Interaction between olfaction and food intake: metabolic state drives changes in the astroglial deployment within the olfactory bulb glomeruli in rats

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Interaction between olfaction and food intake: metabolic state drives changes in the astroglial deployment within

the olfactory bulb glomeruli in rats

Virginie Daumas-Meyer, Gaelle Champeil Potokar, Catherine Papillon, Patrice Dahirel, Marielle Levillain, Patrice Congar, Isabelle Denis

To cite this version:

Virginie Daumas-Meyer, Gaelle Champeil Potokar, Catherine Papillon, Patrice Dahirel, Marielle Lev- illain, et al.. Interaction between olfaction and food intake: metabolic state drives changes in the astroglial deployment within the olfactory bulb glomeruli in rats. 23. meeting of the French Glial Cell Club ”Emerging Concepts in Glial Cell Research”, Jun 2016, Carry-le-Rouet, France. 2016.

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Fed rats and fasted rats (17h of food deprivation) with intra-peritoneal administration of :

Interaction between olfaction and food intake: metabolic state drives changes in the astroglial deployment within the olfactory bulb glomeruli in rats

Fasting status of the rats

Virginie Daumas-Meyer, Gaëlle Champeil-Potokar, Catherine Papillon, Patrice Dahirel, Marielle Levillain, Patrice Congar, Isabelle Denis.

virginie.daumas-meyer@jouy.inra.fr

Glycemia

(n=6)

Glycemia (mg/dL)

Fed 17h 24h 48h

60 80 100 120 140 160

a

b b

b

Body weight loss

(n=12)

Difference of body weight on 48h (in %)

Fed 17h 24h 48h

-20 -10 0 10 20

a

b b

c

Leptinemia

(n=12)

[Leptinemia] ng/mL

Fed 17h 24h 48h

0 1 2 3

4 a

b

b,c

c

Olfactory food seeking

(n=6)

Time of sniffing (in %)

Fed 17h 24h 48h

0 10 20 30 40 50

a

b b b

Neurobiologie de l’Olfaction

Centre de Recherche de Jouy-en-Josas

Domaine de Vilvert • 78352 Jouy-en-Josas Cedex • FRANCE

Olfaction participates in the elaboration of the hedonic value of foods, food choice and the regulation of food intake. Reciprocally, the detection of food odors is influenced by metabolic state and thereby contributes to the initiation and termination of eating behavior. Fasting increases olfactory performances, notably by increasing neuronal activation in the olfactory bulb (OB) (Prud’homme et al, 2009), the first integration site of olfactory signals towards the central nervous system. Within the OB glomeruli, glutamatergic synapses between olfactory sensory neurons and mitral cells are regulated by periglomerular neurons and astrocytes.

Hypothesis

Conclusion Results

Astrocytes are now fully recognized as synaptic partners (Halassa & Haydon 2010) and are thought to generate some kind of “metaplasticity” in the brain (Min et al, 2012) as well as in the OB glomerular region (Roux et al, 2011).

The neuron-astrocyte cross-talk in the glomeruli, albeit poorly known, may be a central player in the metabolic regulation of the olfactory responses^.

Models

Our results show that the deployment of astroglial processes within the OB glomeruli varies according to the metabolic status of the rats and is influenced by peptides involved in food intake regulation, such as PYY 3-36, and/or by changes in glycemia. This morphological plasticity may participate in the adaptation of olfactory sensitivity to food intake, by regulating the first step of odor signal integration in the CNS.

We are now seeking for the functional consequences of this astroglial plasticity on the olfactory signal and the underlying mechanisms.

Overnight (17h) food deprivation results in an increase in the astroglial deployment within glomeruli in all OB regions.

This increased deployment is also observed after 24h fasting in the medial and ventral OB regions but not after 48h fasting.

