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Published in: Brain Structure and Function 1/2019

01-01-2019 | Original Article

Modulation of olfactory-driven behavior by metabolic signals: role of the piriform cortex

Authors: Dolly Al Koborssy, Brigitte Palouzier-Paulignan, Vincent Canova, Marc Thevenet, Debra Ann Fadool, Andrée Karyn Julliard

Published in: Brain Structure and Function | Issue 1/2019

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Abstract

Olfaction is one of the major sensory modalities that regulates food consumption and is in turn regulated by the feeding state. Given that the olfactory bulb has been shown to be a metabolic sensor, we explored whether the anterior piriform cortex (aPCtx)—a higher olfactory cortical processing area—had the same capacity. Using immunocytochemical approaches, we report the localization of Kv1.3 channel, glucose transporter type 4, and the insulin receptor in the lateral olfactory tract and Layers II and III of the aPCtx. In current-clamped superficial pyramidal (SP) cells, we report the presence of two populations of SP cells: glucose responsive and non-glucose responsive. Using varied glucose concentrations and a glycolysis inhibitor, we found that insulin modulation of the instantaneous and spike firing frequency are both glucose dependent and require glucose metabolism. Using a plethysmograph to record sniffing frequency, rats microinjected with insulin failed to discriminate ratiometric enantiomers; considered a difficult task. Microinjection of glucose prevented discrimination of odorants of different chain-lengths, whereas injection of margatoxin increased the rate of habituation to repeated odor stimulation and enhanced discrimination. These data suggest that metabolic signaling pathways that are present in the aPCtx are capable of neuronal modulation and changing complex olfactory behaviors in higher olfactory centers.
Literature
go back to reference Ainscow EK, Mirshamsi S, Tang T, Ashford ML, Rutter GA (2002) Dynamic imaging of free cytosolic ATP concentration during fuel sensing by rat hypothalamic neurones: evidence for ATP-independent control of ATP-sensitive K(+) channels. J Physiol 544(Pt 2):429–445PubMedPubMedCentralCrossRef Ainscow EK, Mirshamsi S, Tang T, Ashford ML, Rutter GA (2002) Dynamic imaging of free cytosolic ATP concentration during fuel sensing by rat hypothalamic neurones: evidence for ATP-independent control of ATP-sensitive K(+) channels. J Physiol 544(Pt 2):429–445PubMedPubMedCentralCrossRef
go back to reference Anand BK, Chhina GS, Sharma KN, Dua S, Singh B (1964) Activity of single neurons in the hypothalamic feeding centers: effect of glucose. Am J Physiol 207:1146–1154PubMedCrossRef Anand BK, Chhina GS, Sharma KN, Dua S, Singh B (1964) Activity of single neurons in the hypothalamic feeding centers: effect of glucose. Am J Physiol 207:1146–1154PubMedCrossRef
go back to reference Banks WA, Kastin AJ, Pan W (1999) Uptake and degradation of blood-borne insulin by the olfactory bulb. Peptides 20(3):373–378PubMedCrossRef Banks WA, Kastin AJ, Pan W (1999) Uptake and degradation of blood-borne insulin by the olfactory bulb. Peptides 20(3):373–378PubMedCrossRef
go back to reference Baskin DG, Porte D, Guest K, Dorsa DM (1983) Regional concentrations of insulin in the rat brain. Endocrinology 112(3):898–903PubMedCrossRef Baskin DG, Porte D, Guest K, Dorsa DM (1983) Regional concentrations of insulin in the rat brain. Endocrinology 112(3):898–903PubMedCrossRef
