Selective activation of cholinergic interneurons enhances accumbal phasic dopamine release: setting the tone for reward processing.
paper
Cited
Public
- Authors
- Cachope, Roger; Mateo, Yolanda; Mathur, Brian N; Irving, James; Wang, Hui-Ling; Morales, Marisela; Lovinger, David M; Cheer, Joseph F
- Year
- 2012
- Journal
- Cell reports
- PMID
- 22840394
- DOI
- 10.1016/j.celrep.2012.05.011
- PMCID
- PMC3408582
Dopamine plays a critical role in motor control, addiction, and reward-seeking behaviors, and its release dynamics have traditionally been linked to changes in midbrain dopamine neuron activity. Here, we report that selective endogenous cholinergic activation achieved via in vitro optogenetic stimulation of nucleus accumbens, a terminal field of dopaminergic neurons, elicits real-time dopamine release. This mechanism occurs via direct actions on dopamine terminals, does not require changes in neuron firing within the midbrain, and is dependent on glutamatergic receptor activity. More importantly, we demonstrate that in vivo selective activation of cholinergic interneurons is sufficient to elicit dopamine release in the nucleus accumbens. Therefore, the control of accumbal extracellular dopamine levels by endogenous cholinergic activity results from a complex convergence of neurotransmitter/neuromodulator systems that may ultimately synergize to drive motivated behavior.
Selective optical stimulation of ChR2-expressing CINs elicits accumbal dopamine releaseA. Top: Trace from a whole-cell recording of a YFP positive neuron (putative CIN). YFP-positive neurons displayed spontaneous, tonic firing at a rate of ~10 Hz. Bottom: Under whole-cell voltage-clamp recording from a YFP-positive neuron, blue light exposure (100 msec, left or 4 msec, middle) induced a ChR2-mediated inward current. Under whole-cell current-clamp recordings of YFP-positive neurons, delivery of a blue light pulse (4 msec, right) induced firing of a single action potential.B. Image of eYFP-positive (green) cell bodies (arrowheads) counterstained for ChAT (red) and processes from the NAc of a ChAT-Cre mouse transfected with a ChR2-eYFP viral vector.C. Scheme of the recording arrangement from coronal NAc striatal slices. DA levels were measured by FSCV through a carbon fiber microelectrode (right) while performing electrical stimulation (left) and/or optical stimulation (blue circle) delivered by an optical fiber in apposition with the tissue.D. Concentration trace (top) and color plot (bottom) for DA release triggered by electrical stimulation of the NAc. Top: Representative trace shows concentration of DA (nM) over time in response to electrical stimulation (indicated by green line). Inset shows characteristic DA voltammogram. Bottom: Corresponding color plot depicts the voltammetric data with time on the X axis, applied scan potential (Eapp) on the Y axis and background-subtracted faradaic current shown on the z-axis in pseudocolor. DA can be identified by an oxidation peak (green) at +0.6V and a smaller reduction peak (yellow) at -0.2V.E. Concentration trace (top) and color plot (bottom) for DA release triggered by optical stimulation of CINs. Top: As in D, representative trace shows concentration of DA (nM) over time in response to optical stimulation (indicated by blue line) Inset shows characteristic DA voltammogram. Bottom: Corresponding color plot of voltammetric data.F. Bar graph represents peak values of accumbal DA release obtained by electrical and optical stimulation.G. Dispersion plot indicating peak values for all the experiments performed under electrical (green circles) and optical stimulation (blue circles).Error bars represent Standard Error of the Mean (SEM).
LLM interpretation
This figure consists of electrophysiological traces (A), a fluorescence microscopy image (B), a schematic of the experimental setup (C), and FSCV data including concentration traces and color plots (D, E). A bar graph (F) and a dispersion plot (G) compare peak dopamine (DA) release triggered by electrical stimulation (green) versus optical stimulation of ChR2-expressing CINs (blue). The data show that both stimulation methods elicit DA release, with electrical stimulation resulting in a higher mean peak concentration than optical stimulation.
