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Research ArticleResearch Article: New Research, Disorders of the Nervous System

Maternal Exposure to the Cannabinoid Agonist WIN 55,12,2 during Lactation Induces Lasting Behavioral and Synaptic Alterations in the Rat Adult Offspring of Both Sexes

Andrew F. Scheyer, Milene Borsoi, Anne-Laure Pelissier-Alicot and Olivier J.J. Manzoni
eNeuro 31 August 2020, 7 (5) ENEURO.0144-20.2020; https://doi.org/10.1523/ENEURO.0144-20.2020
Andrew F. Scheyer
1Institut de Neurobiologie de la Méditerranée, Institut National de la Santé et de la Recherche Médicale Unité 1249, Marseille, France
2Aix-Marseille University, France, 13273
3Cannalab Cannabinoids Neuroscience Research International Associated Laboratory, Institut National de la Santé et de la Recherche Médicale-Aix-Marseille University/Indiana University, 13273
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Milene Borsoi
1Institut de Neurobiologie de la Méditerranée, Institut National de la Santé et de la Recherche Médicale Unité 1249, Marseille, France
2Aix-Marseille University, France, 13273
3Cannalab Cannabinoids Neuroscience Research International Associated Laboratory, Institut National de la Santé et de la Recherche Médicale-Aix-Marseille University/Indiana University, 13273
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Anne-Laure Pelissier-Alicot
1Institut de Neurobiologie de la Méditerranée, Institut National de la Santé et de la Recherche Médicale Unité 1249, Marseille, France
2Aix-Marseille University, France, 13273
3Cannalab Cannabinoids Neuroscience Research International Associated Laboratory, Institut National de la Santé et de la Recherche Médicale-Aix-Marseille University/Indiana University, 13273
4Service de Psychiatrie, Assistance Public Hopitaux de Marseille, Centre Hospitalier Universitaire Conception, Marseille 13005, France
5Service de Médecine Légale, APHM, CHU Timone Adultes, Marseille 13005, France
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Olivier J.J. Manzoni
1Institut de Neurobiologie de la Méditerranée, Institut National de la Santé et de la Recherche Médicale Unité 1249, Marseille, France
2Aix-Marseille University, France, 13273
3Cannalab Cannabinoids Neuroscience Research International Associated Laboratory, Institut National de la Santé et de la Recherche Médicale-Aix-Marseille University/Indiana University, 13273
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  • Figure 1.
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    Figure 1.

    Perinatal WIN alters social approach, but not social memory behavior, nor behavior in the open field environment. A, Adult offspring of WIN-treated dams exhibit significantly higher social preference than those of sham-treated dams (two-tailed t test, p = 0.0001; N = 23, 19, respectively). B, Time spent exploring a novel rat is significantly higher than time spent exploring a novel object for both sham-exposed and WIN-exposed rats (one-way ANOVA, F(3,86) = 14.49; Tukey’s post hoc analysis, p < 0.0001 for both groups; N = 23, 19, respectively). C, D, In the subsequent social memory test, the adult offspring of both sham-treated and WIN-treated dams exhibited significantly higher preference for a novel, as compared with familiar, rats. C, The social memory index does not differ between the two groups (two-tailed t test, p = 0.557). D, Time spent exploring a novel rat is significantly higher than time spent exploring a familiar rat for both sham-exposed and WIN-exposed rats (one-way ANOVA, F(3,86) = 2.137; Tukey’s post hoc analysis, p < 0.0001 for both groups). E–G, Behavior in the open field environment does not differ between the offspring of sham-treated and WIN-treated dams (N = 39, 31, respectively). Time spent in the left of the arena, total distance covered, and the number of rearing events is not significantly different between groups (two-tailed t tests, p = 0.1817, p = 0.5991, and p = 0.9783, respectively); *p < 0.05.

  • Figure 2.
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    Figure 2.

