Dopamine activity encodes the changing valence of the same stimulus in conditioned taste aversion paradigms

  1. Maxine K Loh
  2. Samantha J Hurh
  3. Paula Bazzino
  4. Rachel M Donka
  5. Alexandra T Keinath
  6. Jamie D Roitman
  7. Mitchell F Roitman  Is a corresponding author
  1. Division of Endocrinology, Diabetes and Metabolism, Department of Medicine, University of Illinois at Chicago, United States
  2. Department of Psychology, University of Illinois at Chicago, United States
  3. Graduate Program in Neuroscience, University of Illinois at Chicago, United States
13 figures, 1 table and 1 additional file

Figures

Figure 1 with 1 supplement
In vivo fiber photometry in the mesolimbic dopamine system captures phasic dopamine responses to primary taste stimuli.

(A) Representative images of GRABDA_2h and Cre-dependent GCamp6f expression in the NAc and VTA, respectively. Top row: Dopamine release recordings from the lateral subregion of the NAc shell are …

Figure 1—source data 1

Quantified dopamine responses to intraoral sucrose and quinine.

https://cdn.elifesciences.org/articles/103260/elife-103260-fig1-data1-v1.xlsx
Figure 1—figure supplement 1
NAc lateral shell recording placements from primary taste experiment.

The fiber optic implant locations in the NAc lateral shell were verified via post-experimental histological reconstruction. Measurement values denote anterior–posterior coronal plane in relation to …

Aversive taste stimuli are linked to increased movement of nose and forepaws.

(A) Representative image of nose, forepaws, tail base, and chamber legs tracking of a rat in a cylindrical chamber from a below chamber perspective. Positional coordinates of selected features were …

Figure 2—source data 1

Normalized nose and forepaw movements to intraoral sucrose and quinine and associated dopamine responses.

https://cdn.elifesciences.org/articles/103260/elife-103260-fig2-data1-v1.xlsx
Figure 3 with 1 supplement
Pairing of lithium chloride (LiCl)-induced malaise to sucrose suppresses phasic dopamine responses to intraoral sucrose delivery.

(A) Schematic of Single-pairing conditioned taste aversion (CTA) timeline. Subjects were first habituated to 30 brief intraoral infusions (200 µl/trial) of water at varying intertrial intervals …

Figure 3—source data 1

Quantified NAc dopamine and VTADA activity responses to intraoral sucrose before and after CTA formation.

https://cdn.elifesciences.org/articles/103260/elife-103260-fig3-data1-v1.xlsx
Figure 3—figure supplement 1
NAc lateral shell and VTA recording placements from Single-pairing conditioned taste aversion (CTA) experiment.

The fiber optic implant locations in the NAc lateral shell and VTA were verified via post-experimental histological reconstruction. Measurement values denote anterior–posterior coronal plane in …

Suppressed dopamine responses correlate with enhanced behavioral reactivity to intraoral sucrose delivery after conditioned taste aversion (CTA) formation.

(A, B) Behavioral reactivity was quantified as the change in movement from baseline to infusion period. In Unpaired subjects, the average behavioral reactivity of nose (left) or forepaw (right) …

Figure 4—source data 1

Normalized nose and paw movements to intraoral sucrose before and after CTA formation and associate dopamine responses.

https://cdn.elifesciences.org/articles/103260/elife-103260-fig4-data1-v1.xlsx
Figure 5 with 1 supplement
Sucrose exposure under extinction conditions ameliorates conditioned taste aversion (CTA)’s suppression of phasic dopamine responses to intraoral sucrose.

(A) Schematic of the CTA paradigm consisting of a ingle-pairing of lithium chloride (LiCl) or saline pairing to sucrose followed by five consecutive sessions intraoral sucrose not subject to …

Figure 5—source data 1

Quantified VTADA activity responses to intraoral sucrose across CTA extinction.

https://cdn.elifesciences.org/articles/103260/elife-103260-fig5-data1-v1.xlsx
Figure 5—figure supplement 1
VTA recording placements from Delayed-test conditioned taste aversion (CTA) experiment.

The fiber optic implant locations in the VTA were verified via post-experimental histological reconstruction. Measurement values denote anterior–posterior coronal plane in relation to Bregma. …

Suppressed dopamine responses to sucrose predict conditioned taste avoidance.

(A) Each Extinction session was followed by a 2-hour Two-Bottle Preference test with access to both sucrose and water. Sucrose preference scores were calculated as the percent of sucrose solution …

Figure 6—source data 1

Sucrose preference scores and average VTADA activity responses to sucrose across CTA extinction.

https://cdn.elifesciences.org/articles/103260/elife-103260-fig6-data1-v1.xlsx
Figure 7 with 1 supplement
Delayed testing after sucrose pairing to lithium chloride (LiCl)-induced malaise suppresses dopamine response to sucrose.

