Male spontaneously hypertensive rats demonstrate reduced goal-directed control and difficulty updating previous learning

Instrumental behaviour can be classified as goal-directed or habitual depending on how readily responding adapts when changes are made to the response-outcome (R-O) contingency or to the value of an earned outcome. Performance of goal-directed behaviour changes to reflect modifications in the response-outcome contingency or outcome value, while habitual behaviour is not sensitive to these changes and is instead thought to rely on stimulus–response (S-R) processes (Adams, 1982, Adams and Dickinson, 1981, Dickinson et al., 1983). Because goal-directed behaviours require retrieval of specific R-O associations and evaluation of the current value of the outcome of responding, such behaviours are considered to be more cognitively demanding than the execution of a well-learned habit (Bouton, 2021, Corbit, 2018, Haith and Krakauer, 2018, Watson et al., 2022). Habits develop when a response is repeatedly and consistently successful, allowing efficient and automatic execution of the response while freeing attention and cognitive resources to be devoted to novel behaviours and events in the environment (Bouton, 2021, Watson et al., 2022) and thus are adaptive in some circumstances. Nonetheless, habits are resistant to change which may be problematic when the needs of the individual or environmental conditions change. Thus, it is important to understand the factors that promote habitual control.

Increasing cognitive demand has been shown to promote habitual behaviour in tasks with human participants. Examples include adding time constraints, a secondary task, or acute stress while participants perform the response of interest (Aarts and Dijksterhuis, 2000, Haith and Krakauer, 2018, Hardwick et al., 2019, Hartogsveld et al., 2020, Schwabe and Wolf, 2010, Seabrooke et al., 2019b, Watson et al., 2018, Watson et al., 2022). However, while some studies have demonstrated deficits in outcome devaluation following acute stress (Braun and Hauber, 2013, Dougherty et al., 2024), practically, it has been difficult to capture the concept of cognitive burden in rat subjects, and thus difficult to assess whether this results in diminished goal-directed control.

As a proxy for cognitive load, the present study explored the impact that cognitive deficits may have on instrumental behavioural control by utilizing the spontaneously hypertensive rat (SHR) strain which has been used as a model for attention-deficit/hyperactivity disorder (ADHD; (CDC, 2022, Kim et al., 2024, Natsheh and Shiflett, 2018, Sagvolden, 2000, Sagvolden et al., 2009) or at least components of it (Meneses et al., 2011, Natsheh et al., 2021, Sanabria and Killeen, 2008). Despite the fact that there is debate regarding the validity of the SHR rat as a model of ADHD (Alsop, 2007, Bull et al., 2000, van den Bergh et al., 2006), the goal of the present study is not to argue whether SHRs are an appropriate model for ADHD, but to instead to utilize their well-documented cognitive deficits, including those in attention and response inhibition, to understand how such deficits impact the balance between goal-directed and habitual behavioural control.

Prior studies have investigated the performance of SHR rats in behavioural control tasks, though with mixed results. While Gauthier et al. (2014) reported a reduction in habitual control in SHRs using an outcome devaluation task, a number of findings have reported a deficit in sensitivity to outcome devaluation and contingency degradation (Natsheh and Shiflett, 2015, Natsheh and Shiflett, 2018). Although deficits in goal-directed control are often used to infer habitual control, the following series of tasks was designed to also investigate the extent to which SHRs rely on S-R learning, thought to underly habits, beyond merely demonstrating failures of goal-directed control to achieve a more nuanced understanding of the behavioural control profile of SHRs and provide more direct evidence of a reliance on response habits.

Rats were first tested in an instrumental devaluation task to investigate SHRs’ ability to flexibly adapt instrumental performance when the value of the earned outcome abruptly changed. Second, an omission task was used to assess the rats’ ability to adapt to an altered instrumental contingency and inhibit responding (Yin et al., 2006). Together, these tasks are hallmark assessments of goal-directed control (Balleine & Dickinson, 1998). We also used a Pavlovian devaluation task to investigate whether SHRs had different sensitivity to devaluation when the task involved learning about the relationship between stimuli and rewards. Finally, we examined SHRs’ ability to inhibit prior learning about a conditional stimulus (CS). Based on previous studies, it was hypothesized that SHRs would demonstrate reduced sensitivity to devaluation and omission and that if they instead rely more heavily on S-R learning, stimulus guided responding may be relatively intact. Through this combination of tasks, we aimed to better understand how cognitive impairments bias the behavioural strategies used to solve tasks and to characterize whether SHRs rely on S-R processes.

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