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On the role of subsecond dopamine release in conditioned avoidance.

Oleson EB, Cheer JF - Front Neurosci (2013)

Bottom Line: Current neuroscientific advances are providing new perspectives into this historical literature.Due to its well-established role in reinforcement processes and behavioral control, the mesolimbic dopamine system presented itself as a logical starting point in the search for neural correlates of avoidance and escape behavior.We recently demonstrated that phasic dopamine release events are inhibited by stimuli associated with aversive events but increased by stimuli preceding the successful avoidance of the aversive event.

View Article: PubMed Central - PubMed

Affiliation: Department of Anatomy and Neurobiology, School of Medicine, University of Maryland Baltimore, MD, USA.

ABSTRACT
Using shock avoidance procedures to study conditioned behavioral responses has a rich history within the field of experimental psychology. Such experiments led to the formulation of the general concept of negative reinforcement and specific theories attempting to explain escape and avoidance behavior, or why animals choose to either terminate or prevent the presentation of an aversive event. For example, the two-factor theory of avoidance holds that cues preceding an aversive event begin to evoke conditioned fear responses, and these conditioned fear responses reinforce the instrumental avoidance response. Current neuroscientific advances are providing new perspectives into this historical literature. Due to its well-established role in reinforcement processes and behavioral control, the mesolimbic dopamine system presented itself as a logical starting point in the search for neural correlates of avoidance and escape behavior. We recently demonstrated that phasic dopamine release events are inhibited by stimuli associated with aversive events but increased by stimuli preceding the successful avoidance of the aversive event. The latter observation is inconsistent with the second component of the two-factor theory of avoidance and; therefore, led us propose a new theoretical explanation of conditioned avoidance: (1) fear is initially conditioned to the warning signal and dopamine computes this fear association as a decrease in release, (2) the warning signal, now capable of producing a negative emotional state, suppresses dopamine release and behavior, (3) over repeated trials the warning signal becomes associated with safety rather than fear; dopaminergic neurons already compute safety as an increase in release and begin to encode the warning signal as the earliest predictor of safety (4) the warning signal now promotes conditioned avoidance via dopaminergic modulation of the brain's incentive-motivational circuitry.

No MeSH data available.


Related in: MedlinePlus

Fear-conditioned stimuli freeze behavior and subsecond dopamine release events. (A,B) An otherwise neutral stimulus (trumpet) previously conditioned to inescapable footshock (lightning bolt) produces freezing behavior that extinguishes across repeated trials of conditioned stimulus (CS) presentation on fear-memory retrieval day. (C) Representative color plot (left) and corresponding dopamine concentration trace (right) show a CS-induced decrease in dopamine release. Gray represents CS duration. (D) Mean ± SEM dopamine concentration trace during presentations of the fear-conditioned CS. Originally published in Oleson et al. (2012).
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Figure 3: Fear-conditioned stimuli freeze behavior and subsecond dopamine release events. (A,B) An otherwise neutral stimulus (trumpet) previously conditioned to inescapable footshock (lightning bolt) produces freezing behavior that extinguishes across repeated trials of conditioned stimulus (CS) presentation on fear-memory retrieval day. (C) Representative color plot (left) and corresponding dopamine concentration trace (right) show a CS-induced decrease in dopamine release. Gray represents CS duration. (D) Mean ± SEM dopamine concentration trace during presentations of the fear-conditioned CS. Originally published in Oleson et al. (2012).

