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Articles, Behavioral/Cognitive

Binge-Like Consumption of a Palatable Food Accelerates Habitual Control of Behavior and Is Dependent on Activation of the Dorsolateral Striatum

Teri M. Furlong, Hirosha K. Jayaweera, Bernard W. Balleine and Laura H. Corbit
Journal of Neuroscience 2 April 2014, 34 (14) 5012-5022; https://doi.org/10.1523/JNEUROSCI.3707-13.2014
Teri M. Furlong
1Brain and Mind Research Institute and
2School of Psychology, The University of Sydney, Sydney, New South Wales 2006, Australia
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Hirosha K. Jayaweera
2School of Psychology, The University of Sydney, Sydney, New South Wales 2006, Australia
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Bernard W. Balleine
1Brain and Mind Research Institute and
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Laura H. Corbit
2School of Psychology, The University of Sydney, Sydney, New South Wales 2006, Australia
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    Figure 1.

    Caloric intake and weight gain across weeks of access to SCM. A, Mean (±SE) kilocalories (kcal) consumed in the 2 h access period across weeks for rats in the control, continuous-access, or restricted-access groups. Caloric intake was higher for rats with restricted access to the SCM compared with either those with continuous access to SCM or to control rats receiving only chow. Rats with continuous access to SCM consumed more kilocalories in the access period than controls. B, Mean weight gain (in grams; ±SE) per week across weeks of access to SCM. The continuous-access group gained more weight than controls or the restricted-access group, which did not differ from each other. N = 12 per group.

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    Figure 2.

    Sensitivity to outcome devaluation following long-term exposure to a palatable food. A, Mean (±SE) lever presses across days of instrumental training. Responding increased across days and there were no group differences in responding. B, Mean lever presses in a 5 min extinction test following prefeeding of the earned (devalued condition) or an alternative outcome (nondevalued condition). Control animals selectively decreased responding following the devalued condition compared with the nondevalued condition. Rats in the continuous-access group showed a numerically reduced but significant effect of devaluation. Rats in the restricted-access group responded similarly regardless of devaluation condition, indicating loss of sensitivity to changes in outcome value. Asterisk indicates p < 0.05. N = 12 per group.

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    Figure 3.

    Representative c-Fos IR in the DS and associated cortical regions. A, Schematic representation of the cortical and striatal regions where cell counts were performed (adapted from Paxinos and Watson, 2005). B–G, Representative c-Fos IR in the DLS (B–D) and DMS (E–G) for rats in the control, continuous-access, and restricted-access groups, respectively. It can be seen that in the DLS rats in the restricted group had higher c-Fos IR than rats in the other two groups, while no such differences were seen in the DMS. The results are quantified in Figure 4.

  • Figure 4.
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    Figure 4.

    Quantification of c-Fos IR in the DLS and DMS following devaluation testing. A, Mean total c-Fos IR (±SE) in the DLS for the control, continuous-access, and restricted-access groups. There was greater c-Fos IR in the restricted-access group compared with either the control or continuous-access groups, which did not differ from each other. B, Total c-Fos IR in the DMS for the control, continuous-access, and restricted-access groups. There were no group differences in c-Fos IR in the DMS. Asterisk indicates significant difference between groups (Bonferroni). N = 10, 12, and 12 for the control, continuous-access, and restricted-access groups, respectively.

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    Figure 5.

    Mean c-Fos IR in cortical regions following devaluation testing. A, Mean total c-Fos IR (±SE) in the infralimbic cortex for the control, continuous-access, and restricted-access groups. There was greater c-Fos IR in the restricted-access group compared with the control group but not the continuous-access group. B, Total c-Fos IR in the prelimbic cortex. There were no group differences in c-Fos IR in the prelimbic cortex. C, Total c-Fos IR in the cingulate and motor cortex. There was greater c-Fos IR in the restricted-access group compared with the control but not the continuous-access group. D, Total c-Fos IR in the somatosensory cortex. There was greater c-Fos IR in the restricted-access group compared with the control but not the continuous-access group. Asterisk indicates significant difference between groups (Bonferroni). N = 8, 10, and 10 for the control, continuous-access, and restricted-access groups, respectively.

