Punishment insensitivity in humans is due to failures in instrumental contingency learning

Abstract

Punishment maximises the probability of our individual survival by reducing behaviours that cause us harm, and also sustains trust and fairness in groups essential for social cohesion. However, some individuals are more sensitive to punishment than others and these differences in punishment sensitivity have been linked to a variety of decision-making deficits and psychopathologies. The mechanisms for why individuals differ in punishment sensitivity are poorly understood, although recent studies of conditioned punishment in rodents highlight a key role for punishment contingency detection (Jean-Richard-Dit-Bressel et al., 2019). Here, we applied a novel ‘Planets and Pirates’ conditioned punishment task in humans, allowing us to identify the mechanisms for why individuals differ in their sensitivity to punishment. We show that punishment sensitivity is bimodally distributed in a large sample of normal participants. Sensitive and insensitive individuals equally liked reward and showed similar rates of reward-seeking. They also equally disliked punishment and did not differ in their valuation of cues that signalled punishment. However, sensitive and insensitive individuals differed profoundly in their capacity to detect and learn volitional control over aversive outcomes. Punishment insensitive individuals did not learn the instrumental contingencies, so they could not withhold behaviour that caused punishment and could not generate appropriately selective behaviours to prevent impending punishment. These differences in punishment sensitivity could not be explained by individual differences in behavioural inhibition, impulsivity, or anxiety. This bimodal punishment sensitivity and these deficits in instrumental contingency learning are identical to those dictating punishment sensitivity in non-human animals, suggesting that they are general properties of aversive learning and decision-making.

Linking drug and food addiction via compulsive appetite

“…Accordingly, when tested under a PR schedule (an increasing workload paradigm not involving pain), rats with LgA and ShA histories worked more to obtain SCM (Figure 1b). Because the enhanced responding for SCM was apparent against at least two ‘cost’ measures (foot‐shock and increasing workload), these effects could also reflect insensitivity to punishment contingency (Jean‐Richard‐Dit‐Bressel et al, 2019; Jean‐Richard‐Dit‐Bressel et al, 2021) and/or the development of habitual behaviour (Everitt et al, 2018).…”

Learning of probabilistic punishment as a model of anxiety produces changes in action but not punishment encoding in the dmPFC and VTA

“…This finding suggests that action encoding by the dmPFC and VTA can serve as a locus for punishment contingency learning during reward-guided behavior. This is an important observation because behavioral studies have shown that adaptation to reward and punishment is mostly associated with the learning of safe and/or dangerous contingencies rather than arousal from punishment or reward (Jean-Richard-Dit-Bressel, Lee, et al, 2021; Jean-Richard-dit-Bressel et al, 2019). The neural mechanisms which support reward-punishment contingency learning are thought to be diverse (McNaughton & Corr, 2004) with a recent study providing direct neural data for such processes (Jean-Richard-Dit-Bressel, Tran, et al, 2021).…”

“…This is an important observation because behavioral studies have shown that adaptation to reward and punishment is mostly associated with the learning of safe and/or dangerous contingencies rather than arousal from punishment or reward (Jean-Richard-Dit-Bressel, Lee, et al, 2021; Jean-Richard-dit-Bressel et al, 2019). The neural mechanisms which support reward-punishment contingency learning are thought to be diverse (McNaughton & Corr, 2004) with a recent study providing direct neural data for such processes (Jean-Richard-Dit-Bressel, Tran, et al, 2021). Our findings in the dmPFC and VTA implicate these regions in reward-punishment contingency learning and identify action encoding as a key behavioral event involved in this form of learning.…”

“…An alternative approach to study this form of anxiety is to utilize uncertain punishment contingencies during action execution, which produce self-reported elevations in anxiety in humans and have been validated with anxiolytic treatment with benzodiazepines in rodents and non-human primates (Fischer et al, 2010; Schmitz & Grillon, 2012; Vogel et al, 1971). Recent procedures assessing reward and punishment learning simultaneously, have further indicated that learning of punishment contingencies may be critical to understanding behavioral and neuronal changes related to anxiety (Jean-Richard-Dit-Bressel, Lee, et al, 2021; Jean-Richard-dit-Bressel et al, 2019).…”

Instrumental aversion coding in the basolateral amygdala and its reversion by a benzodiazepine

“…It is worth noting sex differences using immediate punishment tend to be modest and attributable to increased propensity to fear over punishment learning in females (Chowdhury et al, 2019; Jean-Richard-Dit-Bressel et al, 2019; Liley et al, 2019; Orsini et al, 2016). Moreover, our rodent work, based largely on male rats, accurately accounts for punishment learning in female and male humans (Jean-Richard-Dit-Bressel et al, 2021).…”