The sensory features of a food cue influence its ability to act as an incentive stimulus and evoke dopamine release in the nucleus accumbens core

Abstract

The sensory properties of a reward-paired cue (a conditioned stimulus; CS) may impact the motivational value attributed to the cue, and in turn influence the form of the conditioned response (CR) that develops. A cue with multiple sensory qualities, such as a moving lever-CS, may activate numerous neural pathways that process auditory and visual information, resulting in CRs that vary both within and between individuals. For example, CRs include approach to the lever-CS itself (rats that "sign-track"; ST), approach to the location of reward delivery (rats that "goal-track"; GT), or an "intermediate" combination of these behaviors. We found that the multimodal sensory features of the lever-CS were important to the development and expression of sign-tracking. When the lever-CS was covered, and thus could only be heard moving, STs not only continued to approach the lever location but also started to approach the food cup during the CS period. While still predictive of reward, the auditory component of the lever-CS was a much weaker conditioned reinforcer than the visible lever-CS. This plasticity in behavioral responding observed in STs closely resembled behaviors normally seen in rats classified as "intermediates." Furthermore, the ability of both the lever-CS and the reward-delivery to evoke dopamine release in the nucleus accumbens was also altered by covering the lever-dopamine signaling in STs resembled neurotransmission observed in rats that normally only GT. These data suggest that while the visible lever-CS was attractive, wanted, and had incentive value for STs, when presented in isolation, the auditory component of the cue was simply predictive of reward, lacking incentive salience. Therefore, the specific sensory features of cues may differentially contribute to responding and ensure behavioral flexibility.

The ability for cocaine and cocaine-associated cues to compete for attention

“…However, in the current study we chose to use a tone DS for a couple reasons. Although STs attribute more incentive salience to a discrete localizable CS (Beckmann and Chow, 2015; Singer et al 2016), an auditory cue is an equally efficacious conditioned reinforcer in STs and GTs (Meyer et al, 2012), which we confirmed in Experiment 1 here. Therefore, we reasoned that any potential group difference in the propensity to be distracted by the cocaine cue (DS) in the present studies would presumably not be because STs attributed greater incentive salience to it, but because they might be more susceptible to attention disruptors compared to GTs because of their relatively poor attentional control (Paolone et al, 2013) and susceptibility to impulsive action (Lovic et al, 2011).…”

“…That is, if we used a cue that was approached by STs but not GTs it would not be surprising if it disrupted ongoing performance to a greater degree in STs than GTs. It is known, however, that the form of the CS is important in determining the extent to which it acquires motivational value, when a food reward is used, such that an auditory cue is a less effective incentive stimulus (Meyer et al, 2014; Beckmann et a., 2015; Singer et al, In Press). Thus, we first wanted to determine whether an auditory stimulus (a tone-CS) paired with cocaine reward acquired sufficient motivational value to motivate renewed cocaine-seeking behavior, and whether it did so equally in STs and GTs.…”

Rapid induction of dopamine sensitization in the nucleus accumbens shell induced by a single injection of cocaine

“…Following recovery from catheter implantation (~ 1 week), stereotaxic surgeries were performed for insertion of a guide cannula, as well as reference and stimulating electrodes for in vivo FSCV. As previously described [11], a guide cannula was implanted dorsal to the NAc shell (AP, +1.8; ML, ±0.8; DV, −2.5 mm relative to bregma; MD-2251, BASi) and an Ag/AgCl reference electrode was secured in the contralateral cortex (AP, −0.8; ML, ±4.0; DV, −2.0 mm relative to bregma). A bipolar stimulating electrode (AP, −5.2; ML, ±0.8 mm relative to bregma; C315G-MS303/2/SPC, Plastics One) was lowered into the VTA until electrically-evoked DA release was detected in the dorsal striatum, directly above the final recording location in the NAc.…”

“…Following recovery from surgery, experiments were conducted within a Med Associates behavioral testing chamber [11]. At the beginning of the test day, saline-loaded tubing attached to a syringe pump was threaded through the commutator, along the tether, and attached to the back-mounted i.v.…”

“…Next, a carbon fiber electrode (pre-calibrated using DA concentrations of 125 nM, 250 nM, and 1000 nM) was loaded into a micromanipulator (custom-manufactured) and lowered into the NAc shell and tested for its ability to detect both naturally occurring and electrically evoked DA release (via VTA stimulation; 60Hz/24-pulse, 60Hz/12-pulse, 60Hz/6-pulse, 30Hz/24-pulse, 30Hz/12-pulse, 30Hz/6-pulse, 20Hz/4-pulse). As previously described [11], FSCV relied upon the oxidation and reduction of the analyte of interest (i.e. DA) in response to the application of a triangular waveform (oxidative scan, −0.4 to 1.3 V; reductive scan, 1.3 V to −0.4 V; 10Hz, 400V/s).…”