Mentions: As animals displayed either directed avoidance or inhibited freezing responses to warning signal presentation, it might be expected, therefore that distinct dopaminergic responses accompany these divergent behavioral reactions. In accordance with our behavioral observation, dichotomous dopaminergic responses occurred at the warning signal during avoidance and escape behavior. When animals successfully avoided footshock, dopamine release increased during warning signal presentation as would be predicted if dopamine was motivating the avoidance response. Importantly, the warning signal evoked increase in dopamine concentration reliably predicted when an animal would successfully avoid foot shock. Trial-by-trial analysis revealed that the maximal dopamine concentration time-locked to warning signal presentation sharply decreased during trials in which animals failed to avoid and was significantly lower during escape responses irrespective of the number of footshocks received. Averaging dopamine concentrations during escape trials revealed that dopamine levels not only failed to increase during presentation of the warning signal presentation, dopamine release events actually ceased at warning signal onset when the animals failed to avoid. This latter finding is somewhat reminiscent of the previously described classical psychological theory called the two-process theory of avoidance (Mowrer, 1951). The first factor of this theory posits that fear becomes conditioned to the warning signal; the second factor suggests that the conditioned fear that is evoked by the warning signal is what reinforces the instrumental avoidance response via fear reduction. To further test whether our dopamine data align with the first-factor of this theory, we measured whether dopamine release in the nucleus accumbens core is also suppressed during classical fear associations by employing a standard fear-conditioning model. In this fear-conditioned model, animals were conditioned to an auditory stimulus predicting inescapable footshock before we measured dopamine release 24 h later during repeated presentations of the cue alone (Figure 3). As was observed at the warning-signal during escape responses, the fear-associated auditory stimulus produced a decrease in dopamine concentration transients (Oleson et al., 2012), a phenomenon that appears to be exclusive to the core, as opposed to the shell, subregion of the nucleus accumbens (Badrinarayan et al., 2012). This finding supports the first factor of the two-process theory of avoidance that the warning signal can evoke conditioned fear responses, and reveals that dopamine neurons compute this conditioned fear response as a decrease in the frequency of dopamine release events. These data fail to align with the second factor of two-process theory, however, as dopamine release accompanies the presentation of the warning signal when animals successfully avoid foot shock. Rather, fear may become irrelevant during conditioned avoidance in a well-trained animal. The warning signal no longer evokes fear, and fear reduction is no longer the primary motivator of behavior. Instead of evoking a fear response, the warning signal becomes associated exclusively with a positive outcome—avoidance. At this point the warning signal motivates behavior similarly to a reward-predictive cue, by stimulating the incentive-motivational circuitry of the brain.


On the role of subsecond dopamine release in conditioned avoidance.

Oleson EB, Cheer JF - Front Neurosci (2013)

Fear-conditioned stimuli freeze behavior and subsecond dopamine release events. (A,B) An otherwise neutral stimulus (trumpet) previously conditioned to inescapable footshock (lightning bolt) produces freezing behavior that extinguishes across repeated trials of conditioned stimulus (CS) presentation on fear-memory retrieval day. (C) Representative color plot (left) and corresponding dopamine concentration trace (right) show a CS-induced decrease in dopamine release. Gray represents CS duration. (D) Mean ± SEM dopamine concentration trace during presentations of the fear-conditioned CS. Originally published in Oleson et al. (2012).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3675318&req=5

