FRAGRANCE;

ANIMALS; BEHAVIOR, ANIMAL; DISCRIMINATION LEARNING; MALE; MEMORY; ODORANTS; OLFACTORY CORTEX; RATS, LONG-EVANS;

EID: 84926079706     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2014.288381     Document Type: Article

References (75)

1. 3H-imipramine binding: studies in the frontal cortex of normal controls and suicide victims. Biol Psychiatry 29, 1016-1022.
2. Barnes DC, Hofacer RD, Zaman AR, Rennaker RL & Wilson DA (2008). Olfactory perceptual stability and discrimination. Nat Neurosci 11, 1378-1380.
3. Bellas DN, Novelly RA & Eskenazi B (1989). Olfactory lateralization and identification in right hemisphere lesion and control patients. Neuropsychologia 27, 1187-1191.
4. Bojsen-Moller F & Fahrenkrug J (1971). Nasal swell-bodies and cyclic changes in the air passage of the rat and rabbit nose. J Anatomy 110, 25-37.
5. Bokil H, Andrews P, Kulkarni JE, Mehta S & Mitra PP (2010). Chronux: a platform for analyzing neural signals. J Neurosci Meth 192, 146-151.
6. Brand G & Jacquot L (2001). Quality of odor and olfactory lateralization processes in humans. Neurosci Lett 316, 91-94.
7. Brand G, Millot JL & Henquell D (2001). Complexity of olfactory lateralization processes revealed by functional imaging: a review. Neurosci Biobehav Rev 25, 159-166.
8. Bromley SM & Doty RL (1995). Odor recognition memory is better under bilateral than unilateral test conditions. Cortex 31, 25-40.
9. Brown JL & Brunjes PC (1990). Development of the anterior olfactory nucleus in normal and unilaterally odor deprived rats. J Comp Neurol 301, 15-22.
10. Brunjes PC ( 1994). Unilateral naris closure and olfactory system development. Brain Res Brain Res Rev 19, 146-160.
11. Carlson JN & Glick SD (1991). Brain laterality as a determinant of susceptibility to depression in an animal model. Brain Res 550, 324-328.
12. Chabaud P, Ravel N, Wilson DA, Mouly AM, Vigouroux M, Farget V & Gervais R (2000). Exposure to behaviourally relevant odour reveals differential characteristics in rat central olfactory pathways as studied through oscillatory activities. Chem Senses 25, 561-573.
13. Chapuis J, Garcia S, Messaoudi B, Thevenet M, Ferreira G, Gervais R & Ravel N (2009). The way an odor is experienced during aversive conditioning determines the extent of the network recruited during retrieval: a multisite electrophysiological study in rats. J Neurosci 29, 10287-10298.
14. Chapuis J & Wilson DA (2012). Bidirectional plasticity of cortical pattern recognition and behavioral sensory acuity. Nat Neurosci 15, 155-161.
15. Chen CF, Barnes DC & Wilson DA (2011). Generalized versus stimulus-specific learned fear differentially modifies stimulus encoding in primary sensory cortex of awake rats. J Neurophysiol 106, 3136-3144.
16. Cleland TA & Linster C (2003). Central olfactory structures. In Handbook of Olfaction and Gustation, 2nd edn, ed. Doty RL, pp. 165-180. Marcel Dekker, New York, NY.
17. Cohen Y, Avramoav S, Barkai E & Maroun M (2011). Olfactory learning-induced enhancement of the predisposition for LTP induction. Learn Mem 18, 594-597.
18. Cohen Y, Reuveni I, Barkai E & Maroun M (2008). Olfactory learning-induced long-lasting enhancement of descending and ascending synaptic transmission to the piriform cortex. J Neurosci 28, 6664-6669.
19. Cohen Y, Wilson DA & Barkai E (2015). Differential modifications of synaptic weights during odor rule learning: dynamics of interaction between the piriform cortex with lower and higher brain areas. Cereb Cortex 25, 180-191.
20. Cummings DM & Brunjes PC (1994). Changes in cell proliferation in the developing olfactory epithelium following neonatal unilateral naris occlusion. Exp Neurol 128, 124-128.
21. Dade LA, Zatorre RJ & Jones-Gotman M (2002). Olfactory learning: convergent findings from lesion and brain imaging studies in humans. Brain 125, 86-101.
22. Dennis NA, Kim H & Cabeza R (2007). Effects of aging on true and false memory formation: an fMRI study. Neuropsychologia 45, 3157-3166.
23. Fontaine CJ, Harley CW & Yuan Q (2013). Lateralized odor preference training in rat pups reveals an enhanced network response in anterior piriform cortex to olfactory input that parallels extended memory. J Neurosci 33, 15126-15131.
24. Frazier LL & Brunjes PC (1988). Unilateral odor deprivation: early postnatal changes in olfactory bulb cell density and number. J Comp Neurol 269, 355-370.
25. Frazier-Cierpial L & Brunjes PC (1989a). Early postnatal cellular proliferation and survival in the olfactory bulb and rostral migratory stream of normal and unilaterally odor-deprived rats. J Comp Neurol 289, 481-492.