(A) Schematic of the Delayed-test conditioned taste aversion (CTA) paradigm. CTA training as in Figure 3 was conducted. To match the timeline of Single-pairing CTA with Extinction, rats had five …

Figure 7—source data 1

Quantified VTADA activity to intraoral sucrose across the Delayed-test CTA paradigm.

https://cdn.elifesciences.org/articles/103260/elife-103260-fig7-data1-v1.xlsx
Figure 7—figure supplement 1
VTA recording placements from Single-pairing conditioned taste aversion (CTA) with Extinction experiment.

The fiber optic implant locations in the VTA were verified via post-experimental histological reconstruction. Measurement values denote anterior–posterior coronal plane in relation to Bregma. …

Figure 8 with 1 supplement
Phasic dopamine responses to intraoral sucrose scale to the strength of the conditioned taste aversion (CTA).

(A) Schematic of the Repeated-pairing CTA paradigm. The 3-day CTA conditioning process (as in Figure 3) was repeated three times (C1–C3). Following conditioning, subjects received eight daily …

Figure 8—source data 1

Quantified VTADA activity to intraoral sucrose across repeated pairings.

https://cdn.elifesciences.org/articles/103260/elife-103260-fig8-data1-v1.xlsx
Figure 8—source data 2

Quantified VTADA activity to intraoral sucrose across repeated extinction sessions.

https://cdn.elifesciences.org/articles/103260/elife-103260-fig8-data2-v1.zip
Figure 8—source data 3

Quantified averaged VTADA activity to intraoral sucrose across repeated parings and extinction sessions.

https://cdn.elifesciences.org/articles/103260/elife-103260-fig8-data3-v1.xlsx
Figure 8—source data 4

Data for ROC analyses across conditioning and extinction sessions.

https://cdn.elifesciences.org/articles/103260/elife-103260-fig8-data4-v1.xlsx
Figure 8—figure supplement 1
VTA recording placements from Repeated-pairing conditioned taste aversion (CTA) with Extinction experiment.

The fiber optic implant locations in the VTA were verified via post-experimental histological reconstruction. Measurement values denote anterior–posterior coronal plane in relation to Bregma. …

Intraoral sucrose-driven dopamine responses are negatively correlated to behavioral reactivity and predict sucrose preference.

(A) Head movement to intraoral sucrose averaged across trials. Top: Unpaired rats showed comparable average change in head movement behavioral reactivity across testing sessions. Bottom: Paired …

Figure 9—source data 1

Normalized head movement to intraoral infusions across repeated pairings and extinction sessions and associated VTADA responses and sucrose preference scores.

https://cdn.elifesciences.org/articles/103260/elife-103260-fig9-data1-v1.xlsx
Author response image 1
Author response image 2
Author response image 3
Author response image 4

Tables

Author response table 1
Fig.StatisticCombined ConditionsUnpairedPaired
4CR^(2)0.260.100.29
P value0.0009 (****)0.20580.0123 (*)
Best Fit EquationY=-0.025^(**)X+0.35Y=-0.017**X+0.51Y=-0.024^(***)X+0.26
4DR^(2)0.220.0130.31
P value0.0026 (***)0.650.0093 (**)
Best Fit EquationY=-0.021^(**)X+0.33Y=-
0.0047^(**)X+0.58
Y=-0.025^(**)X+0.23
4GR^(2)0.480.530.55
P value0.0002(****)0.016^(**)0.0025 (***)
Best Fit EquationY=-0.057^(**)X-0.36Y=-0.053^(**)X-0.097Y=-0.057^(***)X-0.52
4HR^(2)0.510.530.54
P value<0.0001 (****)0.017 (*){: 0.0026^(******)
Best Fit EquationY=-0.044^(**)X-0.53Y=-0.040***X-0.25Y=-0.044^(***)X-0.65
6BR^(2)0.380.0480.46
P value<0.0001 (****)0.21<0.0001 (****)
Best Fit EquationY=0.33^(***)X+0.61Y=0.037**X+0.86Y=0.46^(**)X+0.53
9BR^(2)0.438.4e-0050.33
P value<0.0001 (****)0.95<0.0001 (****)
Best Fit EquationY=-
0.045^(***)X+0.0036
Y=0.00063^(**)X+0.7
1
Y=-0.033^(***)X-0.11
9CR^(2)0.590.150.36
P value< 0.0001 **** ^("a ")0.0034 (***)< 0.0001 (****)
Best Fit EquationY=0.48**X+0.53Y=0.088^(**)X+0.86Y=0.44^(**)X+0.48

Additional files

Download links