    Perinatal WIN exposure induces a selective deficit in LTD in the PFC of adult offspring. A, A 10-min, 10-Hz field stimulation of layer 2/3 cells in the PFC of the adult offspring of sham-treated dams (N = 14) elicited a robust eCB-LTD at deep layer synapses. However, this same protocol failed to induce eCB-LTD in the adult offspring of dams treat with WIN (N = 14). B, fEPSP magnitude at baseline (−10−0 min) and LTD (35–40 min post-tetanus) values corresponding to the normalized values in A (two-way RM ANOVA, F(1,24) = 16.58, p = 0.0004; Sidak’s multiple comparisons test, p = 0.0332 and p = 0.9412, respectively). C, LTD mediated by mGlu2/3 receptors (mGluR-LTD) is not altered in WIN-exposed offspring. mGluR-LTD, induced via a 10-min application of LY379268 (LY; 30 nm), produced a significant depression at deep layer synapses of the PFC in the adult offspring of both sham-treated and WIN-treated dams (N = 12, 12, respectively). D, fEPSP magnitude at baseline (−10−0 min) and LTD (30−40 min postdrug) values corresponding to the normalized values in C. No differences were found between groups comparing the 10-min baseline period and the last 10 min of recording, however both groups exhibited a significant difference of fEPSP magnitude at baseline (i.e., −10−0 min) as compared with 30−40 min postdrug (two-way RM ANOVA, F(1,11) = 96.69, p < 0.0001; Sidak’s multiple comparisons test, p < 0.0001 for both groups). E, A TBS protocol (five pulses at 100 hz, repeated four times) at layer 2/3 cells in the PFC of the adult offspring of both sham-treated and WIN-treated dams elicited a robust LTP at deep layer synapses (N = 13, 15, respectively). F, fEPSP magnitude at baseline (−10−0 min) and LTP (30−40 min post-TBS) values corresponding to the normalized values in E. Both groups exhibited significant differences between the fEPSP magnitude at 30−40 min as compared with −10−0 min (two-way RM ANOVA, F(1,25) = 1.737; Sidak’s multiple comparisons test, p < 0.0001 for both groups); *p < 0.05.

  • Figure 3.
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    Figure 3.

    Perinatal WIN exposure does not alter properties of intrinsic excitability of deep layer pyramidal neurons in the PFC of adult offspring. A, Current injection steps of 50 pA from –400 to 150 pA revealed no differences in the I-V relationship in pyramidal neurons of the PFC between the adult offspring of sham-treated and WIN-treated dams (N = 12, 13, respectively). B, Action potentials elicited by progressive current injections from 0 to 600 pA revealed no difference in the number of spikes elicited in pyramidal neurons of the PFC in slices obtained from the adult offspring of WIN-injected dams as compared with those from sham-treated dams (N = 13, 12, respectively; two-way RM ANOVA, F(20,460) = 1.112, p = 0.3328). C, Progressive current injections in 10-pA steps from 0 to 200 pA revealed that the minimum current injection required to elicit an action potential (i.e., rheobase) did not differ in deep layer pyramidal neurons of PFC slices obtained from the adult offspring of WIN-treated, as compared with sham-treated, dams (N = 13, 12, respectively; two-tailed t test, p = 0.1896). D, Similarly, no difference was found in the resting membrane potential of deep layer pyramidal cells in PFC slices obtained from the adult offspring of WIN-treated dams, as compared with those obtained from sham-treated dams (N = 13, 12, respectively; two-tailed t test, p = 0.1123); *p < 0.05.

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    Figure 4.