Frequency-dependent response of DA release evoked by stimulation of CINsA. Average traces of DA levels evoked by paired pulses of optical stimulation of CINs delivered at 5, 10, 30 and 60 seconds intervals.B. Summary plot of DA peak amplitudes in response to paired pulse ratio stimulation of CINs.C. Top: Summary bar graph showing the average T80 decay values for DA release evoked by 5, 10, 30 Hz and single pulse stimulation. Bottom: Summary graph of peak values of DA release evoked by 5, 10, 30 Hz and single pulse stimulation.D. Average traces of DA levels triggered by different patterns of electrical stimulation, while sustained optical stimulation of CINs was being performedE. Representative traces from whole-cell recordings under current clamp of CIN neurons showing responsiveness to 10Hz optical stimulation.F. As in E., representative trace depicting CIN responsiveness to 30 Hz optical stimulation.Error shadows or bars represent SEM.
LLM interpretation
This figure consists of multiple panels analyzing dopamine (DA) release evoked by stimulation of CINs. Panel A shows average DA level traces at various interpulse intervals, while Panel B is a scatter plot showing a positive correlation between the interpulse interval (1β100 s) and the paired-pulse ratio (PPR). Panel C contains two bar graphs comparing $T_{80}$ decay values and peak DA concentrations across different stimulation frequencies (1P, 30Hz, 10Hz, 5Hz), with statistical significance indicated by asterisks. Panels D, E, and F provide representative DA release traces under different electrical stimulation patterns and whole-cell current clamp recordings of CIN neurons at 10Hz and 30Hz.
Modulation of DA levels evoked by endogenous cholinergic activityA. Concentration-response plot showing the effect of increasing concentrations of the nAChR antagonist mecamylamine on DA peak levels evoked by single pulses of optical stimulation. IC = 0.61 ΞΌM.B. Effect of the Ξ²2 subunit nAChR antagonist DHΞ²E (1 ΞΌM) on DA levels evoked by single pulse (left) and train (right) optical stimulation of CINs.C. Trace of an EPSC from a medium spiny neuron (MSN) under voltage clamp, elicited by single pulse optical stimulation of CINs. Effect of NBQX (5 ΞΌM) on the MSN EPSC.D. Effect of the application of the AMPA receptor antagonist NBQX (5 ΞΌM) on DA levels evoked by single pulse optical stimulation of CINs.E. Summary bar graph showing the effect of the mAChR antagonist scopolamine (1 ΞΌM) on DA peak levels evoked by single pulse, 5Hz and 10Hz optical stimulation of CINs, compared to pretreatment.F. Representative traces of DA concentration transients triggered by single pulse, 5Hz and 10Hz optical stimulation of CINs in the presence of scopolamine, compared to pretreatment.Error shadows or bars represent SEM.
LLM interpretation
This figure consists of multiple panels analyzing dopamine (DA) release evoked by cholinergic interneuron (CIN) stimulation. Panel A shows a concentration-response curve where mecamylamine reduces DA release (IC = 0.61 ΞΌM), while panels B and D use line plots to show that DH$\beta$E and NBQX reduce DA transients. Panel C displays a voltage clamp trace and bar graph showing that NBQX significantly reduces EPSC amplitude (***p < 0.001). Panels E and F utilize a summary bar graph and representative traces to show that scopolamine increases DA peak levels during 5Hz and 10Hz stimulation compared to baseline (*p < 0.05).
In vivo selective stimulation of CINs evokes accumbal DA releaseA. Scheme depicting implantation of the optrode (optical fiber/carbon fiber arrangement) used to optically stimulate and record FSCV from a contiguous area in the NAc in vivo.B. Concentration trace for DA release triggered by a 7 seconds-long (20 Hz, 150 pulses, 10 mW) optical stimulation of the NAc. Representative trace shows concentration of DA (nM) over time in response to optical stimulation (indicated by blue line). Inset shows characteristic DA voltammogram.C. Corresponding color plot depicts the voltammetric data with time on the X axis, applied scan potential (Eapp) on the Y axis and background-subtracted faradaic current shown on the z-axis in pseudocolor.
LLM interpretation
This figure consists of a schematic and two data plots illustrating dopamine (DA) release in the nucleus accumbens (NAc). Panel A is a diagram showing the implantation of an optrode into the NAc of a brain. Panel B shows a concentration trace of DA ($\mu$M) over time, where a blue bar indicates a period of optical stimulation that triggers a peak in DA concentration, accompanied by a characteristic DA voltammogram inset. Panel C is a color plot (heat map) showing faradaic current (nA) as a function of time (X-axis) and applied scan potential (Y-axis).
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