go back to reference Bignami A, Eng LF, Dahl D, Uyeda CT (1972) Localization of the glial fibrillary acidic protein in astrocytes by immunofluorescence. Brain Res 43(2):429–435CrossRefPubMed Bignami A, Eng LF, Dahl D, Uyeda CT (1972) Localization of the glial fibrillary acidic protein in astrocytes by immunofluorescence. Brain Res 43(2):429–435CrossRefPubMed
go back to reference Cayabyab FS, Khanna R, Jones OT, Schlichter LC (2000) Suppression of the rat microglia Kv1.3 current by src-family tyrosine kinases and oxygen/glucose deprivation. Eur J Neurosci 12(6):1949–1960PubMedCrossRef Cayabyab FS, Khanna R, Jones OT, Schlichter LC (2000) Suppression of the rat microglia Kv1.3 current by src-family tyrosine kinases and oxygen/glucose deprivation. Eur J Neurosci 12(6):1949–1960PubMedCrossRef
go back to reference Cleland TA, Morse A, Yue EL, Linster C (2002) Behavioral models of odor similarity. Behav Neurosci 116(2):222–231PubMedCrossRef Cleland TA, Morse A, Yue EL, Linster C (2002) Behavioral models of odor similarity. Behav Neurosci 116(2):222–231PubMedCrossRef
go back to reference De Rosa E, Hasselmo ME (2000) Muscarinic cholinergic neuromodulation reduces proactive interference between stored odor memories during associative learning in rats. Behav Neurosci 114(1):32–41PubMedCrossRef De Rosa E, Hasselmo ME (2000) Muscarinic cholinergic neuromodulation reduces proactive interference between stored odor memories during associative learning in rats. Behav Neurosci 114(1):32–41PubMedCrossRef
go back to reference Dunn-Meynell AA, Routh VH, Kang L, Gaspers L, Levin BE (2002) Glucokinase is the likely mediator of glucosensing in both glucose-excited and glucose-inhibited central neurons. Diabetes 51(7):2056–2065PubMedCrossRef Dunn-Meynell AA, Routh VH, Kang L, Gaspers L, Levin BE (2002) Glucokinase is the likely mediator of glucosensing in both glucose-excited and glucose-inhibited central neurons. Diabetes 51(7):2056–2065PubMedCrossRef
go back to reference Ekstrand JJ, Domroese ME, Johnson DM, Feig SL, Knodel SM, Behan M, Haberly LB (2001) A new subdivision of anterior piriform cortex and associated deep nucleus with novel features of interest for olfaction and epilepsy. J Comp Neurol 434(3):289–307PubMedCrossRef Ekstrand JJ, Domroese ME, Johnson DM, Feig SL, Knodel SM, Behan M, Haberly LB (2001) A new subdivision of anterior piriform cortex and associated deep nucleus with novel features of interest for olfaction and epilepsy. J Comp Neurol 434(3):289–307PubMedCrossRef
go back to reference El Messari S, Ait-Ikhlef A, Ambroise DH, Penicaud L, Arluison M (2002) Expression of insulin-responsive glucose transporter GLUT4 mRNA in the rat brain and spinal cord: an in situ hybridization study. J Chem Neuroanat 24(4):225–242. (S0891061802000583 [pii])PubMedCrossRef El Messari S, Ait-Ikhlef A, Ambroise DH, Penicaud L, Arluison M (2002) Expression of insulin-responsive glucose transporter GLUT4 mRNA in the rat brain and spinal cord: an in situ hybridization study. J Chem Neuroanat 24(4):225–242. (S0891061802000583 [pii])PubMedCrossRef
go back to reference Eng LF, Vanderhaeghen JJ, Bignami A, Gerstl B (1971) An acidic protein isolated from fibrous astrocytes. Brain Res 28(2):351–354PubMedCrossRef Eng LF, Vanderhaeghen JJ, Bignami A, Gerstl B (1971) An acidic protein isolated from fibrous astrocytes. Brain Res 28(2):351–354PubMedCrossRef
go back to reference Fadool DA, Tucker K, Phillips JJ, Simmen JA (2000) Brain insulin receptor causes activity-dependent current suppression in the olfactory bulb through multiple phosphorylation of Kv1.3. J Neurophysiol 83(4):2332–2348PubMedCrossRef Fadool DA, Tucker K, Phillips JJ, Simmen JA (2000) Brain insulin receptor causes activity-dependent current suppression in the olfactory bulb through multiple phosphorylation of Kv1.3. J Neurophysiol 83(4):2332–2348PubMedCrossRef