    Perinatal WIN exposure abolishes LTD in the NAc of adult offspring and alters the resting membrane potential of NAc MSNs. A, A 10-min, 10-Hz local field stimulation of the NAc of the adult offspring of sham-treated dams (N = 10) elicited a robust eCB-LTD. However, this same protocol failed to induce eCB-LTD in the adult offspring of dams treat with WIN (N = 12). B, fEPSP magnitude at baseline (−10−0 min) and LTD (35–40 min post-tetanus) values corresponding to the normalized values in A (two-way RM ANOVA, F(1,20) = 20.49, p = 0.0002; Sidak’s multiple comparisons test, p = 0.0002 and p = 0.3087 for sham and WIN, respectively). C, Current injection steps of 50 pA from –400 to 150 pA revealed no differences in the I-V relationship in MSNs of the NAc between the adult offspring of sham-treated and WIN-treated dams (N = 14, 14, respectively). D, Action potentials elicited by progressive current injections from 0 to 600 pA revealed no difference in the number of spikes elicited in pyramidal neurons of the PFC in slices obtained from the adult offspring of WIN-injected dams as compared with those from sham-treated dams (N = 14, 14, respectively; two-way RM ANOVA, F(20,250) = 0.6092, p = 0.9071). E, Progressive current injections in 10-pA steps from 0 to 200 pA revealed that the minimum current injection required to elicit an action potential (i.e., rheobase) did not differ in MSNs of NAc slices obtained from the adult offspring of WIN-treated, as compared with sham-treated, dams (N = 14, 14, respectively; two-tailed t test, p = 0.9502). F, However, MSNs in NAc slices obtained from the adult offspring of WIN-treated dams exhibited significantly lower resting membrane potentials than those obtained from sham-exposed offspring (N = 14, 14, respectively; two-tailed t test, p = 0.0003); *p < 0.05.

  • Figure 5.
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    Figure 5.

    Perinatal WIN exposure increases sucrose preference in adult offspring. A, Total quantities of water and 5% sucrose solution (ml) did not differ between the adult offspring of sham-treated or WIN-treated dams during a 20-min sucrose preference test (N = 8, 8, respectively). B, Preference for the 5% sucrose solution over water was significantly higher in WIN- as compared with sham-treated rats (two-tailed t test, p = 0.0091). *p < 0.05.

Tables

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    Table 1

    Social approach and social memory data by sex

    ConditionTest – measure (unit)Valuet test (M vs F)
    Sham maleSocial preference (ratio)0.8647 ± 0.01743 N = 15p = 0.5089
    Sham femaleSocial preference (ratio)0.8375 ± 0.03569 N = 8
    WIN maleSocial preference (ratio)0.9491 ± 0.01282 N = 11p = 0.0255
    WIN femaleSocial preference (ratio)0.8618 ± 0.03219 N = 11
    Sham maleSocial memory (ratio)0.6147 ± 0.03886 N = 15p = 0.0876
    Sham femaleSocial memory (ratio)0.7463 ± 0.05970 N = 8
    WIN maleSocial memory (ratio)0.6282 ± 0.05435 N = 11p > 0.9999
    WIN femaleSocial memory (ratio)0.6282 ± 0.03590 N = 11
    Sham maleSocial preference – time exploring object (s)14.20 ± 1.853 N = 15p = 0.8121
    Sham femaleSocial preference – time exploring object (s)13.61 ± 1.610 N = 8
    WIN maleSocial preference – time exploring object (s)6.586 ± 1.840 N = 11p = 0.0420
    WIN femaleSocial preference – time exploring object (s)16.05 ± 3.822 N = 11
    Sham maleSocial preference – time exploring rat (s)95.38 ± 8.016 N = 15p = 0.3569
    Sham femaleSocial preference – time exploring rat (s)83.02 ± 10.25 N = 8
    WIN maleSocial preference – time exploring rat (s)110.2 ± 9.669 N = 11p = 0.4518
    WIN femaleSocial preference – time exploring rat (s)100.8 ± 7.422 N = 11
    Sham maleSocial memory – time exploring familiar rat (s)29.31 ± 3.733 N = 15p = 0.2200
    Sham femaleSocial memory – time exploring familiar rat (s)20.90 ± 5.375 N = 8
    WIN maleSocial memory – time exploring familiar rat (s)26.17 ± 3.754 N = 11p = 0.3621
    WIN femaleSocial memory – time exploring familiar rat (s)35.52 ± 2.748 N = 11
    Sham maleSocial memory – time exploring novel rat (s)47.06 ± 4.528 N = 15p = 0.1116
    Sham femaleSocial memory – time exploring novel rat (s)58.58 ± 5.159 N = 8
    WIN maleSocial memory – time exploring novel rat (s)49.36 ± 8.196 N = 11p = 0.7014
    WIN femaleSocial memory – time exploring novel rat (s)53.04 ± 4.657 N = 11
    • View popup
    Table 2