Figure 3: Fear-conditioned stimuli freeze behavior and subsecond dopamine release events. (A,B) An otherwise neutral stimulus (trumpet) previously conditioned to inescapable footshock (lightning bolt) produces freezing behavior that extinguishes across repeated trials of conditioned stimulus (CS) presentation on fear-memory retrieval day. (C) Representative color plot (left) and corresponding dopamine concentration trace (right) show a CS-induced decrease in dopamine release. Gray represents CS duration. (D) Mean ± SEM dopamine concentration trace during presentations of the fear-conditioned CS. Originally published in Oleson et al. (2012).
Mentions: As animals displayed either directed avoidance or inhibited freezing responses to warning signal presentation, it might be expected, therefore that distinct dopaminergic responses accompany these divergent behavioral reactions. In accordance with our behavioral observation, dichotomous dopaminergic responses occurred at the warning signal during avoidance and escape behavior. When animals successfully avoided footshock, dopamine release increased during warning signal presentation as would be predicted if dopamine was motivating the avoidance response. Importantly, the warning signal evoked increase in dopamine concentration reliably predicted when an animal would successfully avoid foot shock. Trial-by-trial analysis revealed that the maximal dopamine concentration time-locked to warning signal presentation sharply decreased during trials in which animals failed to avoid and was significantly lower during escape responses irrespective of the number of footshocks received. Averaging dopamine concentrations during escape trials revealed that dopamine levels not only failed to increase during presentation of the warning signal presentation, dopamine release events actually ceased at warning signal onset when the animals failed to avoid. This latter finding is somewhat reminiscent of the previously described classical psychological theory called the two-process theory of avoidance (Mowrer, 1951). The first factor of this theory posits that fear becomes conditioned to the warning signal; the second factor suggests that the conditioned fear that is evoked by the warning signal is what reinforces the instrumental avoidance response via fear reduction. To further test whether our dopamine data align with the first-factor of this theory, we measured whether dopamine release in the nucleus accumbens core is also suppressed during classical fear associations by employing a standard fear-conditioning model. In this fear-conditioned model, animals were conditioned to an auditory stimulus predicting inescapable footshock before we measured dopamine release 24 h later during repeated presentations of the cue alone (Figure 3). As was observed at the warning-signal during escape responses, the fear-associated auditory stimulus produced a decrease in dopamine concentration transients (Oleson et al., 2012), a phenomenon that appears to be exclusive to the core, as opposed to the shell, subregion of the nucleus accumbens (Badrinarayan et al., 2012). This finding supports the first factor of the two-process theory of avoidance that the warning signal can evoke conditioned fear responses, and reveals that dopamine neurons compute this conditioned fear response as a decrease in the frequency of dopamine release events. These data fail to align with the second factor of two-process theory, however, as dopamine release accompanies the presentation of the warning signal when animals successfully avoid foot shock. Rather, fear may become irrelevant during conditioned avoidance in a well-trained animal. The warning signal no longer evokes fear, and fear reduction is no longer the primary motivator of behavior. Instead of evoking a fear response, the warning signal becomes associated exclusively with a positive outcome—avoidance. At this point the warning signal motivates behavior similarly to a reward-predictive cue, by stimulating the incentive-motivational circuitry of the brain.

Bottom Line: Current neuroscientific advances are providing new perspectives into this historical literature.Due to its well-established role in reinforcement processes and behavioral control, the mesolimbic dopamine system presented itself as a logical starting point in the search for neural correlates of avoidance and escape behavior.We recently demonstrated that phasic dopamine release events are inhibited by stimuli associated with aversive events but increased by stimuli preceding the successful avoidance of the aversive event.

View Article: PubMed Central - PubMed

Affiliation: Department of Anatomy and Neurobiology, School of Medicine, University of Maryland Baltimore, MD, USA.

ABSTRACT
Using shock avoidance procedures to study conditioned behavioral responses has a rich history within the field of experimental psychology. Such experiments led to the formulation of the general concept of negative reinforcement and specific theories attempting to explain escape and avoidance behavior, or why animals choose to either terminate or prevent the presentation of an aversive event. For example, the two-factor theory of avoidance holds that cues preceding an aversive event begin to evoke conditioned fear responses, and these conditioned fear responses reinforce the instrumental avoidance response. Current neuroscientific advances are providing new perspectives into this historical literature. Due to its well-established role in reinforcement processes and behavioral control, the mesolimbic dopamine system presented itself as a logical starting point in the search for neural correlates of avoidance and escape behavior. We recently demonstrated that phasic dopamine release events are inhibited by stimuli associated with aversive events but increased by stimuli preceding the successful avoidance of the aversive event. The latter observation is inconsistent with the second component of the two-factor theory of avoidance and; therefore, led us propose a new theoretical explanation of conditioned avoidance: (1) fear is initially conditioned to the warning signal and dopamine computes this fear association as a decrease in release, (2) the warning signal, now capable of producing a negative emotional state, suppresses dopamine release and behavior, (3) over repeated trials the warning signal becomes associated with safety rather than fear; dopaminergic neurons already compute safety as an increase in release and begin to encode the warning signal as the earliest predictor of safety (4) the warning signal now promotes conditioned avoidance via dopaminergic modulation of the brain's incentive-motivational circuitry.

No MeSH data available.


Related in: MedlinePlus