26. Frazier-Cierpial LL & Brunjes PC (1989b). Early postnatal differentiation of granule cell dendrites in the olfactory bulbs of normal and unilaterally odor-deprived rats. Brain Res Dev Brain Res 47, 129-136.
27. Gordon HW & Sperry RW (1969). Lateralization of olfactory perception in the surgically separated hemispheres of man. Neuropsychologia 7, 111-120.
28. Herz RS, McCall C & Cahill L (1999). Hemispheric lateralization in the processing of odor pleasantness versus odor names. Chem Senses 24, 691-695.
29. Hill SY, Wang S, Kostelnik B, Carter H, Holmes B, McDermott M, Zezza N, Stiffler S & Keshavan MS (2009). Disruption of orbitofrontal cortex laterality in offspring from multiplex alcohol dependence families. Biol Psychiatry 65, 129-136.
30. Hudry J, Ryvlin P, Saive AL, Ravel N, Plailly J & Royet JP (2014). Lateralization of olfactory processing: differential impact of right and left temporal lobe epilepsies. Epilepsy Behav 37, 184-190.
31. Hugdahl K ( 2005). Symmetry and asymmetry in the human brain. Eur Rev 13, Supp. 2, 119-133.
32. Jones-Gotman M & Zatorre RJ (1993). Odor recognition memory in humans: role of right temporal and orbitofrontal regions. Brain Cogn 22, 182-198.
33. Kavcic V, Zhong J, Yoshiura T & Doty RW (2003). Frontal cortex, laterality, and memory: encoding versus retrieval. Acta Neurobiol Exp 63, 337-350.
34. Kay LM & Beshel J (2010). A beta oscillation network in the rat olfactory system during a 2-alternative choice odor discrimination task. J Neurophysiol 104, 829-839.
35. Kay LM, Beshel J, Brea J, Martin C, Rojas-Libano D & Kopell N (2009). Olfactory oscillations: the what, how and what for. Trends Neurosci 32, 207-214.
36. Kay LM & Freeman WJ (1998). Bidirectional processing in the olfactory-limbic axis during olfactory behavior. Behav Neurosci 112, 541-553.
37. Kikuta S, Sato K, Kashiwadani H, Tsunoda K, Yamasoba T & Mori K (2010). Neurons in the anterior olfactory nucleus pars externa detect right or left localization of odor sources. Proc Natl Acad Sci USA 107, 12363-12368.
38. Kucharski D, Arnold HM & Hall WG (1995). Unilateral conditioning of an odor aversion in 6-day-old rat pups. Behav Neurosci 109, 563-566.
39. Kucharski D & Hall WG (1987). New routes to early memories. Science 238, 786-788.
40. Liu Q, Li A, Gong L, Zhang L, Wu N & Xu F (2013). Decreased coherence between the two olfactory bulbs in Alzheimer's disease model mice. Neurosci Lett 545, 81-85.
41. Long X, Zhang L, Liao W, Jiang C & Qiu B (2013). Distinct laterality alterations distinguish mild cognitive impairment and Alzheimer's disease from healthy aging: statistical parametric mapping with high resolution MRI. Hum Brain Mapp 34, 3400-3410.
42. Lovitz AM, Sloan AM, Rennaker RL & Wilson DA (2012). Complex mixture discrimination and the role of contaminants. Chem Senses 37, 533-540.
43. Lowell SY, Reynolds RC, Chen G, Horwitz B & Ludlow CL (2012). Functional connectivity and laterality of the motor and sensory components in the volitional swallowing network. Exp Brain Res 219, 85-96.
44. Martin C, Beshel J & Kay LM (2007). An olfacto-hippocampal network is dynamically involved in odor-discrimination learning. J Neurophysiol 98, 2196-2205.
45. Martin C, Gervais R, Hugues E, Messaoudi B & Ravel N (2004). Learning modulation of odor-induced oscillatory responses in the rat olfactory bulb: a correlate of odor recognition? J Neurosci 24, 389-397.
46. Martin C, Gervais R, Messaoudi B & Ravel N (2006). Learning-induced oscillatory activities correlated to odour recognition: a network activity. Eur J Neurosci 23, 1801-1810.
47. Martin C & Ravel N (2014). Beta and gamma oscillatory activities associated with olfactory memory tasks: different rhythms for different functional networks? Front Behav Neurosci 8, 218.
48. Mitra PP & Bokil H (2008). Observed Brain Dynamics. Oxford University Press, New York, NY.
49. Neville KR & Haberly LB (2003). Beta and gamma oscillations in the olfactory system of the urethane-anesthetized rat. J Neurophysiol 90, 3921-3930.
50. Oertel V, Knochel C, Rotarska-Jagiela A, Schonmeyer R, Lindner M, vande Ven V, Haenschel C, Uhlhaas P, Maurer K & Linden DE (2010). Reduced laterality as a trait marker of schizophrenia - evidence from structural and functional neuroimaging. J Neurosci 30, 2289-2299.
51. Olds JL, Anderson ML, McPhie DL, Staten LD & Alkon DL (1989). Imaging of memory-specific changes in the distribution of protein kinase C in the hippocampus. Science 245, 866-869.