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    Figure 6.

    c-Fos IR in ENK-positive and ENK-negative cells in the DLS. A, Representative c-Fos-IR (black arrow), ENK-IR (red arrow), and double-labeled (white arrow) cells. B, Total c-Fos IR in the DLS for the control, continuous-access, and restricted-access groups. There was greater c-Fos IR in the restricted-access group compared with the control but not the continuous-access group. C, Total c-Fos IR in ENK-negative cells also showed effects of group with greater activation in the restricted-access group compared with the control group, but not the continuous-access group. D, Total c-Fos IR in ENK-positive cells also showed effects of group with greater activation in the restricted compared with the control group. Thus, the pattern of activation based on group was similar in the ENK-positive and ENK-negative cells, but overall activation was greater in the ENK-negative population. Asterisk indicates significant difference between groups (Bonferroni). N = 10, 12, and 12 for the control, continuous-access, and restricted-access groups, respectively.

  • Figure 7.
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    Figure 7.

    Prefeeding and instrumental training data and cannulae placements for rats in Experiment 2. A, Mean (±SE) kilocalories (kcal) consumed in the 2 h access period across weeks for rats in the control or restricted-access groups. Caloric intake was higher for rats with restricted access to the SCM compared with control rats receiving only chow. B, Mean weight gain (in grams; ±SE) per week across weeks of access to SCM. There were no group differences in weight gain. C, Mean (±SE) lever presses across days of instrumental training. Responding increased across days and there were no group differences in responding. D, Schematic representation of cannulae placements in the DLS for the control group (black circles) and restricted SCM group (white circles) for animals included in the analysis of Experiment 2 (templates adapted from Paxinos and Watson, 2005). Numbers indicate the distance from bregma in anterior–posterior plane. N = 10 and 8 for the control and restricted-access groups, respectively.

  • Figure 8.
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    Figure 8.

    Sensitivity to outcome devaluation following restricted access to a palatable food and effects of AMPA-receptor and D1-receptor antagonism in the DLS. A, C, Mean lever presses in a 5 min extinction test following prefeeding of the earned (devalued) or an alternative outcome (nondevalued) following infusions of either saline or CNQX. A, Control animals selectively decreased responding following devaluation and performance was unaffected by CNQX. C, Rats in the restricted-access group responded similarly regardless of devaluation condition, indicating loss of sensitivity to changes in outcome value following saline infusion. Infusion of CNQX restored sensitivity to devaluation in this group. Asterisk indicates p < 0.05. B, D, Consumption (in grams) of the same (devalued) or different (nondevalued) food consumed during the specific-satiety treatment for control (B) and SCM (D) groups. Both groups showed consumption that was sensitive to devaluation by specific satiety and ate less when given the same compared with a different food. E, F, Sensitivity to outcome devaluation following D1-receptor antagonism. Both groups showed similar sensitivity to devaluation following infusions of SCH-23390 measured in either lever-press performance (E) or consumption (F). N = 10 and 8 for the control and restricted-access groups, respectively.

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The Journal of Neuroscience: 34 (14)
Journal of Neuroscience
Vol. 34, Issue 14
2 Apr 2014
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Binge-Like Consumption of a Palatable Food Accelerates Habitual Control of Behavior and Is Dependent on Activation of the Dorsolateral Striatum
Teri M. Furlong, Hirosha K. Jayaweera, Bernard W. Balleine, Laura H. Corbit
Journal of Neuroscience 2 April 2014, 34 (14) 5012-5022; DOI: 10.1523/JNEUROSCI.3707-13.2014

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Binge-Like Consumption of a Palatable Food Accelerates Habitual Control of Behavior and Is Dependent on Activation of the Dorsolateral Striatum
Teri M. Furlong, Hirosha K. Jayaweera, Bernard W. Balleine, Laura H. Corbit
Journal of Neuroscience 2 April 2014, 34 (14) 5012-5022; DOI: 10.1523/JNEUROSCI.3707-13.2014
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Keywords

  • diet
  • dorsal striatum
  • goal-directed learning
  • habit learning
  • obesity
  • outcome devaluation

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