    Open field data by sex

    ConditionTest – measure (unit)Valuet test (M vs F)
    Sham maleOpen field – distance (cm)3120 ± 80.10 N = 22p = 0.1490
    Sham femaleOpen field – distance (cm)3348 ± 135.8 N = 17
    WIN maleOpen field – distance (cm)2861 ± 151.9 N = 14p = 0.0070
    WIN femaleOpen field – distance (cm)3396 ± 97.26 N = 17
    Sham maleOpen field – rearing (#)62.23 ± 3.365 N = 22p = 0.2443
    Sham femaleOpen field – rearing (#)68.18 ± 3.735 N = 17
    WIN maleOpen field – rearing (#)56.64 ± 5.840 N = 14p = 0.0333
    WIN femaleOpen field – rearing (#)71.76 ± 3.118 N = 17
    Sham maleOpen field – left (s)54.85 ± 5.348 N = 22p = 0.0839
    Sham femaleOpen field – left (s)42.24 ± 4.674 N = 17
    WIN maleOpen field – left (s)55.87 ± 8.835 N = 14p = 0.0104
    WIN femaleOpen field – left (s)28.92 ± 2.733 N = 17
    • View popup
    Table 3

    PFC LTD data by sex

    ConditionTest – measure (unit)Valuet test (M vs F)
    Sham maleeCB-LTD – normalized fEPSP (35–40 min post-tetanus)80.61 ± 3.408 N = 8p = 0.5478
    Sham femaleeCB-LTD – normalized fEPSP (35–40 min post-tetanus)83.90 ± 4.061 N = 6
    WIN maleeCB-LTD – normalized fEPSP (35–40 min post-tetanus)103.9 ± 8.384 N = 6p = 0.7042
    WIN femaleeCB-LTD – normalized fEPSP (35–40 min post-tetanus)108.8 ± 9.488 N = 7
    Sham malemGlu2/3-LTD – normalized fEPSP (35–40 min postdrug)66.26 ± 4.196 N = 6p = 0.8390
    Sham femalemGlu2/3-LTD – normalized fEPSP (35–40 min postdrug)67.58 ± 4.700 N = 6
    WIN malemGlu2/3-LTD – normalized fEPSP (35–40 min postdrug)67.48 ± 4.156 N = 7p = 0.4467
    WIN femalemGlu2/3-LTD – normalized fEPSP (35–40 min postdrug)72.00 ± 3.900 N = 5
    • View popup
    Table 4

    PFC LTP data by sex

    ConditionTest – measure (unit)Valuet test (M vs F)
    Sham maleTBS-LTP – normalized fEPSP (35–40 min post-tetanus)185.6 ± 26.32 N = 6p = 0.3101
    Sham femaleTBS-LTP – normalized fEPSP (35–40 min post-tetanus)155.4 ± 6.180 N = 7
    WIN maleTBS-LTP – normalized fEPSP (35–40 min post-tetanus)168.0 ± 11.98 N = 9p = 0.3917
    WIN femaleTBS-LTP – normalized fEPSP (35–40 min post-tetanus)152.6 ± 12.58 N = 6
    • View popup
    Table 5

    NAc LTD data by sex

    ConditionTest – measure (unit)Valuet test (M vs F)
    Sham maleTBS-LTP – normalized fEPSP (35–40 min post-tetanus)82.37 ± 6.937 N = 5p = 0.2893
    Sham femaleTBS-LTP – normalized fEPSP (35–40 min post-tetanus)71.51 ± 6.589 N = 5
    WIN maleTBS-LTP – normalized fEPSP (35–40 min post-tetanus)110.9 ± 6.257 N = 5p = 0.0714
    WIN femaleTBS-LTP – normalized fEPSP (35–40 min post-tetanus)95.53 ± 3.039 N = 4
    • View popup
    Table 6

