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Research ArticleConfirmation, Integrative Systems

Postmeal Optogenetic Inhibition of Dorsal or Ventral Hippocampal Pyramidal Neurons Increases Future Intake

Reilly Hannapel, Janavi Ramesh, Amy Ross, Ryan T. LaLumiere, Aaron G. Roseberry and Marise B. Parent
eNeuro 14 January 2019, 6 (1) ENEURO.0457-18.2018; https://doi.org/10.1523/ENEURO.0457-18.2018
Reilly Hannapel
1Neuroscience Institute, Georgia State University, Atlanta, GA 30303
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Janavi Ramesh
1Neuroscience Institute, Georgia State University, Atlanta, GA 30303
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Amy Ross
1Neuroscience Institute, Georgia State University, Atlanta, GA 30303
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Ryan T. LaLumiere
4Department of Psychological and Brain Sciences and Iowa Neuroscience Institute, University of Iowa, Iowa City, IA 52242
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Aaron G. Roseberry
1Neuroscience Institute, Georgia State University, Atlanta, GA 30303
2Department of Biology, Georgia State University, Atlanta, GA 30303
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Marise B. Parent
1Neuroscience Institute, Georgia State University, Atlanta, GA 30303
3Department of Psychology, Georgia State University, Atlanta, GA 30303
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    Figure 1.

    Optical stimulation of eArchT3.0 produced steady, temporally-specific, and reversible inhibition of dHC and vHC glutamatergic neurons. A, Sample light-induced inhibition of a vHC-eArchT3.0-expressing neuron for 2 s (green line). Scale bar: 20 mV/0.5 s. B, Light application for 2 s significantly decreased the mean (±SEM) firing rate of dHC and vHC-eArchT3.0-expressing neurons during that 2-s period (n = 11; dHC and vHC combined). C, Sample light-induced inhibition of a vHC-eArchT3.0-expressing neuron for 10 min (green line); (Ci) at baseline, (Cii) before, (Ciii) during, and (Civ) after light. Scale bars: 20 mV/1 min (i–iv: 20 mV/1 s). D, Light application for 10 min significantly decreased mean (±SEM) AP fidelity (n = 4; dHC and vHC combined); ***p < 0.0005 versus Pre (i.e., before light application) and Post (i.e., after light application was terminated).

  • Figure 2.
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    Figure 2.

    Depiction of virus expression and ferrule placement. A, Depiction of ferrule location in dHC and vHC of the same rat. B, Representative image of robust eArchT3.0-eYFP expression and ferrule location in dHC and in (C) vHC. D, Schematic depiction of virus expression and ferrule placement relative to bregma in dHC and in (E) vHC. Atlas plates adapted from Paxinos and Watson (2007).

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    Figure 3.

    Postmeal inhibition of dHC or vHC glutamatergic neurons promoted sucrose meal initiation and increased future sucrose intake. A, Timeline showing when optical inhibition of dHC or vHC glutamatergic neurons was given for 10 min relative to the first sucrose meal on different experimental days. All of the rats were given all of the seven treatment conditions (i.e., within-subject design) in a counterbalanced order. B, Optical inhibition given before, during, or after the first sucrose meal did not affect the size of the first meal. Optical inhibition given during or after the first meal (C) decreased the ppIMI and (D) satiety ratio, whereas only inhibition after the first meal (E) increased the amount eaten during the second meal, even though the neurons were no longer inactivated during intake of that second meal (n = 20; within-subject). Inhibition of vHC glutamatergic neurons given before intake of the first meal decreased the ppIMI and satiety ratio, but did not affect the other measures. Illumination given before, during, or after the first sucrose chow meal did not affect (F) the size of the first meal (G) the ppIMI, (H) the satiety ratio, or (I) the size of the second meal in the no opsin control rats (n = 11; within-subject). The central line depicts the median and the whiskers represent the maximum-minimum data points for each condition; **p < 0.005; ***p < 0.0005; ****p < 0.0001 versus none.

  • Figure 4.
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    Figure 4.

    Postmeal inhibition of dHC or vHC glutamatergic neurons also promoted chow meal initiation and increased future chow intake. A, Timeline showing when optical inhibition of dHC or vHC glutamatergic neurons was given for 10 min relative to the first chow meal on different experimental days. All of the rats were given all of the seven treatment conditions (i.e., within-subject design) in a counterbalanced order. Optical activation of eArchT3.0 given before intake of the first meal did not affect (B) the amount eaten during the first meal or any of the other measures, whereas optical inhibition given during or after the first meal (C) decreased the ppIMI and (D) satiety ratio. Only inhibition given after the first meal (E) increased the amount eaten during the second meal, even though the neurons were no longer inactivated during intake of that meal (n = 18; within-subject). Illumination given before, during, or after the first chow meal did not affect (F) the size of the first meal (G) the ppIMI, (H) the satiety ratio, or (I) the size of the second meal in the no opsin control rats (n = 8; within-subject). The central line depicts the median and the whiskers represent the maximum-minimum data points for each condition; *p < 0.05; **p < 0.005; ***p < 0.0005; ****p < 0.0001 versus none.

  • Figure 5.
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    Figure 5.

    Postmeal inhibition of dHC or vHC glutamatergic neurons promoted future intake of the noncaloric sweetener saccharin. A, Timeline showing that optical inhibition of dHC or vHC glutamatergic neurons was given for 10 min after intake of the first saccharin meal. All of the rats (n = 13) were given all three treatment conditions (i.e., none and after in dHC or vHC; within-subject design) in a counterbalanced order. Inhibition given after the first saccharin meal (B) did not affect the amount consumed during the preinhibition meal but did (C) decrease the ppIMI and (D) satiety ratio and (E) increase the amount consumed during the second saccharin meal, even though these neurons were not inhibited during intake of that second meal. The central line depicts the median and the whiskers represent the maximum-minimum data points for each condition; *p < 0.05; **p < 0.005 versus none.

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Postmeal Optogenetic Inhibition of Dorsal or Ventral Hippocampal Pyramidal Neurons Increases Future Intake
Reilly Hannapel, Janavi Ramesh, Amy Ross, Ryan T. LaLumiere, Aaron G. Roseberry, Marise B. Parent
eNeuro 14 January 2019, 6 (1) ENEURO.0457-18.2018; DOI: 10.1523/ENEURO.0457-18.2018

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Postmeal Optogenetic Inhibition of Dorsal or Ventral Hippocampal Pyramidal Neurons Increases Future Intake
Reilly Hannapel, Janavi Ramesh, Amy Ross, Ryan T. LaLumiere, Aaron G. Roseberry, Marise B. Parent
eNeuro 14 January 2019, 6 (1) ENEURO.0457-18.2018; DOI: 10.1523/ENEURO.0457-18.2018
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Keywords

  • feeding
  • hippocampus
  • memory
  • postprandial
  • saccharin
  • sucrose

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