go back to reference Fadool DA, Tucker K, Perkins R, Fasciani G, Thompson RN, Parsons AD, Overton JM, Koni PA, Flavell RA, Kaczmarek LK (2004) Kv1.3 channel gene-targeted deletion produces “Super-Smeller Mice” with altered glomeruli, interacting scaffolding proteins, and biophysics. Neuron 41(3):389–404. (S0896627303008444 [pii])PubMedPubMedCentralCrossRef Fadool DA, Tucker K, Perkins R, Fasciani G, Thompson RN, Parsons AD, Overton JM, Koni PA, Flavell RA, Kaczmarek LK (2004) Kv1.3 channel gene-targeted deletion produces “Super-Smeller Mice” with altered glomeruli, interacting scaffolding proteins, and biophysics. Neuron 41(3):389–404. (S0896627303008444 [pii])PubMedPubMedCentralCrossRef
go back to reference Fletcher M, Wilson DA (2001) Ontogeny of odor discrimination: a method to assess novel odor discrimination in neonatal rats. Physiol Behav 74(4–5):589–593PubMedCrossRef Fletcher M, Wilson DA (2001) Ontogeny of odor discrimination: a method to assess novel odor discrimination in neonatal rats. Physiol Behav 74(4–5):589–593PubMedCrossRef
go back to reference Gibb AJ, Edwards FA (1994) Patch clamp recording from cells in sliced tissues. In: Microelectrode Techniques. The Plymouth Workshop Handbook, Cambridge Gibb AJ, Edwards FA (1994) Patch clamp recording from cells in sliced tissues. In: Microelectrode Techniques. The Plymouth Workshop Handbook, Cambridge
go back to reference Haberly LB (2001) Parallel-distributed processing in olfactory cortex: new insights from morphological and physiological analysis of neuronal circuitry. Chem Senses 26(5):551–576PubMedCrossRef Haberly LB (2001) Parallel-distributed processing in olfactory cortex: new insights from morphological and physiological analysis of neuronal circuitry. Chem Senses 26(5):551–576PubMedCrossRef
go back to reference Hill JM, Lesniak MA, Pert CB, Roth J (1986) Autoradiographic localization of insulin receptors in rat brain: prominence in olfactory and limbic areas. Neuroscience 17(4):1127–1138PubMedCrossRef Hill JM, Lesniak MA, Pert CB, Roth J (1986) Autoradiographic localization of insulin receptors in rat brain: prominence in olfactory and limbic areas. Neuroscience 17(4):1127–1138PubMedCrossRef
go back to reference Julliard AK, Hartmann DJ (1998) Spatiotemporal patterns of expression of extracellular matrix molecules in the developing and adult rat olfactory system. Neuroscience 84(4):1135–1150PubMedCrossRef Julliard AK, Hartmann DJ (1998) Spatiotemporal patterns of expression of extracellular matrix molecules in the developing and adult rat olfactory system. Neuroscience 84(4):1135–1150PubMedCrossRef
go back to reference Julliard A, Chaput M, Apelbaum A, Aime P, Mahfouz M, Duchamp-Viret P (2007) Changes in rat olfactory detection performance induced by orexin and leptin mimicking fasting and satiation. Behav Brain Res 183(2):123–129PubMedCrossRef Julliard A, Chaput M, Apelbaum A, Aime P, Mahfouz M, Duchamp-Viret P (2007) Changes in rat olfactory detection performance induced by orexin and leptin mimicking fasting and satiation. Behav Brain Res 183(2):123–129PubMedCrossRef
go back to reference Karschin C, Ecke C, Ashcroft FM, Karschin A (1997) Overlapping distribution of K(ATP) channel-forming Kir6.2 subunit and the sulfonylurea receptor SUR1 in rodent brain. FEBS Lett 401(1):59–64PubMedCrossRef Karschin C, Ecke C, Ashcroft FM, Karschin A (1997) Overlapping distribution of K(ATP) channel-forming Kir6.2 subunit and the sulfonylurea receptor SUR1 in rodent brain. FEBS Lett 401(1):59–64PubMedCrossRef
