Subsecond Dopamine Release in the Nucleus Accumbens Predicts Conditioned Punishment and Its Successful Avoidance

Department of Anatomy and Neurobiology, University of Maryland School of Medicine, Baltimore, Maryland 21201.
The Journal of Neuroscience : The Official Journal of the Society for Neuroscience (Impact Factor: 6.34). 10/2012; 32(42):14804-8. DOI: 10.1523/JNEUROSCI.3087-12.2012
Source: PubMed


The mesolimbic dopamine system is believed to be a pathway that processes rewarding information. While previous studies have also implicated a general role for dopamine in punishment and its avoidance, the precise nature of subsecond dopamine release during these phenomena remains unknown. Here, we used fast-scan cyclic voltammetry to investigate whether subsecond dopamine release events in the nucleus accumbens encode cues predicting the avoidance of punishment during behavior maintained in a signaled footshock avoidance procedure. In this task, rats could initiate an avoidance response by pressing a lever within a warning period, preventing footshock. Alternatively, once footshocks commenced, animals could initiate an escape response by pressing the lever, terminating footshock. This design allowed us to assess subsecond dopamine release events during the presentation of a warning signal, safety periods, and two distinct behavioral responses. We found that release consistently increased upon presentation of the warning signal in a manner that reliably predicted successful punishment avoidance. We also observed subsecond dopamine release during the safety period, as occurs following the receipt of reward. Conversely, we observed a decrease in release at the warning signal during escape responses. Because of this finding, we next assessed dopamine release in a conditioned fear model. As seen during escape responses, we observed a time-locked decrease in dopamine release upon presentation of a cue conditioned to inescapable footshock. Together, these data show that subsecond fluctuations in mesolimbic dopamine release predict when rats will successfully avoid punishment and differentially encode cues related to aversive outcomes.

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    • "Indeed, enhanced phasic DA transmission is reliably observed following unexpected reward delivery or, after conditioning, in response to cues that predict reward (40, 55, 57, 59, 62–64). Further, in congruence with electrophysiological data, reward omission or administration of an aversive stimulus results in decreased extracellular DA within the ventral striatum (65–67). "
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    • "DA was released at the time of the avoided shock and during cue presentation of successful avoidance trials. Thus, as with appetitive paradigms, DA signals adhere to the general rule of firing more or less strongly for cues and outcomes that are better or worse than expected, respectively (Oleson et al., 2012). Importantly, this signal is dependent on input from OFC (Takahashi et al., 2011). "
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    Frontiers in Systems Neuroscience 03/2014; 8:24. DOI:10.3389/fnsys.2014.00024
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    • "Over training with reward experience, this DA activation will occur not only in response to the salient primary stimuli per se, but will also occur in response to previously neutral cues in the environment that the animal has associated with these motivationally relevant outcomes (Schultz, 2013). As a consequence of DA activity, DA in the NAc induces a motivational drive, and this DA signal is modulated by past experience of reward and punishment (Oleson et al., 2012; Howe et al., 2013). In this way, mesolimbic DA has been conceptualized as a teaching signal, coding the magnitude of aversive and rewarding environmental stimuli and increasing behavioral vigor related to these salient stimuli (Peciña and Berridge, 2013). "
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