    PFC intrinsic properties data by sex

    ConditionTest – measure (unit)Valuet test (M vs F)
    Sham maleResting membrane potential (mV)–67.95 ± 1.408 N = 6p = 0.3580
    Sham femaleResting membrane potential (mV)–66.11 ± 0.9624 N = 6
    WIN maleResting membrane potential (mV)–64.12 ± 1.103 N = 7p = 0.2000
    WIN femaleResting membrane potential (mV)–66.22 ± 1.077 N = 6
    Sham maleRheobase (pA)86,67 ± 18.06 N = 6p = 0.7003
    Sham femaleRheobase (pA)76.67 ± 17.64 N = 6
    WIN maleRheobase (pA)66.19 ± 16.34 N = 7p = 0.5487
    WIN femaleRheobase (pA)55.00 ± 7.303 N = 6
    • View popup
    Table 7

    NAc intrinsic properties data by sex

    ConditionTest – measure (unit)Valuet test (M vs F)
    Sham maleResting membrane potential (mV)–83.17 ± 1.463 N = 5p = 0.0491
    Sham femaleResting membrane potential (mV)–78.26 ± 1.684 N = 9
    WIN maleResting membrane potential (mV)–93.95 ± 3.909 N = 8p = 0.5281
    WIN femaleResting membrane potential (mV)–1004 ± 8.945 N = 6
    Sham maleRheobase (pA)199.2 ± 36.64 N = 5p = 0.5827
    Sham femaleRheobase (pA)176.7 ± 10.93 N = 9
    WIN maleRheobase (pA)190.6 ± 20.19 N = 8p = 0.7663
    WIN femaleRheobase (pA)180.0 ± 28.28 N = 6
    • View popup
    Table 8

    Sucrose preference data by sex

    ConditionTest – measure (unit)Valuet test (M vs F)
    Sham maleWater consumed (ml)1.425 ± 0.1181 N = 4p = 0.0045
    Sham femaleWater consumed (ml)3.575 ± 0.3326 N = 4
    WIN maleWater consumed (ml)1.075 ± 0.2287 N = 4p = 0.6953
    WIN femaleWater consumed (ml)1.175 ± 0.04787 N = 4
    Sham maleSucrose consumed (ml)3.550 ± 1.533 N = 4p = 0.1069
    Sham femaleSucrose consumed (ml)7.000 ± 0.7153 N = 4
    WIN maleSucrose consumed (ml)8.800 ± 1.564 N = 4p = 0.5118
    WIN femaleSucrose consumed (ml)6.850 ± 2.291 N = 4
    Sham maleSucrose preference (ratio)2.739 ± 1.376 N = 4p = 0.6530
    Sham femaleSucrose preference (ratio)2.039 ± 0.3597 N = 4
    WIN maleSucrose preference (ratio)8.674 ± 1.744 N = 4p = 0.3462
    WIN femaleSucrose preference (ratio)5.885 ± 2.089 N = 4
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Maternal Exposure to the Cannabinoid Agonist WIN 55,12,2 during Lactation Induces Lasting Behavioral and Synaptic Alterations in the Rat Adult Offspring of Both Sexes
Andrew F. Scheyer, Milene Borsoi, Anne-Laure Pelissier-Alicot, Olivier J.J. Manzoni
eNeuro 31 August 2020, 7 (5) ENEURO.0144-20.2020; DOI: 10.1523/ENEURO.0144-20.2020

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Maternal Exposure to the Cannabinoid Agonist WIN 55,12,2 during Lactation Induces Lasting Behavioral and Synaptic Alterations in the Rat Adult Offspring of Both Sexes
Andrew F. Scheyer, Milene Borsoi, Anne-Laure Pelissier-Alicot, Olivier J.J. Manzoni
eNeuro 31 August 2020, 7 (5) ENEURO.0144-20.2020; DOI: 10.1523/ENEURO.0144-20.2020
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Keywords

  • Accumbens
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