Fed rats 17h of food deprivation 24h of food deprivation 48h of food deprivation

Mitral cells

Olfactory sensory neurons

To test the hypothesis that glomerular astrocytes are involved in the metabolic sensing of the olfactory system, we have compared the expansion of the astroglial processes (Immunohistochemical – Quantification of the GFAP area) within the glomeruli in:

• fed or fasted rats

• Fed and fasted rats injected with differents anorexigenic and orexigenic peptides

GFAP/Hoechst labelling

Astroglial deployment within the OB glomeruli

Quantification of GFAP labelling area/glomerulus : 4 sections/OB region/rat (≈ 200 glomeruli/region/rat)

n= 7 rats/condition

OB Dorsal region

Medial region Ventral region

DORSAL

VENTRAL 640 µm 1840 µm 2620 µm

Context

Granule cell layer and internal plexiform layer

Mitral cell layer

External plexiform layer

Glomerular layer

Olfactory nerve layer

GLOMERULUS

Astrocytes

Objectives

17h fasting Fed

5 week old Wistar rats

Fasting

• ↗ Neuronal activation (OB) (Prud’homme et al, 2009)

• ↗ Olfactory sensitivity (Aimé P. et al, 2007)

Modification of the astroglial coverage within the olfactory

glomeruli

?

Fed rats and fasted rats (17h, 24h or 48h of food deprivation):

Anorexigenic peptide PYY 3-36

Orexigenic peptide Ghrelin

Anorexigenic peptide Leptin

Glucose Physiological

serum

FED RATS

Physiological serum

FASTED RATS

olfactory bulb level

% of GFAP labelling area/glomeruli area

Dorsal Middle Ventral

0 10 20 30 40 50 60 70 80 90 100

n= 6 or 8 rats/condition/region Permutation test (Software R)

* p0.05; **p0.01

**

** *

Fasted rats (17h)+i.p. Phy.S.

Fasted rats (17h)+i.p. Glucose

ASTROGLIAL DEPLOYMENT

0 10 20 30 40 50 60 70 80 90

100 n= 5 or 6 rats/condition/region

Permutation test (Software R)

* p0.05

Fed rats + i.p. Phy.S.

Fed rats + i.p. Ghrelin

0 10 20 30 40 50 60 70 80 90

100 n= 6 rats/condition/region

* p0.05; **p0.01

Fasting rats (17h)+i.p. S.Phy.

Fasting rats(17h)+i.p. PYY3-36

** * *

0 10 20 30 40 50 60 70 80 90

100 n= 5 or 6 rats/condition/region

* p0.05

Fed rats + i.p. Phy.S.

Fed rats + i.p. Leptin

i.p. administration of GHRELIN (40µg/kg) in fed rats

i.p. administration of PYY 3-36 (100µg/kg) in fasted rats (17h)

i.p. administration of LEPTIN (25µg/kg) in fasted rats (17h)

i.p. administration of GLUCOSE (2g/kg) in fasted rats (17h)

FOOD INTAKE

% of Food intake (values relative to food intake of rats injected with physiological serum)

0 10 20 30 40 50 60 70 80 90 100 110 120 130 140 150

n=4 cages/condition

* p0.05 p*0.05

FOOD INTAKE

0 1000 2000 3000 4000 5000 6000 7000 8000

p<0.001***

100

n= 11 or 13 cages/condition Permutation test (Software R)

*** p0.001

FOOD INTAKE

0 10 20 30 40 50 60 70 80 90 100 110 120 130 140 150

p***0.001

n=12 cages/condition

* p0.05

GLYCEMIA

Glycemia (mg/dL)

60 80 100 120 140 160

FED rats FASTED rats (17h of food deprivation) GLYCEMIA Fed rats 1h after i.p. Phy.S.

GLYCEMIA Fasted rats 1h after i.p. Phy.S.

GLYCEMIA Fasted rats 1h after i.p. GLUCOSE

**

GFAP/Hoechst labelling

PYY 3-36 reverses the astroglial deployment induced by fasting

Ghrelin doesn’t mimic the effect of fasting on astroglial deployment

Glucose reverses the astroglial deployment induced by fasting

Leptin doesn’t mimic the effect of satiety on astroglial deployment

Perspectives

Fasted rats (17h) Fed rats

Neuronal activation (OB) PYY 3-36

Glycemia

% of GFAP labelling area/glomeruli area

Dorsal Medial Ventral

0 10 20 30 40 50 60 70 80 90 100

Fed

17h of food deprivation 24h of food deprivation 48h of food deprivation

n= 7 rats/condition/region

** p0.01, *p0.05

** * **

Olfactory Bulb region

Astroglial deployement OB

Hoechst labelling

RAT HEMI HEAD