go back to reference Kaul L, Berdanier CD (1975) Effect of meal-feeding on the daily variations of insulin, glucose, and NADP-linked dehydrogenases in rats. J Nutr 105(9):1132–1140PubMedCrossRef Kaul L, Berdanier CD (1975) Effect of meal-feeding on the daily variations of insulin, glucose, and NADP-linked dehydrogenases in rats. J Nutr 105(9):1132–1140PubMedCrossRef
go back to reference Kobayashi M, Nikami H, Morimatsu M, Saito M (1996) Expression and localization of insulin-regulatable glucose transporter (GLUT4) in rat brain. Neurosci Lett 213(2):103–106PubMedCrossRef Kobayashi M, Nikami H, Morimatsu M, Saito M (1996) Expression and localization of insulin-regulatable glucose transporter (GLUT4) in rat brain. Neurosci Lett 213(2):103–106PubMedCrossRef
go back to reference Krimer LS, Goldman-Rakic PS (1997) An interface holding chamber for anatomical and physiological studies of living brain slices. J Neurosci Methods 75(1):55–58PubMedCrossRef Krimer LS, Goldman-Rakic PS (1997) An interface holding chamber for anatomical and physiological studies of living brain slices. J Neurosci Methods 75(1):55–58PubMedCrossRef
go back to reference Kues WA, Wunder F (1992) Heterogeneous expression patterns of mammalian potassium channel genes in developing and adult rat brain. Eur J Neurosci 4(12):1296–1308PubMedCrossRef Kues WA, Wunder F (1992) Heterogeneous expression patterns of mammalian potassium channel genes in developing and adult rat brain. Eur J Neurosci 4(12):1296–1308PubMedCrossRef
go back to reference Linster C, Hasselmo ME (2001) Neuromodulation and the functional dynamics of piriform cortex. Chem Senses 26(5):585–594PubMedCrossRef Linster C, Hasselmo ME (2001) Neuromodulation and the functional dynamics of piriform cortex. Chem Senses 26(5):585–594PubMedCrossRef
go back to reference Macrides F, Eichenbaum HB, Forbes WB (1982) Temporal relationship between sniffing and the limbic theta rhythm during odor discrimination reversal learning. J Neurosci 2(12):1705–1717PubMedCrossRefPubMedCentral Macrides F, Eichenbaum HB, Forbes WB (1982) Temporal relationship between sniffing and the limbic theta rhythm during odor discrimination reversal learning. J Neurosci 2(12):1705–1717PubMedCrossRefPubMedCentral
go back to reference Moriyama R, Tsukamura H, Kinoshita M, Okazaki H, Kato Y, Maeda K (2004) In vitro increase in intracellular calcium concentrations induced by low or high extracellular glucose levels in ependymocytes and serotonergic neurons of the rat lower brainstem. Endocrinology 145(5):2507–2515. https://doi.org/10.1210/en.2003-1191 PubMedCrossRef Moriyama R, Tsukamura H, Kinoshita M, Okazaki H, Kato Y, Maeda K (2004) In vitro increase in intracellular calcium concentrations induced by low or high extracellular glucose levels in ependymocytes and serotonergic neurons of the rat lower brainstem. Endocrinology 145(5):2507–2515. https://​doi.​org/​10.​1210/​en.​2003-1191 PubMedCrossRef
go back to reference Oomura Y, Ono T, Ooyama H, Wayner MJ (1969) Glucose and osmosensitive neurones of the rat hypothalamus. Nature 222(5190):282–284PubMedCrossRef Oomura Y, Ono T, Ooyama H, Wayner MJ (1969) Glucose and osmosensitive neurones of the rat hypothalamus. Nature 222(5190):282–284PubMedCrossRef
go back to reference Paxinos G, Watson C (2013) The rat brain in stereotaxic coordinates, 7th edn. Academic Press, San Diego Paxinos G, Watson C (2013) The rat brain in stereotaxic coordinates, 7th edn. Academic Press, San Diego