52. Olds JL, Bhalla US, McPhie DL, Lester DS, Bower JM & Alkon DL (1994). Lateralization of membrane-associated protein kinase C in rat piriform cortex: specific to operant training cues in the olfactory modality. Behav Brain Res 61, 37-46.
53. Parthasarathy K & Bhalla US (2013). Laterality and symmetry in rat olfactory behavior and in physiology of olfactory input. J Neurosci 33, 5750-5760.
54. Philpot BD, Men D, McCarty R & Brunjes PC (1998). Activity-dependent regulation of dopamine content in the olfactory bulbs of naris-occluded rats. Neuroscience 85, 969-977.
55. Porter J, Craven B, Khan RM, Chang SJ, Kang I, Judkewitz B, Volpe J, Settles G & Sobel N (2007). Mechanisms of scent-tracking in humans. Nat Neurosci 10, 27-29.
56. Rajan R, Clement JP & Bhalla US (2006). Rats smell in stereo. Science 311, 666-670.
57. Rausch R, Serafetinides EA & Crandall PH (1977). Olfactory memory in patients with anterior temporal lobectomy. Cortex 13, 445-452.
58. Ray JP & Price JL (1992). The organization of the thalamocortical connections of the mediodorsal thalamic nucleus in the rat, related to the ventral forebrain-prefrontal cortex topography. J Comp Neurol 323, 167-197.
59. Royet JP & Plailly J (2004). Lateralization of olfactory processes. Chem Senses 29, 731-745.
60. Saar D & Barkai E (2009). Long-lasting maintenance of learning-induced enhanced neuronal excitability: mechanisms and functional significance. Mol Neurobiol 39, 171-177.
61. Sacktor TC, Osten P, Valsamis H, Jiang X, Naik MU & Sublette E (1993). Persistent activation of the zeta isoform of protein kinase C in the maintenance of long-term potentiation. Proc Natl Acad Sci USA 90, 8342-8346.
62. Serrano P, Friedman EL, Kenney J, Taubenfeld SM, Zimmerman JM, Hanna J, Alberini C, Kelley AE, Maren S, Rudy JW, Yin JC, Sacktor TC & Fenton AA (2008). PKMzeta maintains spatial, instrumental, and classically conditioned long-term memories. PLoS Biol 6, 2698-2706.
63. Shi F, Liu B, Zhou Y, Yu C & Jiang T (2009). Hippocampal volume and asymmetry in mild cognitive impairment and Alzheimer's disease: meta-analyses of MRI studies. Hippocampus 19, 1055-1064.
64. Shipton OA, El-Gaby M, Apergis-Schoute J, Deisseroth K, Bannerman DM, Paulsen O & Kohl MM (2014). Left-right dissociation of hippocampal memory processes in mice. Proc Natl Acad Sci USA 111, 15238-15243.
65. Smaers JB, Mulvaney PI, Soligo C, Zilles K & Amunts K (2012). Sexual dimorphism and laterality in the evolution of the primate prefrontal cortex. Brain Behav Evol 79, 205-212.
66. Sobel N, Khan RM, Saltman A, Sullivan EV & Gabrieli JD (1999). The world smells different to each nostril. Nature 402, 35.
67. Tang AC, Zou B, Reeb BC & Connor JA (2008). An epigenetic induction of a right-shift in hippocampal asymmetry: selectivity for short- and long-term potentiation but not post-tetanic potentiation. Hippocampus 18, 5-10.
68. Thompson PM, Moussai J, Zohoori S, Goldkorn A, Khan AA, Mega MS, Small GW, Cummings JL & Toga AW (1998). Cortical variability and asymmetry in normal aging and Alzheimer's disease. Cereb Cortex 8, 492-509.
69. Thuerauf N, Gossler A, Lunkenheimer J, Lunkenheimer B, Maihofner C, Bleich S, Kornhuber J, Markovic K & Reulbach U (2008). Olfactory lateralization: odor intensity but not the hedonic estimation is lateralized. Neurosci Lett 438, 228-232.
70. von Baumgarten T, Green JD & Mancia M (1962). Recurrent inhibition in the olfactory bulb. II. Effects of antidromic stimulation of commissural fibers. J Neurophysiol 25, 489-500.
71. Werntz DA, Bickford RG & Shannahoff-Khalsa D (1987). Selective hemispheric stimulation by unilateral forced nostril breathing. Hum Neurobiol 6, 165-171.
72. Wilson DA ( 1997). Binaral interactions in the rat piriform cortex. J Neurophysiol 78, 160-169.
73. Wilson DA & Sullivan RM (1999). Respiratory airflow pattern at the rat's snout and an hypothesis regarding its role in olfaction. Physiol Behav 66, 41-44.
74. Zatorre RJ, Jones-Gotman M, Evans AC & Meyer E (1992). Functional localization and lateralization of human olfactory cortex. Nature 360, 339-340.
75. Zucco GM & Tressoldi PE (1989). Hemispheric differences in odour recognition. Cortex 25, 607-615.