go back to reference Schulingkamp RJ, Pagano TC, Hung D, Raffa RB (2000) Insulin receptors and insulin action in the brain: review and clinical implications. Neurosci Biobehav Rev 24(8):855–872PubMedCrossRef Schulingkamp RJ, Pagano TC, Hung D, Raffa RB (2000) Insulin receptors and insulin action in the brain: review and clinical implications. Neurosci Biobehav Rev 24(8):855–872PubMedCrossRef
go back to reference Shepherd GM (2004) The synaptic organization of the brain, 5th edn. Oxford University Press, Oxford; New YorkCrossRef Shepherd GM (2004) The synaptic organization of the brain, 5th edn. Oxford University Press, Oxford; New YorkCrossRef
go back to reference Sitren HS, Stevenson NR (1978) The effects of meal-feeding at different times of the day on daily changes in serum insulin, gastrin and liver enzymes in the rat. J Nutr 108(9):1393–1401PubMedCrossRef Sitren HS, Stevenson NR (1978) The effects of meal-feeding at different times of the day on daily changes in serum insulin, gastrin and liver enzymes in the rat. J Nutr 108(9):1393–1401PubMedCrossRef
go back to reference Staubli U, Schottler F, Nejat-Bina D (1987) Role of dorsomedial thalamic nucleus and piriform cortex in processing olfactory information. Behav Brain Res 25(2):117–129PubMedCrossRef Staubli U, Schottler F, Nejat-Bina D (1987) Role of dorsomedial thalamic nucleus and piriform cortex in processing olfactory information. Behav Brain Res 25(2):117–129PubMedCrossRef
go back to reference Sundberg H, Doving K, Novikov S, Ursin H (1982) A method for studying responses and habituation to odors in rats. Behav Neural Biol 34(1):113–119PubMedCrossRef Sundberg H, Doving K, Novikov S, Ursin H (1982) A method for studying responses and habituation to odors in rats. Behav Neural Biol 34(1):113–119PubMedCrossRef
go back to reference Unger J, McNeill TH, Moxley RT, White M, Moss A, Livingston JN (1989) Distribution of insulin receptor-like immunoreactivity in the rat forebrain. Neuroscience 31(1):143–157PubMedCrossRef Unger J, McNeill TH, Moxley RT, White M, Moss A, Livingston JN (1989) Distribution of insulin receptor-like immunoreactivity in the rat forebrain. Neuroscience 31(1):143–157PubMedCrossRef
go back to reference Wada A, Yokoo H, Yanagita T, Kobayashi H (2005) New twist on neuronal insulin receptor signaling in health, disease, and therapeutics. J Pharmacol Sci 99(2):128–143PubMedCrossRef Wada A, Yokoo H, Yanagita T, Kobayashi H (2005) New twist on neuronal insulin receptor signaling in health, disease, and therapeutics. J Pharmacol Sci 99(2):128–143PubMedCrossRef
go back to reference Welker WI (1964) Analysis of sniffing of the albino rat. Behaviour 22(3–4):223–244CrossRef Welker WI (1964) Analysis of sniffing of the albino rat. Behaviour 22(3–4):223–244CrossRef
go back to reference Youngentob SL, Mozell MM, Sheehe PR, Hornung DE (1987) A quantitative analysis of sniffing strategies in rats performing odor detection tasks. Physiol Behav 41(1):59–69PubMedCrossRef Youngentob SL, Mozell MM, Sheehe PR, Hornung DE (1987) A quantitative analysis of sniffing strategies in rats performing odor detection tasks. Physiol Behav 41(1):59–69PubMedCrossRef
Metadata
Title
Modulation of olfactory-driven behavior by metabolic signals: role of the piriform cortex
Authors
Dolly Al Koborssy
Brigitte Palouzier-Paulignan
Vincent Canova
Marc Thevenet
Debra Ann Fadool
Andrée Karyn Julliard
Publication date
01-01-2019
Publisher
Springer Berlin Heidelberg
Published in
Brain Structure and Function / Issue 1/2019
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-018-1776-0

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